Nanoparticle- and Microparticle-Based Vaccines against Orbiviruses of Veterinary Importance.
Abstract: Bluetongue virus (BTV) and African horse sickness virus (AHSV) are widespread arboviruses that cause important economic losses in the livestock and equine industries, respectively. In addition to these, another arthropod-transmitted orbivirus known as epizootic hemorrhagic disease virus (EHDV) entails a major threat as there is a conducive landscape that nurtures its emergence in non-endemic countries. To date, only vaccinations with live attenuated or inactivated vaccines permit the control of these three viral diseases, although important drawbacks, e.g., low safety profile and effectiveness, and lack of DIVA (differentiation of infected from vaccinated animals) properties, constrain their usage as prophylactic measures. Moreover, a substantial number of serotypes of BTV, AHSV and EHDV have been described, with poor induction of cross-protective immune responses among serotypes. In the context of next-generation vaccine development, antigen delivery systems based on nano- or microparticles have gathered significant attention during the last few decades. A diversity of technologies, such as virus-like particles or self-assembled protein complexes, have been implemented for vaccine design against these viruses. In this work, we offer a comprehensive review of the nano- and microparticulated vaccine candidates against these three relevant orbiviruses. Additionally, we also review an innovative technology for antigen delivery based on the avian reovirus nonstructural protein muNS and we explore the prospective functionality of the nonstructural protein NS1 nanotubules as a BTV-based delivery platform.
Publication Date: 2022-07-14 PubMed ID: 35891288PubMed Central: PMC9319458DOI: 10.3390/vaccines10071124Google Scholar: Lookup
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Summary
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The research article is about the use of nanoparticle- and microparticle-based vaccines to combat Orbiviruses like Bluetongue virus (BTV) and African horse sickness virus (AHSV) that affect livestock and equine industries respectively and are a significant economic burden. Detailed exploration is found on vaccine candidates and innovative technology for antigen delivery against these viruses.
Understanding Orbiviruses and their Impact
- The study centers on orbiviruses like BTV, AHSV, and EHDV. These arboviruses are wide-spread and cause important economic damages especially in livestock and equine industries.
- The EHDV, like BTV and AHSV, is another extensively transmitted orbivirus that is becoming a major threat in non-endemic countries where the landscape can support its spread.
Drawbacks of Current Vaccination Methods
- Today, only live attenuated or inactivated vaccines are used to control orbivrus diseases.
- However, these vaccines have significant limitations including a low safety profile, limited effectiveness, and lack of DIVA properties (the ability to differentiate infected from vaccinated animals).
- These vaccines are also insufficient against a significant number of serotypes of BTV, AHSV, and EHDV for inducing a cross-protective immune response.
New Ways of Vaccine Development
- Given the limitations of current vaccines, this study explores the potential of next-generation vaccine development.
- Nano- or microparticle-based vaccination methods have received substantial interest and could provide a solution.
- Diverse technologies, such as virus-like particles or self-assembled protein complexes, have been implemented for vaccine design against orbiviruses.
Nano- and Microparticle Based Vaccines
- The researchers provide an in-depth review of the different nano- and microparticle-based vaccine candidates against the mentioned orbiviruses.
- An innovative technology for antigen delivery based on the avian reovirus nonstructural protein muNS is also examined.
- Furthermore, the potential use of nanotubules by the nonstructural protein NS1 as a BTV-based delivery platform is also explored in the study.
Cite This Article
APA
Jiménez-Cabello L, Utrilla-Trigo S, Barreiro-Piñeiro N, Pose-Boirazian T, Martínez-Costas J, Marín-López A, Ortego J.
(2022).
Nanoparticle- and Microparticle-Based Vaccines against Orbiviruses of Veterinary Importance.
Vaccines (Basel), 10(7).
https://doi.org/10.3390/vaccines10071124 Publication
Researcher Affiliations
- Centro de Investigación en Sanidad Animal (CISA-INIA/CSIC), 28130 Madrid, Spain.
- Centro Singular de Investigación en Química Biológica y Materiales Moleculares (CIQUS), Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain.
- Centro de Investigación en Sanidad Animal (CISA-INIA/CSIC), 28130 Madrid, Spain.
- Centro Singular de Investigación en Química Biológica y Materiales Moleculares (CIQUS), Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain.
- Centro Singular de Investigación en Química Biológica y Materiales Moleculares (CIQUS), Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain.
- Centro Singular de Investigación en Química Biológica y Materiales Moleculares (CIQUS), Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain.
- Section of Infectious Diseases, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06519, USA.
- Centro de Investigación en Sanidad Animal (CISA-INIA/CSIC), 28130 Madrid, Spain.
Grant Funding
- UL1 TR001863 / NCATS NIH HHS
- PID2020-112992RR-I00 / Ministerio de ciencia e innovación
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 253 references
- Metcalf P, Cyrklaff M, Adrian M. The Three-Dimensional Structure of Reovirus Obtained by Cryo-Electron Microscopy. EMBO J. 1991;10:3129–3136.
- Attoui H, Jaafar FM, de Micco P, de Lamballerie X. Coltiviruses and Seadornaviruses in North America, Europe, and Asia. Emerg. Infect. Dis. 2005;11:1673–1679.
- Schwartz-Cornil I, Mertens PPC, Contreras V, Hemati B, Pascale F, Bréard E, Mellor PS, MacLachlan NJ, Zientara S. Bluetongue Virus: Virology, Pathogenesis and Immunity. Vet. Res. 2008;39:46.
- Carpenter S, Mellor PS, Fall AG, Garros C, Venter GJ. African Horse Sickness Virus: History, Transmission, and Current Status. Annu. Rev. Entomol. 2017;62:343–358.
- Maclachlan NJ. Bluetongue: History, Global Epidemiology, and Pathogenesis. Prev. Vet. Med. 2011;102:107–111.
- Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, Armah G, Bines JE, Brewer TG, Colombara DV. Rotavirus Vaccination and the Global Burden of Rotavirus Diarrhea Among Children Younger Than 5 Years. JAMA Pediatr. 2018;172:958–965.
- Mertens PP, Sangar DV. Analysis of the Terminal Sequences of the Genome Segments of Four Orbiviruses. Prog. Clin. Biol. Res. 1985;178:371–387.
- Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Ziéntara S, Mertens PP, Stuart DI. The Atomic Structure of the Bluetongue Virus Core. Nature 1998;395:470–478.
- Huismans H, Erasmus BJ. Identification of the Serotype-Specific and Group-Specific Antigens of Bluetongue Virus. Onderstepoort J. Vet. Res. 1981;48:51–58.
- Hassan SH, Wirblich C, Forzan M, Roy P. Expression and Functional Characterization of Bluetongue Virus VP5 Protein: Role in Cellular Permeabilization. J. Virol. 2001;75:8356–8367.
- Boyce M, Wehrfritz J, Noad R, Roy P. Purified Recombinant Bluetongue Virus VP1 Exhibits RNA Replicase Activity. J. Virol. 2004;78:3994–4002.
- Ramadevi N, Burroughs NJ, Mertens PPC, Jones IM, Roy P. Capping and Methylation of MRNA by Purified Recombinant VP4 Protein of Bluetongue Virus. Proc. Natl. Acad. Sci. USA 1998;95:13537–13542.
- Stäuber N, Martinez-Costas J, Sutton G, Monastyrskaya K, Roy P. Bluetongue Virus VP6 Protein Binds ATP and Exhibits an RNA-Dependent ATPase Function and a Helicase Activity That Catalyze the Unwinding of Double-Stranded RNA Substrates. J. Virol. 1997;71:7220–7226.
- Alonso C, Utrilla-Trigo S, Calvo-Pinilla E, Jiménez-Cabello L, Ortego J, Nogales A. Inhibition of Orbivirus Replication by Aurintricarboxylic Acid. Int. J. Mol. Sci. 2020;21:7294.
- Mohd Jaafar F, Monsion B, Belhouchet M, Mertens PPC, Attoui H. Inhibition of Orbivirus Replication by Fluvastatin and Identification of the Key Elements of the Mevalonate Pathway Involved. Viruses 2021;13:1437.
- John L, Vernersson C, Kwon H, Elling U, Penninger JM, Mirazimi A. Redirecting Imipramine against Bluetongue Virus Infection: Insights from a Genome-Wide Haploid Screening Study. Pathogens 2022;11:602.
- Jiménez-Cabello L, Utrilla-Trigo S, Calvo-Pinilla E, Moreno S, Nogales A, Ortego J, Marín-López A. Viral Vector Vaccines against Bluetongue Virus. Microorganisms 2020;9:42.
- Van Rijn PA. Prospects of Next-Generation Vaccines for Bluetongue. Front. Vet. Sci. 2019;6:407.
- Calvo-Pinilla E, Marín-López A, Utrilla-Trigo S, Jiménez-Cabello L, Ortego J. Reverse Genetics Approaches: A Novel Strategy for African Horse Sickness Virus Vaccine Design. Curr. Opin. Virol. 2020;44:49–56.
- Savini G, Afonso A, Mellor P, Aradaib I, Yadin H, Sanaa M, Wilson W, Monaco F, Domingo M. Epizootic Heamorragic Disease. Res. Vet. Sci. 2011;91:1–17.
- Qiao C, Liu J, Yang J, Li Y, Weng J, Shao Y, Zhang X. Enhanced Non-Inflammasome Mediated Immune Responses by Mannosylated Zwitterionic-Based Cationic Liposomes for HIV DNA Vaccines. Biomaterials 2016;85:1–17.
- Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Pérez Marc G, Moreira ED, Zerbini C. Safety and Efficacy of the BNT162b2 MRNA COVID-19 Vaccine. N Engl. J. Med. 2020;383:2603–2615.
- Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB. Efficacy and Safety of the MRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med. 2021;384:403–416.
- Wui SR, Kim KS, Ryu JI, Ko A, Do HTT, Lee YJ, Kim HJ, Lim SJ, Park SA, Cho YJ. Efficient Induction of Cell-Mediated Immunity to Varicella-Zoster Virus Glycoprotein E Co-Lyophilized with a Cationic Liposome-Based Adjuvant in Mice. Vaccine 2019;37:2131–2141.
- Rosenkrands I, Vingsbo-Lundberg C, Bundgaard TJ, Lindenstrøm T, Enouf V, van der Werf S, Andersen P, Agger EM. Enhanced Humoral and Cell-Mediated Immune Responses after Immunization with Trivalent Influenza Vaccine Adjuvanted with Cationic Liposomes. Vaccine 2011;29:6283–6291.
- Senchi K, Matsunaga S, Hasegawa H, Kimura H, Ryo A. Development of Oligomannose-Coated Liposome-Based Nasal Vaccine against Human Parainfluenza Virus Type 3. Front. Microbiol. 2013;4:346.
- Tanaka Y, Taneichi M, Kasai M, Kakiuchi T, Uchida T. Liposome-Coupled Antigens Are Internalized by Antigen-Presenting Cells via Pinocytosis and Cross-Presented to CD8 T Cells. PLoS ONE 2010;5:e15225.
- Wei L, Zhao T, Zhang J, Mao Q, Gong G, Sun Y, Chen Y, Wang M, Tan D, Gong Z. Efficacy and Safety of a Nanoparticle Therapeutic Vaccine in Patients with Chronic Hepatitis B: A Randomized Clinical Trial. Hepatology 2022;75:182–195.
- Storm G, Crommelin DJA. Liposomes: Quo Vadis?. Pharm. Sci. Technol. Today 1998;1:19–31.
- Cappellano G, Abreu H, Casale C, Dianzani U, Chiocchetti A. Nano-Microparticle Platforms in Developing Next-Generation Vaccines. Vaccines 2021;9:606.
- Ho HM, Huang CY, Cheng YJ, Shen KY, Tzeng TT, Liu SJ, Chen HW, Huang CH, Huang MH. Assessment of Adjuvantation Strategy of Lipid Squalene Nanoparticles for Enhancing the Immunogenicity of a SARS-CoV-2 Spike Subunit Protein against COVID-19. Int. J. Pharm. 2021;607:121024.
- Sia ZR, Miller MS, Lovell JF. Engineered Nanoparticle Applications for Recombinant Influenza Vaccines. Mol. Pharm. 2021;18:576–592.
- Yang Y, Sun Z, Li H, Tian J, Chen M, Liu T. Preparation and Immune Effect of HEV ORF2 P206@PLGA Nanoparticles. Nanomaterials 2022;12:595.
- Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Préat V. PLGA-Based Nanoparticles: An Overview of Biomedical Applications. J. Control. Release 2012;161:505–522.
- Chaikhumwang P, Madapong A, Saeng-Chuto K, Nilubol D, Tantituvanont A. Intranasal Delivery of Inactivated PRRSV Loaded Cationic Nanoparticles Coupled with Enterotoxin Subunit B Induces PRRSV-Specific Immune Responses in Pigs. Sci. Rep. 2022;12:3725.
- Piperno A, Sciortino MT, Giusto E, Montesi M, Panseri S, Scala A. Recent Advances and Challenges in Gene Delivery Mediated by Polyester-Based Nanoparticles. Int. J. Nanomed. 2021;16:5981–6002.
- Roopngam P, Liu K, Mei L, Zheng Y, Zhu X, Tsai HI, Huang L. Hepatitis C Virus E2 Protein Encapsulation into Poly d, l-Lactic-Co-Glycolide Microspheres Could Induce Mice Cytotoxic T-Cell Response. Int. J. Nanomed. 2016;11:5361–5370.
- Huang S, Li IH, Hong P, Yeh M. Evaluation of Protective Efficacy Using a Nonstructural Protein NS1 in DNA Vaccine-Loaded Microspheres against Dengue 2 Virus. Int. J. Nanomed. 2013;8:3161–3169.
- Bolhassani A, Javanzad S, Saleh T, Hashemi M, Aghasadeghi MR, Sadat SM. Polymeric Nanoparticles. Hum. Vaccin. Immunother. 2014;10:321–332.
- Nguyen QT, Kwak C, Lee WS, Kim J, Jeong J, Sung MH, Yang J, Poo H. Poly-γ-Glutamic Acid Complexed With Alum Induces Cross-Protective Immunity of Pandemic H1N1 Vaccine. Front. Immunol. 2019;10:1604.
- Akagi T, Watanabe K, Kim H, Akashi M. Stabilization of Polyion Complex Nanoparticles Composed of Poly(Amino Acid) Using Hydrophobic Interactions. Langmuir 2010;26:2406–2413.
- Peleteiro M, Presas E, González-Aramundiz JV, Sánchez-Correa B, Simón-Vázquez R, Csaba N, Alonso MJ, González-Fernández Á. Polymeric Nanocapsules for Vaccine Delivery: Influence of the Polymeric Shell on the Interaction With the Immune System. Front. Immunol. 2018;9:791.
- Gao X, Liu N, Wang Z, Gao J, Zhang H, Li M, Du Y, Gao X, Zheng A. Development and Optimization of Chitosan Nanoparticle-Based Intranasal Vaccine Carrier. Molecules 2021;27:204.
- Niculescu AG, Grumezescu AM. Applications of Chitosan-Alginate-Based Nanoparticles—An Up-to-Date Review. Nanomaterials 2022;12:186.
- Nguyen HV, Campbell K, Painter GF, Young SL, Walker GF. Nanoparticle System Based on Amino-Dextran as a Drug Delivery Vehicle: Immune-Stimulatory CpG-Oligonucleotide Loading and Delivery. Pharmaceutics 2020;12:1150.
- Liu Q, Zheng X, Zhang C, Shao X, Zhang X, Zhang Q, Jiang X. Conjugating Influenza a (H1N1) Antigen to n-Trimethylaminoethylmethacrylate Chitosan Nanoparticles Improves the Immunogenicity of the Antigen after Nasal Administration. J. Med. Virol. 2015;87:1807–1815.
- Singh M, Chakrapani A, O’Hagan D. Nanoparticles and Microparticles as Vaccine-Delivery Systems. Expert. Rev. Vaccines 2007;6:797–808.
- Chowdhury S, Toth I, Stephenson RJ. Dendrimers in Vaccine Delivery: Recent Progress and Advances. Biomaterials 2022;280:121303.
- Chahal JS, Khan OF, Cooper CL, McPartlan JS, Tsosie JK, Tilley LD, Sidik SM, Lourido S, Langer R, Bavari S. Dendrimer-RNA Nanoparticles Generate Protective Immunity against Lethal Ebola, H1N1 Influenza, and Toxoplasma Gondii Challenges with a Single Dose. Proc. Natl. Acad. Sci. USA 2016;113:E4133–E4142.
- Cañas-Arranz R, de León P, Defaus S, Torres E, Forner M, Bustos MJ, Andreu D, Blanco E, Sobrino F. Immunogenicity of Foot-and-Mouth Disease Virus Dendrimer Peptides: Need for a T-Cell Epitope and Ability to Elicit Heterotypic Responses. Molecules 2021;26:4714.
- Bahadoran A, Moeini H, Bejo MH, Hussein MZ, Omar AR. Development of Tat-Conjugated Dendrimer for Transdermal DNA Vaccine Delivery. J. Pharm. Pharm. Sci. 2016;19:325–338.
- Pati R, Shevtsov M, Sonawane A. Nanoparticle Vaccines Against Infectious Diseases. Front. Immunol. 2018;9:2224.
- Tao W, Hurst BL, Shakya AK, Uddin MJ, Ingrole RSJ, Hernandez-Sanabria M, Arya RP, Bimler L, Paust S, Tarbet EB. Consensus M2e Peptide Conjugated to Gold Nanoparticles Confers Protection against H1N1, H3N2 and H5N1 Influenza A Viruses. Antivir. Res. 2017;141:62–72.
- Mateu Ferrando R, Lay L, Polito L. Gold Nanoparticle-Based Platforms for Vaccine Development. Drug Discov. Today Technol. 2020;38:57–67.
- Joyce MG, Chen WH, Sankhala RS, Hajduczki A, Thomas PV, Choe M, Martinez EJ, Chang WC, Peterson CE, Morrison EB. SARS-CoV-2 Ferritin Nanoparticle Vaccines Elicit Broad SARS Coronavirus Immunogenicity. Cell Rep. 2021;37:110143.
- Hou F, Teng Z, Ru J, Liu H, Li J, Zhang Y, Sun S, Guo H. Flower-like Mesoporous Silica Nanoparticles as an Antigen Delivery Platform to Promote Systemic Immune Response. Nanomedicine 2022;42:102541.
- Wang T, Zou M, Jiang H, Ji Z, Gao P, Cheng G. Synthesis of a Novel Kind of Carbon Nanoparticle with Large Mesopores and Macropores and Its Application as an Oral Vaccine Adjuvant. Eur. J. Pharm. Sci. 2011;44:653–659.
- Flenniken ML, Willits DA, Harmsen AL, Liepold LO, Harmsen AG, Young MJ, Douglas T. Melanoma and Lymphocyte Cell-Specific Targeting Incorporated into a Heat Shock Protein Cage Architecture. Chem. Biol. 2006;13:161–170.
