FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Virology / Infectious entry of equine herpesvirus-1 into host cells thr...
Virology2009; 393(2); 198-209; doi: 10.1016/j.virol.2009.07.032

Infectious entry of equine herpesvirus-1 into host cells through different endocytic pathways.

Abstract: We investigated the mechanism by which equine herpesvirus-1 (EHV-1) enters primary cultured equine brain microvascular endothelial cells (EBMECs) and equine dermis (E. Derm) cells. EHV-1 colocalized with caveolin in EBMECs and the infection was greatly reduced by the expression of a dominant negative form of equine caveolin-1 (ecavY14F), suggesting that EHV-1 enters EBMECs via caveolar endocytosis. EHV-1 entry into E. Derm cells was significantly reduced by ATP depletion and treatments with lysosomotropic agents. Enveloped virions were detected from E. Derm cells by infectious virus recovery assay after viral internalization, suggesting that EHV-1 enters E. Derm cells via energy- and pH-dependent endocytosis. These results suggest that EHV-1 utilizes multiple endocytic pathways in different cell types to establish productive infection.
Get Full Text
Publication Date: 2009-08-31 PubMed ID: 19720389PubMed Central: PMC7111996DOI: 10.1016/j.virol.2009.07.032Google 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.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 investigates how the equine herpesvirus-1 (EHV-1) enters certain types of equine cells — specifically, brain microvascular endothelial cells and dermis cells. The findings indicate that EHV-1 uses various methods of endocytosis to infect different cell types.

Research Context

  • This study focuses on understanding how equine herpesvirus-1 (EHV-1) enters host cells. EHV-1 is a virus that affects horses and can cause a variety of diseases, such as respiratory disease, abortion, and neurological disease.
  • The researchers investigated this infection process in two types of equine cells: brain microvascular endothelial cells (termed EBMECs) and dermis cells (referred as E. Derm cells). Both cells are part of the horse’s natural environment for EHV-1.

Methodology and Findings

  • The researchers tested whether EHV-1 was spotted with a protein called caveolin in EBMECs. When viruses enter cells via “caveolar endocytosis,” they often use caveolin as a marker.
  • By using a modified form of caveolin, called “ecavY14F,” which inhibits the normal function of caveolin, they found that the EBMEC infection rate dropped dramatically. This suggests that EHV-1 primarily uses “caveolar endocytosis” to enter EBMECs.
  • The entry of EHV-1 into E. Derm cells was tested differently. The researchers lowered ATP levels and used lysosomotropic agents – both methods to disrupt endocytosis. As the infection rate dropped significantly after these measures, it implies that EHV-1 uses an “energy- and pH-dependent endocytosis” to enter these cells.
  • They also detected virus particles in E. Derm cells after it had been taken up by the cell, further reinforcing that EHV-1 uses endocytosis to enter these cells.

Conclusion

  • The findings underscore that EHV-1 uses multiple pathways to enter different types of cells, a characteristic feature of many viruses that can complicate development of vaccines or treatments.
  • Further research would help identify if other cell types also show this versatility and how these endocytic pathways can be potentially inhibited to prevent EHV-1 infections.

Cite This Article

APA
Hasebe R, Sasaki M, Sawa H, Wada R, Umemura T, Kimura T. (2009). Infectious entry of equine herpesvirus-1 into host cells through different endocytic pathways. Virology, 393(2), 198-209. https://doi.org/10.1016/j.virol.2009.07.032

Publication

Virology
ISSN: 1096-0341
NlmUniqueID: 0110674
Country: United States
Language: English
Volume: 393
Issue: 2
Pages: 198-209

Researcher Affiliations

Hasebe, Rie
  • Laboratory of Prion Diseases, Graduate School of Veterinary Medicine, Hokkaido University, West 9 North 18, Kita-ku, Sapporo 060-0818, Japan. r-hasebe@vetmed.hokudai.ac.jp
Sasaki, Michihito
    Sawa, Hirofumi
      Wada, Ryuichi
        Umemura, Takashi
          Kimura, Takashi

