Analyze Diet
Pathogens (Basel, Switzerland)2022; 11(12); 1478; doi: 10.3390/pathogens11121478

Differential Expression of Immune Genes in the Rhipicephalus microplus Gut in Response to Theileria equi Infection.

Abstract: is the only tick species known to serve as a biological vector of for horses and other equids in Brazil. The protozoan is one of the causal agents of equine piroplasmosis, a major threat in horse breeding systems. Vector competence is closely linked to the pathogens' ability to evade tick defense mechanisms. However, knowledge of tick immune response against infections by hemoparasites of the genus is scarce. In the present study, the expression of genes involved in immune signaling pathways of adults' guts when challenged with a high or low parasitic load of was evaluated. This research demonstrates divergences in the immune gene expression pattern linked to infection in since the Toll, IMD, and JNK signaling pathways were transcriptionally repressed in the guts of adult ticks infected with . Moreover, the results showed that different infectious doses of induce differential gene expression of key components of immune signaling cascades in gut, suggesting a link between the intensity of infection and the activation of tick immunity response. The present study adds knowledge to elucidate the gut immune signaling response of to infection. In addition, the generated data can serve as a basis for further investigations to develop strategies for controlling and preventing equine piroplasmosis.
Publication Date: 2022-12-06 PubMed ID: 36558812PubMed Central: PMC9782190DOI: 10.3390/pathogens11121478Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research study focuses on how tick defense mechanisms respond to Theileria equi, a parasite implicated in equine piroplasmosis, a significant threat to horse breeding in Brazil. The study particularly investigates the patterns of immune gene expression in the gut of adult Rhipicephalus microplus ticks when exposed to different parasitic loads of the protozoan.

Objective and Background of the Study

  • The study revolves around Rhipicephalus microplus, a tick species known as the principal vector for Theileria equi, a harmful parasite that instigates equine piroplasmosis. This disease poses a serious hazard to horse breeding programs, especially in Brazil.
  • The effectiveness of the tick as a vector is linked to the ability of the pathogen to evade the tick’s defense mechanisms, implying that the tick’s immune response plays a significant role in the spread of the disease.
  • Given this implication, the study sought to fill the knowledge gap associated with the tick’s immune response by assessing the expression of genes involved in its immune signaling pathways when challenged with varying levels of Theileria equi infection.

Methods and Findings

  • The researchers investigated the effect of different parasitic loads of Theileria equi on the gut gene expression in adult Rhipicephalus microplus ticks.
  • The study revealed that immune gene expression varies according to the intensity of Theileria equi infection. Specifically, immune signaling pathways like Toll, IMD, and JNK were transcriptionally repressed in infected ticks’ guts.
  • It was found out that different infectious doses of Theileria equi could induce differential gene expression of crucial components of immune signaling cascades.

Significance and Implications of the Research

  • The research is key in enhancing the understanding of the gut immune signaling response of Rhipicephalus microplus ticks to Theileria equi infection.
  • The findings underscore the link between the severity of infection and activation of the tick’s immunity response. As such, the study adds to the pool of knowledge that can be used to inform strategies aimed at controlling and preventing equine piroplasmosis.
  • The dataset generated from the study can act as a basis for additional investigations towards developing effective control and preventative measures against this disease.

Cite This Article

APA
Paulino PG, Peckle M, Mendonça LP, Massard CL, Antunes S, Couto J, Domingos A, Guedes Junior DDS, Cabezas-Cruz A, Santos HA. (2022). Differential Expression of Immune Genes in the Rhipicephalus microplus Gut in Response to Theileria equi Infection. Pathogens, 11(12), 1478. https://doi.org/10.3390/pathogens11121478

Publication

ISSN: 2076-0817
NlmUniqueID: 101596317
Country: Switzerland
Language: English
Volume: 11
Issue: 12
PII: 1478