- Sasaki E, Hilvert D. Self-Assembly of Proteinaceous Multishell Structures Mediated by a Supercharged Protein. J. Phys. Chem. B 2016;120:6089–6095.
- Lee LA, Wang Q. Adaptations of Nanoscale Viruses and Other Protein Cages for Medical Applications. Nanomed. Nanotechnol. Biol. Med. 2006;2:137–149.
- Kanekiyo M, Wei CJ, Yassine HM, McTamney PM, Boyington JC, Whittle JRR, Rao SS, Kong WP, Wang L, Nabel GJ. Self-Assembling Influenza Nanoparticle Vaccines Elicit Broadly Neutralizing H1N1 Antibodies. Nature 2013;499:102–106.
- Zeltins A. Construction and Characterization of Virus-Like Particles: A Review. Mol. Biotechnol. 2013;53:92–107.
- Johnson JE, Chiu W. Structures of Virus and Virus-like Particles. Curr. Opin. Struct. Biol. 2000;10:229–235.
- Grgacic EVL, Anderson DA. Virus-like Particles: Passport to Immune Recognition. Methods 2006;40:60–65.
- Pushko P, Pumpens P, Grens E. Development of Virus-like Particle Technology from Small Highly Symmetric to Large Complex Virus-like Particle Structures. Intervirology 2013;56:141–165.
- Garcea RL, Gissmann L. Virus-like Particles as Vaccines and Vessels for the Delivery of Small Molecules. Curr. Opin. Biotechnol. 2004;15:513–517.
- Nooraei S, Bahrulolum H, Hoseini ZS, Katalani C, Hajizade A, Easton AJ, Ahmadian G. Virus-like Particles: Preparation, Immunogenicity and Their Roles as Nanovaccines and Drug Nanocarriers. J. Nanobiotechnol. 2021;19:59.
- Dai S, Wang H, Deng F. Advances and Challenges in Enveloped Virus-like Particle (VLP)-Based Vaccines. J. Immunol. Sci. 2018;2:36–41.
- Fort M, Sibila M, Allepuz A, Mateu E, Roerink F, Segalés J. Porcine Circovirus Type 2 (PCV2) Vaccination of Conventional Pigs Prevents Viremia against PCV2 Isolates of Different Genotypes and Geographic Origins. Vaccine 2008;26:1063–1071.
- Rutkowska DA, Mokoena NB, Tsekoa TL, Dibakwane VS, O’Kennedy MM. Plant-Produced Chimeric Virus-like Particles—A New Generation Vaccine against African Horse Sickness. BMC Vet. Res. 2019;15:432.
- Kang YM, Cho HK, Kim JH, Lee SJ, Park SJ, Kim DY, Kim SY, Park JW, Lee MH, Kim MC. Single Dose of Multi-Clade Virus-like Particle Vaccine Protects Chickens against Clade 2.3.2.1 and Clade 2.3.4.4 Highly Pathogenic Avian Influenza Viruses. Sci. Rep. 2021;11:13786.
- Stewart M, Dubois E, Sailleau C, Bréard E, Viarouge C, Desprat A, Thiéry R, Zientara S, Roy P. Bluetongue Virus Serotype 8 Virus-like Particles Protect Sheep against Virulent Virus Infection as a Single or Multi-Serotype Cocktail Immunogen. Vaccine 2013;31:553–558.
- Guo HC, Sun SQ, Jin Y, Yang SL, Wei YQ, Sun DH, Yin SH, Ma JW, Liu ZX, Guo JH. Foot-and-Mouth Disease Virus-like Particles Produced by a SUMO Fusion Protein System in Escherichia Coli Induce Potent Protective Immune Responses in Guinea Pigs, Swine and Cattle. Vet. Res. 2013;44:48.
- Park JK, Lee DH, Yuk SS, Tseren-Ochir EO, Kwon JH, Noh JY, Kim BY, Choi SW, Kang SM, Lee JB. Virus-like Particle Vaccine Confers Protection against a Lethal Newcastle Disease Virus Challenge in Chickens and Allows a Strategy of Differentiating Infected from Vaccinated Animals. Clin. Vaccine Immunol. 2014;21:360–365.
- Hua T, Zhang D, Tang B, Chang C, Liu G, Zhang X. The Immunogenicity of the Virus-like Particles Derived from the VP2 Protein of Porcine Parvovirus. Vet. Microbiol. 2020;248:108795.
- Näslund J, Lagerqvist N, Habjan M, Lundkvist A, Evander M, Ahlm C, Weber F, Bucht G. Vaccination with Virus-like Particles Protects Mice from Lethal Infection of Rift Valley Fever Virus. Virology 2009;385:409–415.
- Liu F, Ge S, Li L, Wu X, Liu Z, Wang Z. Virus-like Particles: Potential Veterinary Vaccine Immunogens. Res. Vet. Sci. 2012;93:553–559.
- Crisci E, Bárcena J, Montoya M. Virus-like Particle-Based Vaccines for Animal Viral Infections. Inmunologia 2013;32:102–116.
- Chung YH, Church D, Koellhoffer EC, Osota E, Shukla S, Rybicki EP, Pokorski JK, Steinmetz NF. Integrating Plant Molecular Farming and Materials ReseArch. for Next-Generation Vaccines. Nat. Rev. Mater. 2022;7:372–388.
- Chan JC, Chan AT. Biologics and Biosimilars: What, Why and How?. ESMO Open 2017;2:e000180.
- Goeddel DV, Kleid DG, Bolivar F, Heyneker HL, Yansura DG, Crea R, Hirose T, Kraszewski A, Itakura K, Riggs AD. Expression in Escherichia Coli of Chemically Synthesized Genes for Human Insulin. Proc. Natl. Acad. Sci. USA 1979;76:106–110.
- Overton TW. Recombinant Protein Production in Bacterial Hosts. Drug Discov. Today 2014;19:590–601.
- Makrides SC. Strategies for Achieving High-Level Expression of Genes in Escherichia Coli. Microbiol. Rev. 1996;60:512–538.
- Kim HJ, Kim HJ. Yeast as an Expression System for Producing Virus-like Particles: What Factors Do We Need to Consider?. Lett. Appl. Microbiol. 2017;64:111–123.
- Jefferis R. Posttranslational Modifications and the Immunogenicity of Biotherapeutics. J. Immunol. Res. 2016;2016:5358272.
- Rybicki EP. Plant Molecular Farming of Virus-like Nanoparticles as Vaccines and Reagents. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2020;12:e1587.
- Zahmanova G, Takova K, Valkova R, Toneva V, Minkov I, Andonov A, Lukov GL. Plant-Derived Recombinant Vaccines against Zoonotic Viruses. Life 2022;12:156.
- Scotti N, Rybicki EP. Virus-like Particles Produced in Plants as Potential Vaccines. Expert Rev. Vaccines 2013;12:211–224.
- Walwyn DR, Huddy SM, Rybicki EP. Techno-Economic Analysis of Horseradish Peroxidase Production Using a Transient Expression System in Nicotiana benthamiana. Appl. Biochem. Biotechnol. 2015;175:841–854.
- Ward BJ, Makarkov A, Séguin A, Pillet S, Trépanier S, Dhaliwall J, Libman MD, Vesikari T, Landry N. Efficacy, Immunogenicity, and Safety of a Plant-Derived, Quadrivalent, Virus-like Particle Influenza Vaccine in Adults (18–64 Years) and Older Adults (≥65 Years): Two Multicentre, Randomised Phase 3 Trials. Lancet 2020;396:1491–1503.
- Kyriakidis NC, López-Cortés A, González EV, Grimaldos AB, Prado EO. SARS-CoV-2 Vaccines Strategies: A Comprehensive Review of Phase 3 Candidates. npj Vaccines 2021;6:28.
- Kurokawa N, Robinson MK, Bernard C, Kawaguchi Y, Koujin Y, Koen A, Madhi S, Polasek TM, McNeal M, Dargis M. Safety and Immunogenicity of a Plant-Derived Rotavirus-like Particle Vaccine in Adults, Toddlers and Infants. Vaccine 2021;39:5513–5523.
- Jordan LE, Mayor HD. The Fine Structure of Reovirus, a New Member of the Icosahedral Series. Virology 1962;17:597–599.
- Silverstein SC, Schur PH. Immunofluorescent Localization of Double-Stranded RNA in Reovirus-Infected Cells. Virology 1970;41:564–566.
- Touris-Otero F, Martínez-Costas J, Vakharia VN, Benavente J. Avian Reovirus Nonstructural Protein MicroNS Forms Viroplasm-like Inclusions and Recruits Protein SigmaNS to These Structures. Virology 2004;319:94–106.
- Tourís-Otero F, Cortez-San Martín M, Martínez-Costas J, Benavente J. Avian Reovirus Morphogenesis Occurs within Viral Factories and Begins with the Selective Recruitment of SigmaNS and LambdaA to MicroNS Inclusions. J. Mol. Biol. 2004;341:361–374.
- Brandariz-Nuñez A, Menaya-Vargas R, Benavente J, Martinez-Costas J. Avian Reovirus MicroNS Protein Forms Homo-Oligomeric Inclusions in a Microtubule-Independent Fashion, Which Involves Specific Regions of Its C-Terminal Domain. J. Virol. 2010;84:4289–4301.
- Brandariz-Nuñez A, Menaya-Vargas R, Benavente J, Martinez-Costas J. A Versatile Molecular Tagging Method for Targeting Proteins to Avian Reovirus MuNS Inclusions. Use in Protein Immobilization and Purification. PLoS ONE 2010;5:e13961.