            MeSH Terms

            • Animals
            • Caveolin 1 / genetics
            • Caveolin 1 / metabolism
            • Cell Line
            • Endocytosis
            • Endothelial Cells / virology
            • Herpesviridae Infections / veterinary
            • Herpesviridae Infections / virology
            • Herpesvirus 1, Equid / growth & development
            • Herpesvirus 1, Equid / physiology
            • Horse Diseases / virology
            • Horses
            • Hydrogen-Ion Concentration
            • Microscopy, Confocal
            • Protein-Tyrosine Kinases / metabolism
            • Transgenes
            • Virus Internalization

            References

            This article includes 59 references
            1. Abodeely RA, Lawson LA, Randall CC. Morphology and entry of enveloped and deenveloped equine abortion (herpes) virus.. J Virol 1970 Apr;5(4):513-23.
              pmc: PMC376034pubmed: 4195054doi: 10.1128/jvi.5.4.513-523.1970google scholar: lookup
            2. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases.. J Biol Chem 1987 Apr 25;262(12):5592-5.
              pubmed: 3106339
            3. Anderson RG. The caveolae membrane system.. Annu Rev Biochem 1998;67:199-225.
              pubmed: 9759488doi: 10.1146/annurev.biochem.67.1.199google scholar: lookup
            4. Anderson HA, Chen Y, Norkin LC. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae.. Mol Biol Cell 1996 Nov;7(11):1825-34.
              pmc: PMC276029pubmed: 8930903doi: 10.1091/mbc.7.11.1825google scholar: lookup
            5. Aoki T, Nomura R, Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium.. Exp Cell Res 1999 Dec 15;253(2):629-36.
              pubmed: 10585286doi: 10.1006/excr.1999.4652google scholar: lookup
            6. Ashok A, Atwood WJ. Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40.. J Virol 2003 Jan;77(2):1347-56.
              pmc: PMC140837pubmed: 12502851doi: 10.1128/jvi.77.2.1347-1356.2003google scholar: lookup
            7. Blumenthal R, Bali-Puri A, Walter A, Covell D, Eidelman O. pH-dependent fusion of vesicular stomatitis virus with Vero cells. Measurement by dequenching of octadecyl rhodamine fluorescence.. J Biol Chem 1987 Oct 5;262(28):13614-9.
              pubmed: 2820977
            8. Bousarghin L, Touzé A, Sizaret PY, Coursaget P. Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells.. J Virol 2003 Mar;77(6):3846-50.
              pmc: PMC149499pubmed: 12610160doi: 10.1128/jvi.77.6.3846-3850.2003google scholar: lookup
            9. Campadelli-Fiume G, Arsenakis M, Farabegoli F, Roizman B. Entry of herpes simplex virus 1 in BJ cells that constitutively express viral glycoprotein D is by endocytosis and results in degradation of the virus.. J Virol 1988 Jan;62(1):159-67.
              pmc: PMC250514pubmed: 2824844doi: 10.1128/jvi.62.1.159-167.1988google scholar: lookup
            10. Caughman GB, Staczek J, O'Callaghan DJ. Equine herpesvirus type 1 infected cell polypeptides: evidence for immediate early/early/late regulation of viral gene expression.. Virology 1985 Aug;145(1):49-61.