Researcher Affiliations

Paulino, Patrícia Gonzaga
  • Department of Epidemiology and Public Health, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil.
Peckle, Maristela
  • Department of Animal Parasitology, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil.
Mendonça, Leo Paulis
  • Department of Epidemiology and Public Health, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil.
Massard, Carlos Luiz
  • Department of Animal Parasitology, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil.
Antunes, Sandra
  • Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, 1349-008 Lisboa, Portugal.
Couto, Joana
  • Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, 1349-008 Lisboa, Portugal.
Domingos, Ana
  • Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, 1349-008 Lisboa, Portugal.
Guedes Junior, Daniel da Silva
  • Vaccine Complex, Quality Department-Biomolecular and Immunocytochemistry Tests Section, FIOCRUZ, Rio de Janeiro 21040-900, Brazil.
Cabezas-Cruz, Alejandro
  • UMR BIPAR INRAE-ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France.
Santos, Huarrisson Azevedo
  • Department of Epidemiology and Public Health, Federal Rural University of Rio de Janeiro (UFRRJ), Seropedica 23890-000, Brazil.

Grant Funding

  • E-26/201.342/2021 / Fundau00e7u00e3o Carlos Chagas Filho de Amparo u00e0 Pesquisa do Estado do Rio de Janeiro
  • 313753/2021-0 / National Council for Scientific and Technological Development

Conflict of Interest Statement

The authors declare no conflict of interest. The funding sponsors had no role in the study’s design, experimental procedures, analyses, interpretation of data, writing of the manuscript, or decision to publish the results.