- Brandariz-Nuñez A, Menaya-Vargas R, Benavente J, Martinez-Costas J. IC-Tagging and Protein Relocation to ARV MuNS Inclusions: A Method to Study Protein-Protein Interactions in the Cytoplasm or Nucleus of Living Cells. PLoS ONE 2010;5:e13785.
- Barreiro-Piñeiro N, Lostalé-Seijo I, Varela-Calviño R, Benavente J, Martínez-Costas JM. IC-Tagging Methodology Applied to the Expression of Viral Glycoproteins and the Difficult-to-Express Membrane-Bound IGRP Autoantigen. Sci. Rep. 2018;8:16286.
- Pose-Boirazian T, Eibes G, Barreiro-Piñeiro N, Díaz-Jullien C, Lema JM, Martínez-Costas J. Chemical and Thermal Stabilization of CotA Laccase via a Novel One-Step Expression and Immobilization in MuNS-Mi Nanospheres. Sci. Rep. 2021;11:2802.
- Bastús NG, Sánchez-Tilló E, Pujals S, Farrera C, Kogan MJ, Giralt E, Celada A, Lloberas J, Puntes V. Peptides Conjugated to Gold Nanoparticles Induce Macrophage Activation. Mol. Immunol. 2009;46:743–748.
- Zepeda-Cervantes J, Ramírez-Jarquín JO, Vaca L. Interaction Between Virus-Like Particles (VLPs) and Pattern Recognition Receptors (PRRs) From Dendritic Cells (DCs): Toward Better Engineering of VLPs. Front Immunol. 2020;11:1100.
- Fromen CA, Rahhal TB, Robbins GR, Kai MP, Shen TW, Luft JC, DeSimone JM. Nanoparticle Surface Charge Impacts Distribution, Uptake and Lymph Node Trafficking by Pulmonary Antigen-Presenting Cells. Nanomedicine 2016;12:677–687.
- Benne N, van Duijn J, Kuiper J, Jiskoot W, Slütter B. Orchestrating Immune Responses: How Size, Shape and Rigidity Affect the Immunogenicity of Particulate Vaccines. J. Control. Release 2016;234:124–134.
- Zinkhan S, Ogrina A, Balke I, Reseviča G, Zeltins A, de Brot S, Lipp C, Chang X, Zha L, Vogel M. The Impact of Size on Particle Drainage Dynamics and Antibody Response. J. Control. Release 2021;331:296–308.
- Reddy ST, Rehor A, Schmoekel HG, Hubbell JA, Swartz MA. In Vivo Targeting of Dendritic Cells in Lymph Nodes with Poly(Propylene Sulfide) Nanoparticles. J. Control. Release 2006;112:26–34.
- Smith DM, Simon JK, Baker Jr JR. Applications of Nanotechnology for Immunology. Nat. Rev. Immunol. 2013;13:592–605.
- Cruz LJ, Tacken PJ, Fokkink R, Joosten B, Stuart MC, Albericio F, Torensma R, Figdor CG. Targeted PLGA Nano- but Not Microparticles Specifically Deliver Antigen to Human Dendritic Cells via DC-SIGN in Vitro. J. Control. Release 2010;144:118–126.
- Blank F, Stumbles PA, Seydoux E, Holt PG, Fink A, Rothen-Rutishauser B, Strickland DH, von Garnier C. Size-Dependent Uptake of Particles by Pulmonary Antigen-Presenting Cell Populations and Trafficking to Regional Lymph Nodes. Am. J. Respir. Cell Mol. Biol. 2013;49:67–77.
- Dacoba TG, Olivera A, Torres D, Crecente-Campo J, Alonso MJ. Modulating the Immune System through Nanotechnology. Semin. Immunol. 2017;34:78–102.
- Pacheco P, White D, Sulchek T. Effects of Microparticle Size and Fc Density on Macrophage Phagocytosis. PLoS ONE 2013;8:e60989.
- He C, Hu Y, Yin L, Tang C, Yin C. Effects of Particle Size and Surface Charge on Cellular Uptake and Biodistribution of Polymeric Nanoparticles. Biomaterials 2010;31:3657–3666.
- Beduneau A, Ma Z, Grotepas CB, Kabanov A, Rabinow BE, Gong N, Mosley RL, Dou H, Boska MD, Gendelman HE. Facilitated Monocyte-Macrophage Uptake and Tissue Distribution of Superparmagnetic Iron-Oxide Nanoparticles. PLoS ONE 2009;4:e4343.
- Storni T, Bachmann MF. Loading of MHC Class I and II Presentation Pathways by Exogenous Antigens: A Quantitative in Vivo Comparison. J. Immunol. 2004;172:6129–6135.
- Barth H, Ulsenheimer A, Pape GR, Diepolder HM, Hoffmann M, Neumann-Haefelin C, Thimme R, Henneke P, Klein R, Paranhos-Baccalà G. Uptake and Presentation of Hepatitis C Virus-like Particles by Human Dendritic Cells. Blood 2005;105:3605–3614.
- Wang Z, Liu M, Zhao H, Wang P, Ma W, Zhang Y, Wu W, Peng C. Induction of Robust and Specific Humoral and Cellular Immune Responses by Bovine Viral Diarrhea Virus Virus-Like Particles (BVDV-VLPs) Engineered with Baculovirus Expression Vector System. Vaccines 2021;9:350.
- Morón VG, Rueda P, Sedlik C, Leclerc C. In Vivo, Dendritic Cells Can Cross-Present Virus-like Particles Using an Endosome-to-Cytosol Pathway. J. Immunol. 2003;171:2242–2250.
- Joffre OP, Segura E, Savina A, Amigorena S. Cross-Presentation by Dendritic Cells. Nat. Rev. Immunol. 2012;12:557–569.
- Jeggo MH, Wardley RC, Brownlie J. A Study of the Role of Cell-Mediated Immunity in Bluetongue Virus Infection in Sheep, Using Cellular Adoptive Transfer Techniques. Immunology 1984;52:403–410.
- Umeshappa CS, Singh KP, Pandey AB, Singh RP, Nanjundappa RH. Cell-Mediated Immune Response and Cross-Protective Efficacy of Binary Ethylenimine-Inactivated Bluetongue Virus Serotype-1 Vaccine in Sheep. Vaccine 2010;28:2522–2531.
- Sánchez-Cordón PJ, Pérez de Diego AC, Gómez-Villamandos JC, Sánchez-Vizcaíno JM, Pleguezuelos FJ, Garfia B, del Carmen P, Pedrera M. Comparative Analysis of Cellular Immune Responses and Cytokine Levels in Sheep Experimentally Infected with Bluetongue Virus Serotype 1 and 8. Vet. Microbiol. 2015;177:95–105.
- Martín V, Pascual E, Avia M, Peña L, Valcárcel F, Sevilla N. Protective Efficacy in Sheep of Adenovirus-Vectored Vaccines against Bluetongue Virus Is Associated with Specific T Cell Responses. PLoS ONE 2015;10:e0143273.
- Utrilla-Trigo S, Jiménez-Cabello L, Alonso-Ravelo R, Calvo-Pinilla E, Marín-López A, Moreno S, Lorenzo G, Benavides J, Gilbert S, Nogales A. Heterologous Combination of ChAdOx1 and MVA Vectors Expressing Protein NS1 as Vaccination Strategy to Induce Durable and Cross-Protective CD8+ T Cell Immunity to Bluetongue Virus. Vaccines 2020;8:346.
- Utrilla-Trigo S, Jiménez-Cabello L, Calvo-Pinilla E, Marín-López A, Lorenzo G, Sánchez-Cordón P, Moreno S, Benavides J, Gilbert S, Nogales A. The Combined Expression of the Non-Structural Protein NS1 and the N-Terminal Half of NS2 (NS21-180) by ChAdOx1 and MVA Confers Protection against Clinical Disease in Sheep upon Bluetongue Virus Challenge. J. Virol. 2021;96:e01614–e01621.
- Anderson J, Hägglund S, Bréard E, Comtet L, Lövgren Bengtsson K, Pringle J, Zientara S, Valarcher JF. Evaluation of the Immunogenicity of an Experimental Subunit Vaccine That Allows Differentiation between Infected and Vaccinated Animals against Bluetongue Virus Serotype 8 in Cattle. Clin. Vaccine Immunol. 2013;20:1115–1122.
- Marín-López A, Calvo-Pinilla E, Barriales D, Lorenzo G, Brun A, Anguita J, Ortego J. CD8 T Cell Responses to an Immunodominant Epitope within the Nonstructural Protein NS1 Provide Wide Immunoprotection against Bluetongue Virus in IFNAR −/− Mice. J. Virol. 2018;92:e00938-18.
- Marín-López A, Barreiro-Piñeiro N, Utrilla-Trigo S, Barriales D, Benavente J, Nogales A, Martínez-Costas J, Ortego J, Calvo-Pinilla E. Cross-Protective Immune Responses against African Horse Sickness Virus after Vaccination with Protein NS1 Delivered by Avian Reovirus MuNS Microspheres and Modified Vaccinia Virus Ankara. Vaccine 2020;38:882–889.
- Fearon SH, Dennis SJ, Hitzeroth II, Rybicki EP, Meyers AE. Humoral and Cell-Mediated Immune Responses to Plant-Produced African Horse Sickness Virus VP7 Quasi-Crystals. Virus Res. 2021;294:198284.
- Rojas JM, Peña L, Martín V, Sevilla N. Ovine and Murine T Cell Epitopes from the Non-Structural Protein 1 (NS1) of Bluetongue Virus Serotype 8 (BTV-8) Are Shared among Viral Serotypes. Vet. Res. 2014;45:30.