              pubmed: 2990102doi: 10.1016/0042-6822(85)90200-4google scholar: lookup
            11. Chen Y, Norkin LC. Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae.. Exp Cell Res 1999 Jan 10;246(1):83-90.
              pubmed: 9882517doi: 10.1006/excr.1998.4301google scholar: lookup
            12. Colin M, Mailly L, Rogée S, D'Halluin JC. Efficient species C HAdV infectivity in plasmocytic cell lines using a clathrin-independent lipid raft/caveola endocytic route.. Mol Ther 2005 Feb;11(2):224-36.
              pubmed: 15668134doi: 10.1016/j.ymthe.2004.10.007google scholar: lookup
            13. Dröse S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases.. J Exp Biol 1997 Jan;200(Pt 1):1-8.
              pubmed: 9023991doi: 10.1242/jeb.200.1.1google scholar: lookup
            14. Eash S, Querbes W, Atwood WJ. Infection of vero cells by BK virus is dependent on caveolae.. J Virol 2004 Nov;78(21):11583-90.
              pmc: PMC523296pubmed: 15479799doi: 10.1128/jvi.78.21.11583-11590.2004google scholar: lookup
            15. Edington N, Bridges CG, Patel JR. Endothelial cell infection and thrombosis in paralysis caused by equid herpesvirus-1: equine stroke.. Arch Virol 1986;90(1-2):111-24.
              pubmed: 3015074doi: 10.1007/bf01314149google scholar: lookup
            16. Empig CJ, Goldsmith MA. Association of the caveola vesicular system with cellular entry by filoviruses.. J Virol 2002 May;76(10):5266-70.
              pmc: PMC136134pubmed: 11967340doi: 10.1128/jvi.76.10.5266-5270.2002google scholar: lookup
            17. Frampton AR Jr, Smith PM, Zhang Y, Matsumura T, Osterrieder N, O'Callaghan DJ. Contribution of gene products encoded within the unique short segment of equine herpesvirus 1 to virulence in a murine model.. Virus Res 2002 Dec;90(1-2):287-301.
              pubmed: 12457983doi: 10.1016/s0168-1702(02)00245-9google scholar: lookup
            18. Frampton AR Jr, Stolz DB, Uchida H, Goins WF, Cohen JB, Glorioso JC. Equine herpesvirus 1 enters cells by two different pathways, and infection requires the activation of the cellular kinase ROCK1.. J Virol 2007 Oct;81(20):10879-89.
              pmc: PMC2045510pubmed: 17670830doi: 10.1128/jvi.00504-07google scholar: lookup
            19. Fuller AO, Spear PG. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface.. Proc Natl Acad Sci U S A 1987 Aug;84(15):5454-8.
              pmc: PMC298876pubmed: 3037552doi: 10.1073/pnas.84.15.5454google scholar: lookup
            20. Fuller AO, Lee WC. Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration.. J Virol 1992 Aug;66(8):5002-12.
              pmc: PMC241354pubmed: 1321283doi: 10.1128/jvi.66.8.5002-5012.1992google scholar: lookup
            21. Fuller AO, Santos RE, Spear PG. Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration.. J Virol 1989 Aug;63(8):3435-43.
              pmc: PMC250919pubmed: 2545914doi: 10.1128/jvi.63.8.3435-3443.1989google scholar: lookup
            22. Gilbert J, Benjamin T. Uptake pathway of polyomavirus via ganglioside GD1a.. J Virol 2004 Nov;78(22):12259-67.
              pmc: PMC525080pubmed: 15507613doi: 10.1128/jvi.78.22.12259-12267.2004google scholar: lookup