References

This article includes 40 references
  1. Tirosh-Levy S, Gottlieb Y, Fry LM, Knowles DP, Steinman A. Twenty Years of Equine Piroplasmosis Research: Global Distribution, Molecular Diagnosis, and Phylogeny.. Pathogens 2020 Nov 8;9(11).
    doi: 10.3390/pathogens9110926pmc: PMC7695325pubmed: 33171698google scholar: lookup
  2. Sears K, Knowles D, Dinkel K, Mshelia PW, Onzere C, Silva M, Fry L. Imidocarb Dipropionate Lacks Efficacy against Theileria haneyi and Fails to Consistently Clear Theileria equi in Horses Co-Infected with T. haneyi.. Pathogens 2020 Dec 10;9(12).
    doi: 10.3390/pathogens9121035pmc: PMC7764667pubmed: 33321715google scholar: lookup
  3. Friedhoff KT, Tenter AM, Müller I. Haemoparasites of equines: impact on international trade of horses.. Rev Sci Tech 1990 Dec;9(4):1187-94.
    pubmed: 2132711
  4. Ikadai H, Sasaki M, Ishida H, Matsuu A, Igarashi I, Fujisaki K, Oyamada T. Molecular evidence of Babesia equi transmission in Haemaphysalis longicornis.. Am J Trop Med Hyg 2007 Apr;76(4):694-7.
    doi: 10.4269/ajtmh.2007.76.694pubmed: 17426172google scholar: lookup
  5. Scoles GA, Ueti MW. Vector ecology of equine piroplasmosis.. Annu Rev Entomol 2015 Jan 7;60:561-80.
  6. Guimarães AM, Lima JD, Ribeiro MF, Camargos ER, Bozzi IA. Ultrastructure of sporogony in Babesia equi in salivary glands of adult female Boophilus microplus ticks.. Parasitol Res 1998;84(1):69-74.
    doi: 10.1007/s004360050359pubmed: 9491430google scholar: lookup
  7. Guimarães AM, Lima JD, Ribeiro MF. Sporogony and experimental transmission of Babesia equi by Boophilus microplus.. Parasitol Res 1998;84(4):323-7.
    doi: 10.1007/s004360050404pubmed: 9580425google scholar: lookup
  8. Peckle M, Santos H, Pires M, Silva C, Costa R, Vitari G, Camilo T, Meireles N, Paulino P, Massard C. Dynamics of Theileria equi Infection in Rhipicephalus (Boophilus) microplus during the Parasitic Phase in a Chronically Infected Horse.. Pathogens 2022 Apr 29;11(5).
    doi: 10.3390/pathogens11050525pmc: PMC9142995pubmed: 35631046google scholar: lookup
  9. Kopácek P, Hajdusek O, Buresová V, Daffre S. Tick innate immunity.. Adv Exp Med Biol 2010;708:137-62.
    doi: 10.1007/978-1-4419-8059-5_8pubmed: 21528697google scholar: lookup
  10. Fogaça AC, Sousa G, Pavanelo DB, Esteves E, Martins LA, Urbanová V, Kopáček P, Daffre S. Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges.. Front Immunol 2021;12:628054.
    doi: 10.3389/fimmu.2021.628054pmc: PMC7962413pubmed: 33737931google scholar: lookup
  11. Shaw DK, Wang X, Brown LJ, Chávez AS, Reif KE, Smith AA, Scott AJ, McClure EE, Boradia VM, Hammond HL, Sundberg EJ, Snyder GA, Liu L, DePonte K, Villar M, Ueti MW, de la Fuente J, Ernst RK, Pal U, Fikrig E, Pedra JH. Infection-derived lipids elicit an immune deficiency circuit in arthropods.. Nat Commun 2017 Feb 14;8:14401.
    doi: 10.1038/ncomms14401pmc: PMC5316886pubmed: 28195158google scholar: lookup
  12. Aguilar-Díaz H, Quiroz-Castañeda RE, Salazar-Morales K, Cossío-Bayúgar R, Miranda-Miranda E. Tick Immunobiology and Extracellular Traps: An Integrative Vision to Control of Vectors.. Pathogens 2021 Nov 19;10(11).
    doi: 10.3390/pathogens10111511pmc: PMC8621429pubmed: 34832666google scholar: lookup
  13. Rosa RD, Capelli-Peixoto J, Mesquita RD, Kalil SP, Pohl PC, Braz GR, Fogaça AC, Daffre S. Exploring the immune signalling pathway-related genes of the cattle tick Rhipicephalus microplus: From molecular characterization to transcriptional profile upon microbial challenge.. Dev Comp Immunol 2016 Jun;59:1-14.
    doi: 10.1016/j.dci.2015.12.018pubmed: 26724380google scholar: lookup