- Calvo-Pinilla E, Marín-López A, Moreno S, Lorenzo G, Utrilla-Trigo S, Jiménez-Cabello L, Benavides J, Nogales A, Blasco R, Brun A. A Protective Bivalent Vaccine against Rift Valley Fever and Bluetongue. npj Vaccines 2020;5:70.
- Storni T, Lechner F, Erdmann I, Bächi T, Jegerlehner A, Dumrese T, Kündig TM, Ruedl C, Bachmann MF. Critical Role for Activation of Antigen-Presenting Cells in Priming of Cytotoxic T Cell Responses after Vaccination with Virus-like Particles. J. Immunol. 2002;168:2880–2886.
- Selby LI, Cortez-Jugo CM, Such GK, Johnston APR. Nanoescapology: Progress toward Understanding the Endosomal Escape of Polymeric Nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2017;9:e1452.
- Mant A, Chinnery F, Elliott T, Williams AP. The Pathway of Cross-Presentation Is Influenced by the Particle Size of Phagocytosed Antigen. Immunology 2012;136:163–175.
- Silva AL, Rosalia RA, Varypataki E, Sibuea S, Ossendorp F, Jiskoot W. Poly-(Lactic-Co-Glycolic-Acid)-Based Particulate Vaccines: Particle Uptake by Dendritic Cells Is a Key Parameter for Immune Activation. Vaccine 2015;33:847–854.
- Hirai T, Yoshioka Y, Takahashi H, Ichihashi K, Yoshida T, Tochigi S, Nagano K, Abe Y, Kamada H, Tsunoda S. Amorphous Silica Nanoparticles Enhance Cross-Presentation in Murine Dendritic Cells. Biochem. Biophys. Res. Commun. 2012;427:553–556.
- Rodríguez-Martín D, Louloudes-Lázaro A, Avia M, Martín V, Rojas JM, Sevilla N. The Interplay between Bluetongue Virus Infections and Adaptive Immunity. Viruses 2021;13:1511.
- French TJ, Marshall JJ, Roy P. Assembly of Double-Shelled, Viruslike Particles of Bluetongue Virus by the Simultaneous Expression of Four Structural Proteins. J. Virol. 1990;64:5695–5700.
- Martinez-Torrecuadrada JL, Iwata H, Venteo A, Casal I, Roy P. Expression and Characterization of the Two Outer Capsid Proteins of African Horsesickness Virus: The Role of VP2 in Virus Neutralization. Virology 1994;202:348–359.
- Sailleau C, Breard E, Viarouge C, Belbis G, Lilin T, Vitour D, Zientara S. Experimental Infection of Calves with Seven Serotypes of Epizootic Hemorrhagic Disease Virus: Production and Characterization of Reference Sera. Vet. Ital. 2019;55:339–346.
- Jeggo MH, Wardley RC, Taylor WP. Role of Neutralising Antibody in Passive Immunity to Bluetongue Infection. Res. Vet. Sci. 1984;36:81–86.
- Mosmann TR, Coffman RL. TH1 and TH2 Cells: Different Patterns of Lymphokine Secretion Lead to Different Functional Properties. Annu. Rev. Immunol. 1989;7:145–173.
- Abbas AK, Murphy KM, Sher A. Functional Diversity of Helper T Lymphocytes. Nature 1996;383:787–793.
- Yao Q, Zhang R, Guo L, Li M, Chen C. Th Cell-Independent Immune Responses to Chimeric Hemagglutinin/Simian Human Immunodeficiency Virus-like Particles Vaccine. J. Immunol. 2004;173:1951–1958.
- Ramirez K, Wahid R, Richardson C, Bargatze RF, El-Kamary SS, Sztein MB, Pasetti MF. Intranasal Vaccination with an Adjuvanted Norwalk Virus-like Particle Vaccine Elicits Antigen-Specific B Memory Responses in Human Adult Volunteers. Clin. Immunol. 2012;144:98–108.
- Schmidt MR, McGinnes LW, Kenward SA, Willems KN, Woodland RT, Morrison TG. Long-Term and Memory Immune Responses in Mice against Newcastle Disease Virus-like Particles Containing Respiratory Syncytial Virus Glycoprotein Ectodomains. J. Virol. 2012;86:11654–11662.
- Giannini SL, Hanon E, Moris P, Van Mechelen M, Morel S, Dessy F, Fourneau MA, Colau B, Suzich J, Losonksy G. Enhanced Humoral and Memory B Cellular Immunity Using HPV16/18 L1 VLP Vaccine Formulated with the MPL/Aluminium Salt Combination (AS04) Compared to Aluminium Salt Only. Vaccine 2006;24:5937–5949.
- Zabel F, Mohanan D, Bessa J, Link A, Fettelschoss A, Saudan P, Kündig TM, Bachmann MF. Viral Particles Drive Rapid Differentiation of Memory B Cells into Secondary Plasma Cells Producing Increased Levels of Antibodies. J. Immunol. 2014;192:5499–5508.
- Jiao YY, Fu YH, Yan YF, Hua Y, Ma Y, Zhang XJ, Song JD, Peng XL, Huang J, Hong T. A Single Intranasal Administration of Virus-like Particle Vaccine Induces an Efficient Protection for Mice against Human Respiratory Syncytial Virus. Antivir. Res. 2017;144:57–69.
- Landry N, Pillet S, Favre D, Poulin JF, Trépanier S, Yassine-Diab B, Ward BJ. Influenza Virus-like Particle Vaccines Made in Nicotiana benthamiana Elicit Durable, Poly-Functional and Cross-Reactive T Cell Responses to Influenza HA Antigens. Clin. Immunol. 2014;154:164–177.
- Karuturi BVK, Tallapaka SB, Yeapuri P, Curran SM, Sanderson SD, Vetro JA. Encapsulation of an EP67-Conjugated CTL Peptide Vaccine in Nanoscale Biodegradable Particles Increases the Efficacy of Respiratory Immunization and Affects the Magnitude and Memory Subsets of Vaccine-Generated Mucosal and Systemic CD8+ T Cells in a Diameter-Dependent Manner. Mol. Pharm. 2017;14:1469–1481.
- Bhardwaj P, Bhatia E, Sharma S, Ahamad N, Banerjee R. Advancements in Prophylactic and Therapeutic Nanovaccines. Acta Biomater. 2020;108:1–21.
- King AM, Lefkowitz E, Adams MJ, Carstens EB. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. .
- Du Toit RM. The Transmission of Blue-Tongue and Horse-Sickness by Culicoides. J. Vet. Sci. Anim. Ind. 1944;19:7–16.
- Maclachlan NJ, Drew CP, Darpel KE, Worwa G. The Pathology and Pathogenesis of Bluetongue. J. Comp. Pathol. 2009;141:1–16.
- Drolet BS, Reister LM, Rigg TD, Nol P, Podell BK, Mecham JO, VerCauteren KC, van Rijn PA, Wilson WC, Bowen RA. Experimental Infection of White-Tailed Deer (Odocoileus virginianus) with Northern European Bluetongue Virus Serotype 8. Vet. Microbiol. 2013;166:347–355.
- Erasmus BJ. Bluetongue in Sheep and Goats. Aust. Vet. J. 1975;51:165–170.
- Rushton J, Lyons N. Economic Impact of Bluetongue: A Review of the Effects on Production. Vet. Ital. 2015;51:401–406.
- Gethmann J, Probst C, Conraths FJ. Economic Impact of a Bluetongue Serotype 8 Epidemic in Germany. Front. Vet. Sci. 2020;7:65.
- Maan S, Maan NS, Samuel AR, Rao S, Attoui H, Mertens PPC. Analysis and Phylogenetic Comparisons of Full-Length VP2 Genes of the 24 Bluetongue Virus Serotypes. J. Gen. Virol. 2007;88:621–630.
- Saminathan M, Singh KP, Khorajiya JH, Dinesh M, Vineetha S, Maity M, Rahman AF, Misri J, Malik YS, Gupta VK. An Updated Review on Bluetongue Virus: Epidemiology, Pathobiology, and Advances in Diagnosis and Control with Special Reference to India. Vet. Q. 2020;40:258–321.
- French TJ, Roy P. Synthesis of Bluetongue Virus (BTV) Corelike Particles by a Recombinant Baculovirus Expressing the Two Major Structural Core Proteins of BTV. J. Virol. 1990;64:1530–1536.
- Loudon PT, Hirasawa T, Oldfield S, Murphy M, Roy P. Expression of the Outer Capsid Protein VP5 of Two Bluetongue Viruses, and Synthesis of Chimeric Double-Shelled Virus-like Particles Using Combinations of Recombinant Baculoviruses. Virology 1991;182:793–801.
- Thuenemann EC, Meyers AE, Verwey J, Rybicki EP, Lomonossoff GP. A Method for Rapid Production of Heteromultimeric Protein Complexes in Plants: Assembly of Protective Bluetongue Virus-like Particles. Plant Biotechnol. J. 2013;11:839–846.
- Mokoena NB, Moetlhoa B, Rutkowska DA, Mamputha S, Dibakwane VS, Tsekoa TL, O’Kennedy MM. Plant-Produced Bluetongue Chimaeric VLP Vaccine Candidates Elicit Serotype-Specific Immunity in Sheep. Vaccine 2019;37:6068–6075.
- Stewart M, Dovas CI, Chatzinasiou E, Athmaram TN, Papanastassopoulou M, Papadopoulos O, Roy P. Protective Efficacy of Bluetongue Virus-like and Subvirus-like Particles in Sheep: Presence of the Serotype-Specific VP2, Independent of Its Geographic Lineage, Is Essential for Protection. Vaccine 2012;30:2131–2139.