            23. Gilbert JM, Goldberg IG, Benjamin TL. Cell penetration and trafficking of polyomavirus.. J Virol 2003 Feb;77(4):2615-22.
              pmc: PMC141103pubmed: 12552000doi: 10.1128/jvi.77.4.2615-2622.2003google scholar: lookup
            24. Greenberg S, Chang P, Silverstein SC. Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages.. J Exp Med 1993 Feb 1;177(2):529-34.
              pmc: PMC2190886pubmed: 7678851doi: 10.1084/jem.177.2.529google scholar: lookup
            25. Hasebe R, Kimura T, Nakamura K, Ochiai K, Okazaki K, Wada R, Umemura T. Differential susceptibility of equine and mouse brain microvascular endothelial cells to equine herpesvirus 1 infection.. Arch Virol 2006 Apr;151(4):775-86.
              pubmed: 16328147doi: 10.1007/s00705-005-0653-3google scholar: lookup
            26. Helenius A, Kartenbeck J, Simons K, Fries E. On the entry of Semliki forest virus into BHK-21 cells.. J Cell Biol 1980 Feb;84(2):404-20.
              pmc: PMC2110562pubmed: 6991511doi: 10.1083/jcb.84.2.404google scholar: lookup
            27. Helenius A, Marsh M, White J. Inhibition of Semliki forest virus penetration by lysosomotropic weak bases.. J Gen Virol 1982 Jan;58 Pt 1:47-61.
              pubmed: 7142969doi: 10.1099/0022-1317-58-1-47google scholar: lookup
            28. Ibrahim el SM, Pagmajav O, Yamaguchi T, Matsumura T, Fukushi H. Growth and virulence alterations of equine herpesvirus 1 by insertion of a green fluorescent protein gene in the intergenic region between ORFs 62 and 63.. Microbiol Immunol 2004;48(11):831-42.
              pubmed: 15557741doi: 10.1111/j.1348-0421.2004.tb03615.xgoogle scholar: lookup
            29. Joó F. Endothelial cells of the brain and other organ systems: some similarities and differences.. Prog Neurobiol 1996 Feb;48(3):255-73.
              pubmed: 8735879doi: 10.1016/0301-0082(95)00046-1google scholar: lookup
            30. Kawakami Y, Tokui T, Nakano K, Kume T, Hiramune T, Murase N. An outbreak of abortion due to equine rhinopneumonitis virus among mares in the Hidaka district, Hokkaido. I. Epizootiological survey and virus isolation.. Bull. Natl. Inst. Anim. Hlth. 1970;61:9–16.
            31. Kimura T, Hasebe R, Mukaiya R, Ochiai K, Wada R, Umemura T. Decreased expression of equine herpesvirus-1 early and late genes in the placenta of naturally aborted equine fetuses.. J Comp Pathol 2004 Jan;130(1):41-7.
              pubmed: 14693123doi: 10.1016/s0021-9975(03)00068-9google scholar: lookup
            32. Lamaze C, Baba T, Redelmeier TE, Schmid SL. Recruitment of epidermal growth factor and transferrin receptors into coated pits in vitro: differing biochemical requirements.. Mol Biol Cell 1993 Jul;4(7):715-27.
              pmc: PMC300981pubmed: 8400457doi: 10.1091/mbc.4.7.715google scholar: lookup
            33. Li Q, Ali MA, Cohen JI. Insulin degrading enzyme is a cellular receptor mediating varicella-zoster virus infection and cell-to-cell spread.. Cell 2006 Oct 20;127(2):305-16.
              pmc: PMC7125743pubmed: 17055432doi: 10.1016/j.cell.2006.08.046google scholar: lookup