  14. Capelli-Peixoto J, Carvalho DD, Johnson WC, Scoles GA, Fogaça AC, Daffre S, Ueti MW. The transcription factor Relish controls Anaplasma marginale infection in the bovine tick Rhipicephalus microplus.. Dev Comp Immunol 2017 Sep;74:32-39.
    doi: 10.1016/j.dci.2017.04.005pubmed: 28408334google scholar: lookup
  15. Liu L, Dai J, Zhao YO, Narasimhan S, Yang Y, Zhang L, Fikrig E. Ixodes scapularis JAK-STAT pathway regulates tick antimicrobial peptides, thereby controlling the agent of human granulocytic anaplasmosis.. J Infect Dis 2012 Oct;206(8):1233-41.
    doi: 10.1093/infdis/jis484pmc: PMC3448968pubmed: 22859824google scholar: lookup
  16. Baldani CD, Machado RZ, Botteon PDTL, Takakura FS, Massard CL. An enzyme-linked immunosorbent assay for the detection of IgG antibodies against Babesia equi in horses.. Ciência Rural 2004;34:1525–1529.
  17. Paulino P, Vitari G, Rezende A, Couto J, Antunes S, Domingos A, Peckle M, Massard C, Araújo F, Santos H. Characterization of the Rhipicephalus (Boophilus) microplus Sialotranscriptome Profile in Response to Theileria equi Infection.. Pathogens 2021 Feb 4;10(2).
    doi: 10.3390/pathogens10020167pmc: PMC7913801pubmed: 33557100google scholar: lookup
  18. Reck J Jr, Berger M, Terra RM, Marks FS, da Silva Vaz I Jr, Guimarães JA, Termignoni C. Systemic alterations of bovine hemostasis due to Rhipicephalus (Boophilus) microplus infestation.. Res Vet Sci 2009 Feb;86(1):56-62.
    doi: 10.1016/j.rvsc.2008.05.007pubmed: 18571684google scholar: lookup
  19. Ceci L, Carelli G, Boscia D, Lacinio R. The effect of corticosteroid administration on the pathogenicity of Babesia equi infection in horses [Campania]. Atti della Societa Italiana delle Scienze Veterinarie 1997;51:543–544.
  20. Oladosu LA. Effects of intravenous corticosteroid on the pathogenicity of Babesia equi infection of donkeys (Equus asinus).. Zentralbl Veterinarmed B 1988 Aug;35(7):509-14.
  21. Antunes S, Galindo RC, Almazán C, Rudenko N, Golovchenko M, Grubhoffer L, Shkap V, do Rosário V, de la Fuente J, Domingos A. Functional genomics studies of Rhipicephalus (Boophilus) annulatus ticks in response to infection with the cattle protozoan parasite, Babesia bigemina.. Int J Parasitol 2012 Feb;42(2):187-95.
    doi: 10.1016/j.ijpara.2011.12.003pubmed: 22265898google scholar: lookup
  22. Edwards KT, Goddard J, Varela-Stokes AS. Examination of the internal morphology of the Ixodid tick, Amblyomma maculatum Koch,(Acari: Ixodidae); a “how-to” pictorial dissection guide.. Midsouth Entomol 2009;2:28–39.
  23. Kim CM, Blanco LB, Alhassan A, Iseki H, Yokoyama N, Xuan X, Igarashi I. Diagnostic real-time PCR assay for the quantitative detection of Theileria equi from equine blood samples.. Vet Parasitol 2008 Feb 14;151(2-4):158-63.
    doi: 10.1016/j.vetpar.2007.10.023pubmed: 18077095google scholar: lookup
  24. Nijhof AM, Balk JA, Postigo M, Jongejan F. Selection of reference genes for quantitative RT-PCR studies in Rhipicephalus (Boophilus) microplus and Rhipicephalus appendiculatus ticks and determination of the expression profile of Bm86.. BMC Mol Biol 2009 Dec 29;10:112.
    doi: 10.1186/1471-2199-10-112pmc: PMC2809063pubmed: 20040102google scholar: lookup
  25. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.. Clin Chem 2009 Apr;55(4):611-22.
    doi: 10.1373/clinchem.2008.112797pubmed: 19246619google scholar: lookup
  26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods 2001 Dec;25(4):402-8.
    doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
  27. Zhang G, Ghosh S. Negative regulation of toll-like receptor-mediated signaling by Tollip.. J Biol Chem 2002 Mar 1;277(9):7059-65.
    doi: 10.1074/jbc.M109537200pubmed: 11751856google scholar: lookup