- Wade-Evans AM, Romero CH, Mellor P, Takamatsu H, Anderson J, Thevasagayam J, Fleming MJ, Mertens PP, Black DN. Expression of the Major Core Structural Protein (VP7) of Bluetongue Virus, by a Recombinant Capripox Virus, Provides Partial Protection of Sheep against a Virulent Heterotypic Bluetongue Virus Challenge. Virology 1996;220:227–231.
- Calvo-Pinilla E, Rodríguez-Calvo T, Sevilla N, Ortego J. Heterologous Prime Boost Vaccination with DNA and Recombinant Modified Vaccinia Virus Ankara Protects IFNAR(−/−) Mice against Lethal Bluetongue Infection. Vaccine 2009;28:437–445.
- Roy P, Bishop DH, LeBlois H, Erasmus BJ. Long-Lasting Protection of Sheep against Bluetongue Challenge after Vaccination with Virus-like Particles: Evidence for Homologous and Partial Heterologous Protection. Vaccine 1994;12:805–811.
- Stewart M, Bhatia Y, Athmaran TN, Noad R, Gastaldi C, Dubois E, Russo P, Thiéry R, Sailleau C, Bréard E. Validation of a Novel Approach for the Rapid Production of Immunogenic Virus-like Particles for Bluetongue Virus. Vaccine 2010;28:3047–3054.
- Pérez de Diego AC, Athmaram TN, Stewart M, Rodríguez-Sánchez B, Sánchez-Vizcaíno JM, Noad R, Roy P. Characterization of Protection Afforded by a Bivalent Virus-Like Particle Vaccine against Bluetongue Virus Serotypes 1 and 4 in Sheep. PLoS ONE 2011;6:e26666.
- Roy P, French T, Erasmus BJ. Protective Efficacy of Virus-like Particles for Bluetongue Disease. Vaccine 1992;10:28–32.
- Guy B, Barban V, Mantel N, Aguirre M, Gulia S, Pontvianne J, Jourdier TM, Ramirez L, Gregoire V, Charnay C. Evaluation of Interferences between Dengue Vaccine Serotypes in a Monkey Model. Am. J. Trop. Med. Hyg. 2009;80:302–311.
- McClain DJ, Pittman PR, Ramsburg HH, Nelson GO, Rossi CA, Mangiafico JA, Schmaljohn AL, Malinoski FJ. Immunologic Interference from Sequential Administration of Live Attenuated Alphavirus Vaccines. J. Infect. Dis. 1998;177:634–641.
- Parker EPK, Kampmann B, Kang G, Grassly NC. Influence of Enteric Infections on Response to Oral Poliovirus Vaccine: A Systematic Review and Meta-Analysis. J. Infect. Dis. 2014;210:853–864.
- Wu W, Roy P. Sialic Acid Binding Sites in VP2 of Bluetongue Virus and Their Use during Virus Entry. J. Virol. 2022;96:e0167721.
- Dishlers A, Skrastina D, Renhofa R, Petrovskis I, Ose V, Lieknina I, Jansons J, Pumpens P, Sominskaya I. The Hepatitis B Virus Core Variants That Expose Foreign C-Terminal Insertions on the Outer Surface of Virus-Like Particles. Mol. Biotechnol. 2015;57:1038–1049.
- Gedvilaite A, Frömmel C, Sasnauskas K, Micheel B, Ozel M, Behrsing O, Staniulis J, Jandrig B, Scherneck S, Ulrich R. Formation of Immunogenic Virus-like Particles by Inserting Epitopes into Surface-Exposed Regions of Hamster Polyomavirus Major Capsid Protein. Virology 2000;273:21–35.
- Aston-Deaville S, Carlsson E, Saleem M, Thistlethwaite A, Chan H, Maharjan S, Facchetti A, Feavers IM, Alistair Siebert C, Collins RF. An Assessment of the Use of Hepatitis B Virus Core Protein Virus-like Particles to Display Heterologous Antigens from Neisseria Meningitidis. Vaccine 2020;38:3201–3209.
- Li G, Liu L, Xu B, Hu J, Kuang H, Wang X, Wang L, Cui X, Sun H, Rong J. Displaying Epitope B and Epitope 7 of Porcine Reproductive and Respiratory Syndrome Virus on Virus like Particles of Porcine Circovirus Type 2 Provides Partial Protection to Pigs. J. Vet. Med. Sci. 2021;83:1263–1272.
- Pascual E, Mata CP, Gómez-Blanco J, Moreno N, Bárcena J, Blanco E, Rodríguez-Frandsen A, Nieto A, Carrascosa JL, Castón JR. Structural Basis for the Development of Avian Virus Capsids That Display Influenza Virus Proteins and Induce Protective Immunity. J. Virol. 2015;89:2563–2574.
- Roose K, De Baets S, Schepens B, Saelens X. Hepatitis B Core-Based Virus-like Particles to Present Heterologous Epitopes. Expert Rev. Vaccines 2013;12:183–198.
- Nagesha HS, Wang LF, Hyatt AD. Virus-like Particles of Calicivirus as Epitope Carriers. Arch. Virol. 1999;144:2429–2439.
- Belyaev AS, Roy P. Presentation of Hepatitis B Virus PreS2 Epitope on Bluetongue Virus Core-like Particles. Virology 1992;190:840–844.
- Le Blois H, Roy P. A Single Point Mutation in the VP7 Major Core Protein of Bluetongue Virus Prevents the Formation of Core-like Particles. J. Virol. 1993;67:353–359.
- Adler S, Reay P, Roy P, Klenk HD. Induction of T Cell Response by Bluetongue Virus Core-like Particles Expressing a T Cell Epitope of the M1 Protein of Influenza A Virus. Med. Microbiol. Immunol. 1998;187:91–96.
- Tanaka S, Mikhailov M, Roy P. Synthesis of Bluetongue Virus Chimeric VP3 Molecules and Their Interactions with VP7 Protein to Assemble into Virus Core-like Particles. Virology 1995;214:593–601.
- Ponndorf D, Meshcheriakova Y, Thuenemann EC, Dobon Alonso A, Overman R, Holton N, Dowall S, Kennedy E, Stocks M, Lomonossoff GP. Plant-made Dengue Virus-like Particles Produced by Co-expression of Structural and Non-structural Proteins Induce a Humoral Immune Response in Mice. Plant Biotechnol. J. 2021;19:745–756.
- Brillault L, Jutras PV, Dashti N, Thuenemann EC, Morgan G, Lomonossoff GP, Landsberg MJ, Sainsbury F. Engineering Recombinant Virus-like Nanoparticles from Plants for Cellular Delivery. ACS Nano 2017;11:3476–3484.
- Jeggo MH, Wardley RC, Brownlie J. Importance of Ovine Cytotoxic T Cells in Protection against Bluetongue Virus Infection. Prog. Clin. Biol. Res. 1985;178:477–487.
- Marín-López A, Otero-Romero I, de la Poza F, Menaya-Vargas R, Calvo-Pinilla E, Benavente J, Martínez-Costas JM, Ortego J. VP2, VP7, and NS1 Proteins of Bluetongue Virus Targeted in Avian Reovirus MuNS-Mi Microspheres Elicit a Protective Immune Response in IFNAR(-/−) Mice. Antivir. Res. 2014;110:42–51.
- Marín-López A, Calvo-Pinilla E, Barriales D, Lorenzo G, Benavente J, Brun A, Martínez-Costas JM, Ortego J. Microspheres-Prime/RMVA-Boost Vaccination Enhances Humoral and Cellular Immune Response in IFNAR(−/−) Mice Conferring Protection against Serotypes 1 and 4 of Bluetongue Virus. Antivir. Res. 2017;142:55–62.
- Hewat EA, Booth TF, Wade RH, Roy P. 3-D Reconstruction of Bluetongue Virus Tubules Using Cryoelectron Microscopy. J. Struct. Biol. 1992;108:35–48.
- Boyce M, Celma CCP, Roy P. Bluetongue Virus Non-Structural Protein 1 Is a Positive Regulator of Viral Protein Synthesis. Virol. J. 2012;9:178.
- Urakawa T, Roy P. Bluetongue Virus Tubules Made in Insect Cells by Recombinant Baculoviruses: Expression of the NS1 Gene of Bluetongue Virus Serotype 10. J. Virol. 1988;62:3919–3927.
- Huismans H, Els HJ. Characterization of the Tubules Associated with the Replication of Three Different Orbiviruses. Virology 1979;92:397–406.
- Kerviel A, Ge P, Lai M, Jih J, Boyce M, Zhang X, Zhou ZH, Roy P. Atomic Structure of the Translation Regulatory Protein NS1 of Bluetongue Virus. Nat. Microbiol. 2019;4:837–845.
- Koo M, Bendahmane M, Lettieri GA, Paoletti AD, Lane TE, Fitchen JH, Buchmeier MJ, Beachy RN. Protective Immunity against Murine Hepatitis Virus (MHV) Induced by Intranasal or Subcutaneous Administration of Hybrids of Tobacco Mosaic Virus That Carries an MHV Epitope. Proc. Natl. Acad. Sci. USA 1999;96:7774–7779.
- Špakova A, Dalgėdienė I, Insodaitė R, Sasnauskienė A, Žvirblienė A, Petraitytė-Burneikienė R. VB_EcoS_NBD2 Bacteriophage-Originated Polytubes as a Carrier for the Presentation of Foreign Sequences. Virus Res. 2020;290:198194.