            34. Marjomäki V, Pietiäinen V, Matilainen H, Upla P, Ivaska J, Nissinen L, Reunanen H, Huttunen P, Hyypiä T, Heino J. Internalization of echovirus 1 in caveolae.. J Virol 2002 Feb;76(4):1856-65.
              pmc: PMC135881pubmed: 11799180doi: 10.1128/jvi.76.4.1856-1865.2002google scholar: lookup
            35. Matlin KS, Reggio H, Helenius A, Simons K. Infectious entry pathway of influenza virus in a canine kidney cell line.. J Cell Biol 1981 Dec;91(3 Pt 1):601-13.
              pmc: PMC2112819pubmed: 7328111doi: 10.1083/jcb.91.3.601google scholar: lookup
            36. Matlin KS, Reggio H, Helenius A, Simons K. Pathway of vesicular stomatitis virus entry leading to infection.. J Mol Biol 1982 Apr 15;156(3):609-31.
              pubmed: 6288961doi: 10.1016/0022-2836(82)90269-8google scholar: lookup
            37. McPherson PS, Kay BK, Hussain NK. Signaling on the endocytic pathway.. Traffic 2001 Jun;2(6):375-84.
              pubmed: 11389765doi: 10.1034/j.1600-0854.2001.002006375.xgoogle scholar: lookup
            38. Milne RS, Nicola AV, Whitbeck JC, Eisenberg RJ, Cohen GH. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1.. J Virol 2005 Jun;79(11):6655-63.
              pmc: PMC1112142pubmed: 15890903doi: 10.1128/jvi.79.11.6655-6663.2005google scholar: lookup
            39. Nichols B. Caveosomes and endocytosis of lipid rafts.. J Cell Sci 2003 Dec 1;116(Pt 23):4707-14.
              pubmed: 14600257doi: 10.1242/jcs.00840google scholar: lookup
            40. Nicola AV, Straus SE. Cellular and viral requirements for rapid endocytic entry of herpes simplex virus.. J Virol 2004 Jul;78(14):7508-17.
              pmc: PMC434080pubmed: 15220424doi: 10.1128/jvi.78.14.7508-7517.2004google scholar: lookup
            41. Nicola AV, McEvoy AM, Straus SE. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells.. J Virol 2003 May;77(9):5324-32.
              pmc: PMC153978pubmed: 12692234doi: 10.1128/jvi.77.9.5324-5332.2003google scholar: lookup
            42. Nicola AV, Hou J, Major EO, Straus SE. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway.. J Virol 2005 Jun;79(12):7609-16.
              pmc: PMC1143659pubmed: 15919913doi: 10.1128/jvi.79.12.7609-7616.2005google scholar: lookup
            43. Nomura R, Kiyota A, Suzaki E, Kataoka K, Ohe Y, Miyamoto K, Senda T, Fujimoto T. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae.. J Virol 2004 Aug;78(16):8701-8.
              pmc: PMC479086pubmed: 15280478doi: 10.1128/jvi.78.16.8701-8708.2004google scholar: lookup
            44. O'Callaghan DJ, Cheevers WP, Gentry GA, Randall CC. Kinetics of cellular and viral DNA synthesis in equine abortion (herpes) virus infection of L-M cells.. Virology 1968 Sep;36(1):104-14.
              pubmed: 5669981doi: 10.1016/0042-6822(68)90120-7google scholar: lookup
            45. Orlichenko L, Huang B, Krueger E, McNiven MA. Epithelial growth factor-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells.. J Biol Chem 2006 Feb 24;281(8):4570-9.
              pubmed: 16332692doi: 10.1074/jbc.m512088200google scholar: lookup
            46. Palade GE. Fine structure of blood capillaries.. J. Appl. Phys. 1953;24:1424.