  28. Kopp E, Medzhitov R, Carothers J, Xiao C, Douglas I, Janeway CA, Ghosh S. ECSIT is an evolutionarily conserved intermediate in the Toll/IL-1 signal transduction pathway.. Genes Dev 1999 Aug 15;13(16):2059-71.
    doi: 10.1101/gad.13.16.2059pmc: PMC316957pubmed: 10465784google scholar: lookup
  29. Chakraborty S, Roy S, Mistry HU, Murthy S, George N, Bhandari V, Sharma P. Potential Sabotage of Host Cell Physiology by Apicomplexan Parasites for Their Survival Benefits.. Front Immunol 2017;8:1261.
    doi: 10.3389/fimmu.2017.01261pmc: PMC5645534pubmed: 29081773google scholar: lookup
  30. Lee FS, Peters RT, Dang LC, Maniatis T. MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta.. Proc Natl Acad Sci U S A 1998 Aug 4;95(16):9319-24.
    doi: 10.1073/pnas.95.16.9319pmc: PMC21336pubmed: 9689078google scholar: lookup
  31. Silverman N, Zhou R, Stöven S, Pandey N, Hultmark D, Maniatis T. A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity.. Genes Dev 2000 Oct 1;14(19):2461-71.
    doi: 10.1101/gad.817800pmc: PMC316979pubmed: 11018014google scholar: lookup
  32. Tsapras P, Petridi S, Chan S, Geborys M, Jacomin AC, Sagona AP, Meier P, Nezis IP. Selective autophagy controls innate immune response through a TAK1/TAB2/SH3PX1 axis.. Cell Rep 2022 Jan 25;38(4):110286.
    doi: 10.1016/j.celrep.2021.110286pubmed: 35081354google scholar: lookup
  33. Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E, Schneider D, Maniatis T. Immune activation of NF-kappaB and JNK requires Drosophila TAK1.. J Biol Chem 2003 Dec 5;278(49):48928-34.
    doi: 10.1074/jbc.M304802200pubmed: 14519762google scholar: lookup
  34. Tsuda M, Langmann C, Harden N, Aigaki T. The RING-finger scaffold protein Plenty of SH3s targets TAK1 to control immunity signalling in Drosophila.. EMBO Rep 2005 Nov;6(11):1082-7.
    doi: 10.1038/sj.embor.7400537pmc: PMC1371032pubmed: 16179944google scholar: lookup
  35. Park JM, Brady H, Ruocco MG, Sun H, Williams D, Lee SJ, Kato T Jr, Richards N, Chan K, Mercurio F, Karin M, Wasserman SA. Targeting of TAK1 by the NF-kappa B protein Relish regulates the JNK-mediated immune response in Drosophila.. Genes Dev 2004 Mar 1;18(5):584-94.
    doi: 10.1101/gad.1168104pmc: PMC374239pubmed: 15037551google scholar: lookup
  36. Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila.. Science 2008 Feb 8;319(5864):777-82.
    doi: 10.1126/science.1149357pubmed: 18218863google scholar: lookup
  37. Clayton AM, Cirimotich CM, Dong Y, Dimopoulos G. Caudal is a negative regulator of the Anopheles IMD pathway that controls resistance to Plasmodium falciparum infection.. Dev Comp Immunol 2013 Apr;39(4):323-32.
    doi: 10.1016/j.dci.2012.10.009pmc: PMC3892953pubmed: 23178401google scholar: lookup
  38. Lizundia R, Chaussepied M, Huerre M, Werling D, Di Santo JP, Langsley G. c-Jun NH2-terminal kinase/c-Jun signaling promotes survival and metastasis of B lymphocytes transformed by Theileria.. Cancer Res 2006 Jun 15;66(12):6105-10.
    doi: 10.1158/0008-5472.CAN-05-3861pubmed: 16778183google scholar: lookup
  39. Kershaw NJ, Murphy JM, Liau NP, Varghese LN, Laktyushin A, Whitlock EL, Lucet IS, Nicola NA, Babon JJ. SOCS3 binds specific receptor-JAK complexes to control cytokine signaling by direct kinase inhibition.. Nat Struct Mol Biol 2013 Apr;20(4):469-76.
    doi: 10.1038/nsmb.2519pmc: PMC3618588pubmed: 23454976google scholar: lookup
  40. Ueti MW, Palmer GH, Scoles GA, Kappmeyer LS, Knowles DP. Persistently infected horses are reservoirs for intrastadial tick-borne transmission of the apicomplexan parasite Babesia equi.. Infect Immun 2008 Aug;76(8):3525-9.
    doi: 10.1128/IAI.00251-08pmc: PMC2493223pubmed: 18490466google scholar: lookup

Citations

This article has been cited 0 times.