- Harada LK, Silva EC, Campos WF, Del Fiol FS, Vila M, Dąbrowska K, Krylov VN, Balcão VM. Biotechnological Applications of Bacteriophages: State of the Art. Microbiol. Res. 2018;212–213:38–58.
- Aghebati-Maleki L, Bakhshinejad B, Baradaran B, Motallebnezhad M, Aghebati-Maleki A, Nickho H, Yousefi M, Majidi J. Phage Display as a Promising Approach for Vaccine Development. J. Biomed. Sci. 2016;23:66.
- Smith GP. Filamentous Fusion Phage: Novel Expression Vectors That Display Cloned Antigens on the Virion Surface. Science 1985;228:1315–1317.
- De la Cruz VF, Lal AA, McCutchan TF. Immunogenicity and Epitope Mapping of Foreign Sequences via Genetically Engineered Filamentous Phage. J. Biol. Chem. 1988;263:4318–4322.
- Larke N, Murphy A, Wirblich C, Teoh D, Estcourt MJ, McMichael AJ, Roy P, Hanke T. Induction of Human Immunodeficiency Virus Type 1-Specific T Cells by a Bluetongue Virus Tubule-Vectored Vaccine Prime-Recombinant Modified Virus Ankara Boost Regimen. J. Virol. 2005;79:14822–14833.
- Marshall JJA, Fayard B, Roy P. Biophysical Studies on the Morphology of Baculovirus-Expressed Bluetongue Virus Tubules. J. Gen. Virol. 1990;71:1839–1844.
- Murphy A, Roy P. Manipulation of the Bluetongue Virus Tubules for Immunogen Delivery. Future Microbiol. 2008;3:351–359.
- Monastyrskaya K, Gould EA, Roy P. Characterization and Modification of the Carboxy-Terminal Sequences of Bluetongue Virus Type 10 NS1 Protein in Relation to Tubule Formation and Location of an Antigenic Epitope in the Vicinity of the Carboxy Terminus of the Protein. J. Virol. 1995;69:2831–2841.
- Mikhailov M, Monastyrskaya K, Bakker T, Roy P. A New Form of Particulate Single and Multiple Immunogen Delivery System Based on Recombinant Bluetongue Virus-Derived Tubules. Virology 1996;217:323–331.
- Andrade S, Pinho F, Ribeiro AM, Carreira M, Casanueva FF, Roy P, Monteiro MP. Immunization Against Active Ghrelin Using Virus-Like Particles for Obesity Treatment. Curr. Pharm. Des. 2013;19:6551–6558.
- Ghosh MK, Dériaud E, Saron MF, Lo-Man R, Henry T, Jiao X, Roy P, Leclerc C. Induction of Protective Antiviral Cytotoxic T Cells by a Tubular Structure Capable of Carrying Large Foreign Sequences. Vaccine 2002;20:1369–1377.
- Ghosh MK, Borca MV, Roy P. Virus-Derived Tubular Structure Displaying Foreign Sequences on the Surface Elicit CD4+ Th Cell and Protective Humoral Responses. Virology 2002;302:383–392.
- Ghosh MK, Li CL, Fayolle C, Dadaglio G, Murphy A, Lemonnier FA, Roy P, Leclerc C. Induction of HLA-A2-Restricted CTL Responses by a Tubular Structure Carrying Human Melanoma Epitopes. Vaccine 2002;20:2463–2473.
- Soi RK, Rurangirwa FR, McGuire TC, Rwambo PM, DeMartini JC, Crawford TB. Protection of Sheep against Rift Valley Fever Virus and Sheep Poxvirus with a Recombinant Capripoxvirus Vaccine. Clin. Vaccine Immunol. 2010;17:1842–1849.
- Ngichabe CK, Wamwayi HM, Barrett T, Ndungu EK, Black DN, Bostock CJ. Trial of a Capripoxvirus-Rinderpest Recombinant Vaccine in African Cattle. Epidemiol. Infect. 1997;118:63–70.
- Romero CH, Barrett T, Kitching RP, Carn VM, Black DN. Protection of Cattle against Rinderpest and Lumpy Skin Disease with a Recombinant Capripoxvirus Expressing the Fusion Protein Gene of Rinderpest Virus. Vet. Rec. 1994;135:152–154.
- Ngichabe CK, Wamwayi HM, Ndungu EK, Mirangi PK, Bostock CJ, Black DN, Barrett T. Long Term Immunity in African Cattle Vaccinated with a Recombinant Capripox-Rinderpest Virus Vaccine. Epidemiol. Infect. 2002;128:343–349.
- Romero CH, Barrett T, Kitching RP, Bostock C, Black DN. Protection of Goats against Peste Des Petits Ruminants with Recombinant Capripoxviruses Expressing the Fusion and Haemagglutinin Protein Genes of Rinderpest Virus. Vaccine 1995;13:36–40.
- Mellor PS, Hamblin C. African Horse Sickness. Vet. Res. 2004;35:445–466.
- Fassi-Fihri O, el Harrak M, Fassi-Fehri MM. Clinical, Virological and Immune Responses of Normal and Immunosuppressed Donkeys (Equus Asinus Africanus) after Inoculation with African Horse Sickness Virus. Arch. Virol. Suppl. 1998;14:49–56.
- Becker E, Venter GJ, Greyling T, Molini U, van Hamburg H. Evidence of African Horse Sickness Virus Infection of Equus Zebra Hartmannae in the South-Western Khomas Region, Namibia. Transbound. Emerg. Dis. 2018;65:278–280.
- Weyer CT, Grewar JD, Burger P, Rossouw E, Lourens C, Joone C, le Grange M, Coetzee P, Venter E, Martin DP. African Horse Sickness Caused by Genome Reassortment and Reversion to Virulence of Live, Attenuated Vaccine Viruses, South Africa, 2004–2014. Emerg. Infect. Dis. 2016;22:2087–2096.
- Molini U, Marucchella G, Maseke A, Ronchi GF, Di Ventura M, Salini R, Scacchia M, Pini A. Immunization of Horses with a Polyvalent Live-Attenuated African Horse Sickness Vaccine: Serological Response and Disease Occurrence under Field Conditions. Trials Vaccinol. 2015;4:24–28.
- Dennis SJ, Meyers AE, Hitzeroth II, Rybicki EP. African Horse Sickness: A Review of Current Understanding and Vaccine Development. Viruses 2019;11:844.
- Maree S, Durbach S, Huismans H. Intracellular Production of African Horsesickness Virus Core-like Particles by Expression of the Two Major Core Proteins, VP3 and VP7, in Insect Cells. J. Gen. Virol. 1998;79:333–337.
- Maree S, Maree FF, Putterill JF, de Beer TAP, Huismans H, Theron J. Synthesis of Empty African Horse Sickness Virus Particles. Virus Res. 2016;213:184–194.
- Burroughs JN, O’Hara RS, Smale CJ, Hamblin C, Walton A, Armstrong R, Mertens PP. Purification and Properties of Virus Particles, Infectious Subviral Particles, Cores and VP7 Crystals of African Horsesickness Virus Serotype 9. J. Gen. Virol. 1994;75:1849–1857.
- Dennis SJ, Meyers AE, Guthrie AJ, Hitzeroth II, Rybicki EP. Immunogenicity of Plant-produced African Horse Sickness Virus-like Particles: Implications for a Novel Vaccine. Plant Biotechnol. J. 2018;16:442–450.
- Dennis SJ, O’Kennedy MM, Rutkowska D, Tsekoa T, Lourens CW, Hitzeroth II, Meyers AE, Rybicki EP. Safety and Immunogenicity of Plant-Produced African Horse Sickness Virus-like Particles in Horses. Vet. Res. 2018;49:105.
- Maree FF, Huismans H. Characterization of Tubular Structures Composed of Nonstructural Protein NS1 of African Horsesickness Virus Expressed in Insect Cells. J. Gen. Virol. 1997;78:1077–1082.
- De la Poza F, Marín-López A, Castillo-Olivares J, Calvo-Pinilla E, Ortego J. Identification of CD8 T Cell Epitopes in VP2 and NS1 Proteins of African Horse Sickness Virus in IFNAR(-/−) Mice. Virus Res. 2015;210:149–153.
- Yadin H, Brenner J, Bumbrov V, Oved Z, Stram Y, Klement E, Perl S, Anthony S, Maan S, Batten C. Epizootic Haemorrhagic Disease Virus Type 7 Infection in Cattle in Israel. Vet. Rec. 2008;162:53–56.
- Mahmoud A, Danzetta ML, di Sabatino D, Spedicato M, Alkhatal Z, Dayhum A, Tolari F, Forzan M, Mazzei M, Savini G. First Seroprevalence Investigation of Epizootic Haemorrhagic Disease Virus in Libya. Open Vet. J. 2021;11:301–308.
- Allison AB, Goekjian VH, Potgieter AC, Wilson WC, Johnson DJ, Mertens PPC, Stallknecht DE. Detection of a Novel Reassortant Epizootic Hemorrhagic Disease Virus (EHDV) in the USA Containing RNA Segments Derived from Both Exotic (EHDV-6) and Endemic (EHDV-2) Serotypes. J. Gen. Virol. 2010;91:430–439.
- Brown-Joseph T, Rajko-Nenow P, Hicks H, Sahadeo N, Harrup LE, Carrington CV, Batten C, Oura CAL. Identification and Characterization of Epizootic Hemorrhagic Disease Virus Serotype 6 in Cattle Co-Infected with Bluetongue Virus in Trinidad, West Indies. Vet. Microbiol. 2019;229:1–6.