            47. Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae.. J Cell Biol 1994 Dec;127(5):1199-215.
              pmc: PMC2120257pubmed: 7962085doi: 10.1083/jcb.127.5.1199google scholar: lookup
            48. Richterová Z, Liebl D, Horák M, Palková Z, Stokrová J, Hozák P, Korb J, Forstová J. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei.. J Virol 2001 Nov;75(22):10880-91.
              pmc: PMC114668pubmed: 11602728doi: 10.1128/jvi.75.22.10880-10891.2001google scholar: lookup
            49. Smith JL, Campos SK, Ozbun MA. Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes.. J Virol 2007 Sep;81(18):9922-31.
              pmc: PMC2045393pubmed: 17626097doi: 10.1128/jvi.00988-07google scholar: lookup
            50. Stein BS, Gowda SD, Lifson JD, Penhallow RC, Bensch KG, Engleman EG. pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane.. Cell 1987 Jun 5;49(5):659-68.
              pubmed: 3107838doi: 10.1016/0092-8674(87)90542-3google scholar: lookup
            51. Storts RW, Montgomery DL. The nervous system.. 2001. pp. 430–431.
            52. Sukumaran SK, Quon MJ, Prasadarao NV. Escherichia coli K1 internalization via caveolae requires caveolin-1 and protein kinase Calpha interaction in human brain microvascular endothelial cells.. J Biol Chem 2002 Dec 27;277(52):50716-24.
              pubmed: 12386163doi: 10.1074/jbc.m208830200google scholar: lookup
            53. Tsiang H, Superti F. Ammonium chloride and chloroquine inhibit rabies virus infection in neuroblastoma cells. Brief report.. Arch Virol 1984;81(3-4):377-82.
              pubmed: 6148053doi: 10.1007/bf01310010google scholar: lookup
            54. Van de Walle GR, Peters ST, VanderVen BC, O'Callaghan DJ, Osterrieder N. Equine herpesvirus 1 entry via endocytosis is facilitated by alphaV integrins and an RSD motif in glycoprotein D.. J Virol 2008 Dec;82(23):11859-68.
              pmc: PMC2583640pubmed: 18815313doi: 10.1128/jvi.00868-08google scholar: lookup
            55. van Weert AW, Dunn KW, Geuze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump.. J Cell Biol 1995 Aug;130(4):821-34.
              pmc: PMC2199957pubmed: 7642700doi: 10.1083/jcb.130.4.821google scholar: lookup
            56. Virgintino D, Robertson D, Errede M, Benagiano V, Tauer U, Roncali L, Bertossi M. Expression of caveolin-1 in human brain microvessels.. Neuroscience 2002;115(1):145-52.
              pubmed: 12401329doi: 10.1016/s0306-4522(02)00374-3google scholar: lookup
            57. Wittels M, Spear PG. Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway.. Virus Res 1991 Mar;18(2-3):271-90.
              pubmed: 1645908doi: 10.1016/0168-1702(91)90024-pgoogle scholar: lookup
            58. YAMADA E. The fine structure of the gall bladder epithelium of the mouse.. J Biophys Biochem Cytol 1955 Sep 25;1(5):445-58.
              pmc: PMC2229656pubmed: 13263332doi: 10.1083/jcb.1.5.445google scholar: lookup
            59. Yoshimura A, Ohnishi S. Uncoating of influenza virus in endosomes.. J Virol 1984 Aug;51(2):497-504.
              pmc: PMC254465pubmed: 6431119doi: 10.1128/jvi.51.2.497-504.1984google scholar: lookup