- Ruder MG, Johnson D, Ostlund E, Allison AB, Kienzle C, Phillips JE, Poulson RL, Stallknecht DE. The First 10 Years (2006-15) of Epizootic Hemorrhagic Disease Virus Serotype 6 in the USA. J. Wildl. Dis. 2017;53:901–905.
- Homan EJ, Taylor WP, de Ruiz HL, Yuill TM. Bluetongue Virus and Epizootic Haemorrhagic Disease of Deer Virus Serotypes in Northern Colombian Cattle. J. Hyg. 1985;95:165–172.
- Viarouge C, Lancelot R, Rives G, Bréard E, Miller M, Baudrimont X, Doceul V, Vitour D, Zientara S, Sailleau C. Identification of Bluetongue Virus and Epizootic Hemorrhagic Disease Virus Serotypes in French Guiana in 2011 and 2012. Vet. Microbiol. 2014;174:78–85.
- Verdezoto J, Breard E, Viarouge C, Quenault H, Lucas P, Sailleau C, Zientara S, Augot D, Zapata S. Novel Serotype of Bluetongue Virus in South America and First Report of Epizootic Haemorrhagic Disease Virus in Ecuador. Transbound. Emerg. Dis. 2018;65:244–247.
- Vinueza RL, Cruz M, Bréard E, Viarouge C, Zanella G. Bluetongue Virus and Epizootic Hemorrhagic Disease Virus Survey in Cattle of the Galapagos Islands. J. Vet. Diagn. Investig. 2019;31:271–275.
- Weir RP, Harmsen MB, Hunt NT, Blacksell SD, Lunt RA, Pritchard LI, Newberry KM, Hyatt AD, Gould AR, Melville LF. EHDV-1, a New Australian Serotype of Epizootic Haemorrhagic Disease Virus Isolated from Sentinel Cattle in the Northern Territory. Vet. Microbiol. 1997;58:135–143.
- Kedmi M, Van Straten M, Ezra E, Galon N, Klement E. Assessment of the Productivity Effects Associated with Epizootic Hemorrhagic Disease in Dairy Herds. J. Dairy Sci. 2010;93:2486–2495.
- Spedicato M, Carmine I, Teodori L, Leone A, Portanti O, Marini V, Pisciella M, Lorusso A, Savini G. Innocuity of a Commercial Live Attenuated Vaccine for Epizootic Hemorrhagic Disease Virus Serotype 2 in Late-Term Pregnant Cows. Vaccine 2016;34:1430–1435.
- Sunwoo SY, Noronha LE, Morozov I, Trujillo JD, Kim IJ, Schirtzinger EE, Faburay B, Drolet BS, Urbaniak K, McVey DS. Evaluation of A Baculovirus-Expressed VP2 Subunit Vaccine for the Protection of White-Tailed Deer (Odocoileus virginianus) from Epizootic Hemorrhagic Disease. Vaccines 2020;8:59.
- Yang T, Zhang J, Xu Q, Sun E, Li J, Lv S, Feng Y, Zhang Q, Wang H. Development of a Reverse Genetics System for Epizootic Hemorrhagic Disease Virus and Evaluation of Novel Strains Containing Duplicative Gene Rearrangements. J. Gen. Virol. 2015;96:2714–2720.
- Matsuo E, Saeki K, Roy P, Kawano J. Development of Reverse Genetics for Ibaraki Virus to Produce Viable VP6-Tagged IBAV. FEBS Open Bio. 2015;5:445–453.
- Alshaikhahmed K, Roy P. Generation of Virus-like Particles for Emerging Epizootic Haemorrhagic Disease Virus: Towards the Development of Safe Vaccine Candidates. Vaccine 2016;34:1103–1108.
- Mecham JO, Stallknecht D, Wilson WC. The S7 Gene and VP7 Protein Are Highly Conserved among Temporally and Geographically Distinct American Isolates of Epizootic Hemorrhagic Disease Virus. Virus Res. 2003;94:129–133.
- Forzan M, Maan S, Mazzei M, Belaganahalli MN, Bonuccelli L, Calamari M, Carrozza ML, Cappello V, Di Luca M, Bandecchi P. Generation of Virus like Particles for Epizootic Hemorrhagic Disease Virus. Res. Vet. Sci. 2016;107:116–122.
- De la Poza F, Calvo-Pinilla E, López-Gil E, Marín-López A, Mateos F, Castillo-Olivares J, Lorenzo G, Ortego J. Ns1 Is a Key Protein in the Vaccine Composition to Protect Ifnar(−/−) Mice against Infection with Multiple Serotypes of African Horse Sickness Virus. PLoS ONE 2013;8:e0070197.
- Marín-Lopez A, Calvo-Pinilla E, Moreno S, Utrilla-Trigo S, Nogales A, Brun A, Ortego J. Modeling Arboviral Infection in Mice Lacking the Interferon Alpha/Beta Receptor. Viruses 2019;11:35.
- Marín-López A, Bermúdez R, Calvo-Pinilla E, Moreno S, Brun A, Ortego J. Pathological Characterization of IFNAR(−/−) Mice Infected With Bluetongue Virus Serotype 4. Int. J. Biol. Sci. 2016;12:1448–1460.
- Calvo-Pinilla E, Rodríguez-Calvo T, Anguita J, Sevilla N, Ortego J. Establishment of a Bluetongue Virus Infection Model in Mice That Are Deficient in the Alpha/Beta Interferon Receptor. PLoS ONE 2009;4:e5171.
- Eschbaumer M, Keller M, Beer M, Hoffmann B. Epizootic Hemorrhagic Disease Virus Infection of Type I Interferon Receptor Deficient Mice. Vet. Microbiol. 2012;155:417–419.
Citations
This article has been cited 11 times.- Jurado S, Jiménez-Cabello L, Nuñez MDC, Utrilla-Trigo S, Calvo-Pinilla E, Mazuecos-Aragonés I, Gutierrez JR, Falcón A, Ortego J, Escribano JM. Structure-Guided Engineering of Protein VP2 from Epizootic Hemorrhagic Disease Virus Maximizes Production and Confers Complete Protection as Subunit Vaccine. Vaccines (Basel) 2025 Dec 20;14(1).
- Jiménez-Cabello L, Utrilla-Trigo S, Illescas-Amo M, Rodríguez-Sabando K, Benavides-Silván J, Calvo-Pinilla E, Ortego J. The MVA-VP2-NS1-2A-NS2-Nt vaccine candidate provides heterologous protection in sheep against bluetongue virus. Front Immunol 2025;16:1566225.
- Calvo-Pinilla E, Moreno S, Barreiro-Piñeiro N, Sánchez-Puig JM, Blasco R, Martínez-Costas J, Brun A, Lorenzo G. Prime-Boost Vaccination Based on Nanospheres and MVA Encoding the Nucleoprotein of Crimean-Congo Hemorrhagic Fever Virus Elicits Broad Immune Responses. Vaccines (Basel) 2025 Mar 10;13(3).
- Wang X, Yu G. Advancing veterinary vaccines design through trained immunity insights. Front Vet Sci 2024;11:1524668.
- Barua S, Rana EA, Prodhan MA, Akter SH, Gogoi-Tiwari J, Sarker S, Annandale H, Eagles D, Abraham S, Uddin JM. The Global Burden of Emerging and Re-Emerging Orbiviruses in Livestock: An Emphasis on Bluetongue Virus and Epizootic Hemorrhagic Disease Virus. Viruses 2024 Dec 26;17(1).
- Jiménez-Cabello L, Utrilla-Trigo S, Rodríguez-Sabando K, Carra-Valenzuela A, Illescas-Amo M, Calvo-Pinilla E, Ortego J. Vaccine candidates based on MVA viral vectors expressing VP2 or VP7 confer full protection against Epizootic hemorrhagic disease virus in IFNAR(-/-) mice. J Virol 2024 Dec 17;98(12):e0168724.
- Jiménez-Cabello L, Utrilla-Trigo S, Calvo-Pinilla E, Lorenzo G, Illescas-Amo M, Benavides J, Moreno S, Marín-López A, Nogales A, Ortego J. Co-expression of VP2, NS1 and NS2-Nt proteins by an MVA viral vector induces complete protection against bluetongue virus. Front Immunol 2024;15:1440407.
- Jiménez-Cabello L, Utrilla-Trigo S, Benavides-Silván J, Anguita J, Calvo-Pinilla E, Ortego J. IFNAR(-/-) Mice Constitute a Suitable Animal Model for Epizootic Hemorrhagic Disease Virus Study and Vaccine Evaluation. Int J Biol Sci 2024;20(8):3076-3093.
- Calvo-Pinilla E, Jiménez-Cabello L, Utrilla-Trigo S, Illescas-Amo M, Ortego J. Cytokine mRNA Expression Profile in Target Organs of IFNAR (-/-) Mice Infected with African Horse Sickness Virus. Int J Mol Sci 2024 Feb 8;25(4).
- Utrilla-Trigo S, Jiménez-Cabello L, Marín-López A, Illescas-Amo M, Andrés G, Calvo-Pinilla E, Lorenzo G, van Rijn PA, Ortego J, Nogales A. Engineering recombinant replication-competent bluetongue viruses expressing reporter genes for in vitro and non-invasive in vivo studies. Microbiol Spectr 2024 Mar 5;12(3):e0249323.
- Jiménez-Cabello L, Utrilla-Trigo S, Lorenzo G, Ortego J, Calvo-Pinilla E. Epizootic Hemorrhagic Disease Virus: Current Knowledge and Emerging Perspectives. Microorganisms 2023 May 19;11(5).
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