            Citations

            This article has been cited 16 times.
            1. Ripa I, Andreu S, López-Guerrero JA, Bello-Morales R. Membrane Rafts: Portals for Viral Entry.. Front Microbiol 2021;12:631274.
              doi: 10.3389/fmicb.2021.631274pubmed: 33613502google scholar: lookup
            2. Dudãu M, Codrici E, Tanase C, Gherghiceanu M, Enciu AM, Hinescu ME. Caveolae as Potential Hijackable Gates in Cell Communication.. Front Cell Dev Biol 2020;8:581732.
              doi: 10.3389/fcell.2020.581732pubmed: 33195223google scholar: lookup
            3. Pavulraj S, Kamel M, Stephanowitz H, Liu F, Plendl J, Osterrieder N, Azab W. Equine Herpesvirus Type 1 Modulates Cytokine and Chemokine Profiles of Mononuclear Cells for Efficient Dissemination to Target Organs.. Viruses 2020 Sep 8;12(9).
              doi: 10.3390/v12090999pubmed: 32911663google scholar: lookup
            4. Xing Y, Wen Z, Gao W, Lin Z, Zhong J, Jiu Y. Multifaceted Functions of Host Cell Caveolae/Caveolin-1 in Virus Infections.. Viruses 2020 Apr 26;12(5).
              doi: 10.3390/v12050487pubmed: 32357558google scholar: lookup
            5. Wei R, Van Renne N, Nauwynck HJ. Strain-Dependent Porcine Circovirus Type 2 (PCV2) Entry and Replication in T-Lymphoblasts.. Viruses 2019 Sep 2;11(9).
              doi: 10.3390/v11090813pubmed: 31480752google scholar: lookup
            6. Nicola AV. Herpesvirus Entry into Host Cells Mediated by Endosomal Low pH.. Traffic 2016 Sep;17(9):965-75.
              doi: 10.1111/tra.12408pubmed: 27126894google scholar: lookup
            7. Walker EB, Pritchard SM, Cunha CW, Aguilar HC, Nicola AV. Polyethylene glycol-mediated fusion of herpes simplex type 1 virions with the plasma membrane of cells that support endocytic entry.. Virol J 2015 Nov 16;12:190.
              doi: 10.1186/s12985-015-0423-0pubmed: 26573723google scholar: lookup
            8. Piccini LE, Castilla V, Damonte EB. Dengue-3 Virus Entry into Vero Cells: Role of Clathrin-Mediated Endocytosis in the Outcome of Infection.. PLoS One 2015;10(10):e0140824.
              doi: 10.1371/journal.pone.0140824pubmed: 26469784google scholar: lookup
            9. Azab W, Lehmann MJ, Osterrieder N. Glycoprotein H and α4β1 integrins determine the entry pathway of alphaherpesviruses.. J Virol 2013 May;87(10):5937-48.
              doi: 10.1128/JVI.03522-12pubmed: 23514881google scholar: lookup
            10. Azab W, Zajic L, Osterrieder N. The role of glycoprotein H of equine herpesviruses 1 and 4 (EHV-1 and EHV-4) in cellular host range and integrin binding.. Vet Res 2012 Aug 21;43(1):61.
              doi: 10.1186/1297-9716-43-61pubmed: 22909178google scholar: lookup
            11. Azab W, Osterrieder N. Glycoproteins D of equine herpesvirus type 1 (EHV-1) and EHV-4 determine cellular tropism independently of integrins.. J Virol 2012 Feb;86(4):2031-44.
              doi: 10.1128/JVI.06555-11pubmed: 22171258google scholar: lookup
            12. Zaichick SV, Bohannon KP, Smith GA. Alphaherpesviruses and the cytoskeleton in neuronal infections.. Viruses 2011 Jul;3(7):941-81.
              doi: 10.3390/v3070941pubmed: 21994765google scholar: lookup
            13. Sasaki M, Kim E, Igarashi M, Ito K, Hasebe R, Fukushi H, Sawa H, Kimura T. Single amino acid residue in the A2 domain of major histocompatibility complex class I is involved in the efficiency of equine herpesvirus-1 entry.. J Biol Chem 2011 Nov 11;286(45):39370-8.
              doi: 10.1074/jbc.M111.251751pubmed: 21949188google scholar: lookup
            14. Guo CJ, Liu D, Wu YY, Yang XB, Yang LS, Mi S, Huang YX, Luo YW, Jia KT, Liu ZY, Chen WJ, Weng SP, Yu XQ, He JG. Entry of tiger frog virus (an Iridovirus) into HepG2 cells via a pH-dependent, atypical, caveola-mediated endocytosis pathway.. J Virol 2011 Jul;85(13):6416-26.
              doi: 10.1128/JVI.01500-10pubmed: 21543502google scholar: lookup
            15. Sasaki M, Hasebe R, Makino Y, Suzuki T, Fukushi H, Okamoto M, Matsuda K, Taniyama H, Sawa H, Kimura T. Equine major histocompatibility complex class I molecules act as entry receptors that bind to equine herpesvirus-1 glycoprotein D.. Genes Cells 2011 Apr;16(4):343-57.
              doi: 10.1111/j.1365-2443.2011.01491.xpubmed: 21306483google scholar: lookup
            16. Stiles KM, Krummenacher C. Glycoprotein D actively induces rapid internalization of two nectin-1 isoforms during herpes simplex virus entry.. Virology 2010 Mar 30;399(1):109-119.
              doi: 10.1016/j.virol.2009.12.034pubmed: 20089288google scholar: lookup
            Subscribe to our newsletter
            Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.