FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Vet Microbiol / Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dyn...
Veterinary microbiology2009; 141(1-2); 12-21; doi: 10.1016/j.vetmic.2009.07.035

Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dynein, and ROCK1 to productively infect cells.

Abstract: To initiate infection, equine herpesvirus type 1 (EHV-1) attaches to heparan sulfate on cell surfaces and then interacts with a putative glycoprotein D receptor(s). After attachment, virus entry occurs either by direct fusion of the virus envelope with the plasma membrane or via endocytosis followed by fusion between the virus envelope and an endosomal membrane. Upon fusion, de-enveloped virus particles are deposited into the cytoplasm and travel to the nucleus for viral replication. In this report, we examined the mechanism of EHV-1 intracellular trafficking and investigated the ability of EHV-1 to utilize specific cellular components to efficiently travel to the nucleus post-entry. Using a panel of microtubule-depolymerizing drugs and inhibitors of microtubule motor proteins, we show that EHV-1 infection is dependent on both the integrity of the microtubule network and the minus-end microtubule motor protein, dynein. In addition, we show that EHV-1 actively induces the acetylation of tubulin, a marker of microtubule stabilization, as early as 15 min post-infection. Finally, our data support a role for the cellular kinase, ROCK1, in virus trafficking to the nucleus.
Copyright 2009 Elsevier B.V. All rights reserved.
Get Full Text
Publication Date: 2009-08-08 PubMed ID: 19713056PubMed Central: PMC2819619DOI: 10.1016/j.vetmic.2009.07.035Google 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
  • N.I.H.
  • Extramural

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.

The research article is about how the equine herpesvirus type 1 (EHV-1) uses certain cell components to efficiently infect cells. It shows that EHV-1 infection relies on the microtubule structure and the protein dynein, and suggests that the cellular kinase, ROCK1, also plays a part in virus trafficking to the cell’s nucleus.

Background of the Study

  • The focus of the research is the equine herpesvirus type 1 (EHV-1) and its mechanism of infection in cells.
  • The authors explain how EHV-1 initially connects to cell surfaces by attaching to heparan sulfate and then engages with a presumed glycoprotein D receptor(s).
  • The entry of the virus into the cell can occur through direct fusion of the virus envelope with the plasma membrane or via endocytosis, followed by fusion between the virus envelope and an endosomal membrane.
  • Once fusion occurs, the virus particles are deposited into the cytoplasm and move towards the nucleus for viral replication.

Details of the Study and Findings

  • The study investigates the EHV-1 intracellular trafficking mechanism and how the virus leverages specific cellular components for efficient transport to the nucleus post-entry.
  • For this purpose, the researchers used a range of microtubule-depolymerizing medications and inhibitors of microtubule motor proteins.
  • The researchers found that EHV-1 infection is dependent on both the integrity of the microtubule network and the minus-end microtubule motor protein known as dynein.
  • Notably, the researchers showed that EHV-1 actively contributes to the acetylation of tubulin, a marker of microtubule stabilization, as early as 15 minutes post-infection.

Role of ROCK1 in Viral Infection

  • The authors’ data indicates a potential role for the cellular kinase, ROCK1, in virus trafficking to the nucleus.
  • ROCK1 could be another critical factor in how EHV-1 infects cells, though the exact mechanism by which it contributes is not clearly spelled out in the abstract and requires further research.

Conclusion

  • This study sheds light on the role of various cell components in the infection process of EHV-1.
  • It provides foundational knowledge on how viruses can “hijack” cellular components for their replication, catalysts for potential therapeutic interventions targeting these processes.

Cite This Article

APA
Frampton AR, Uchida H, von Einem J, Goins WF, Grandi P, Cohen JB, Osterrieder N, Glorioso JC. (2009). Equine herpesvirus type 1 (EHV-1) utilizes microtubules, dynein, and ROCK1 to productively infect cells. Vet Microbiol, 141(1-2), 12-21. https://doi.org/10.1016/j.vetmic.2009.07.035

Publication

Veterinary microbiology
ISSN: 1873-2542
NlmUniqueID: 7705469
Country: Netherlands
Language: English
Volume: 141
Issue: 1-2
Pages: 12-21

Researcher Affiliations

Frampton, Arthur R
  • Department of Microbiology and Molecular Genetics, University of Pittsburgh, School of Medicine, Pittsburgh, PA 15261, United States. framptona@uncw.edu
Uchida, Hiroaki
    von Einem, Jens
      Goins, William F
        Grandi, Paola
          Cohen, Justus B
            Osterrieder, Nikolaus
              Glorioso, Joseph C

                MeSH Terms

                • Acetylation
                • Animals
                • Blotting, Western
                • CHO Cells
                • Cell Line
                • Cricetinae
                • Cricetulus
                • Dyneins / metabolism
                • Herpesvirus 1, Equid / genetics
                • Herpesvirus 1, Equid / metabolism
                • Herpesvirus 1, Equid / pathogenicity
                • Horses
                • Microscopy, Confocal
                • Microtubules / metabolism
                • Rabbits
                • Tubulin / metabolism
                • rho-Associated Kinases / metabolism

                Grant Funding

                • R01 CA119298 / NCI NIH HHS
                • U01 HL066949-050003 / NHLBI NIH HHS
                • NS040923 / NINDS NIH HHS
                • CA119298 / NCI NIH HHS
                • P01 NS040923 / NINDS NIH HHS
                • P01 NS040923-070006 / NINDS NIH HHS
                • R01 CA119298-04 / NCI NIH HHS
                • R01 NS044323 / NINDS NIH HHS
                • U01 HL066949 / NHLBI NIH HHS
                • NS44323 / NINDS NIH HHS
                • R01 NS044323-04 / NINDS NIH HHS
                • HL066949 / NHLBI NIH HHS

                References

                This article includes 38 references
                1. Allen GP, Bryans JT. Molecular epizootiology, pathogenesis, and prophylaxis of equine herpesvirus-1 infections.. Prog Vet Microbiol Immunol 1986;2:78-144.
                  pubmed: 2856183
                2. Alonso C, Miskin J, Hernáez B, Fernandez-Zapatero P, Soto L, Cantó C, Rodríguez-Crespo I, Dixon L, Escribano JM. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein.. J Virol 2001 Oct;75(20):9819-27.
                  pmc: PMC114554pubmed: 11559815doi: 10.1128/jvi.75.20.9819-9827.2001google scholar: lookup
                3. Bouchard P, Penningroth SM, Cheung A, Gagnon C, Bardin CW. erythro-9-[3-(2-Hydroxynonyl)]adenine is an inhibitor of sperm motility that blocks dynein ATPase and protein carboxylmethylase activities.. Proc Natl Acad Sci U S A 1981 Feb;78(2):1033-6.
                  pmc: PMC319940pubmed: 6453342doi: 10.1073/pnas.78.2.1033google scholar: lookup
                4. Cheshenko N, Liu W, Satlin LM, Herold BC. Focal adhesion kinase plays a pivotal role in herpes simplex virus entry.. J Biol Chem 2005 Sep 2;280(35):31116-25.
                  pubmed: 15994312doi: 10.1074/jbc.m503518200google scholar: lookup
                5. Cheung PY, Zhang Y, Long J, Lin S, Zhang M, Jiang Y, Wu Z. p150(Glued), Dynein, and microtubules are specifically required for activation of MKK3/6 and p38 MAPKs.. J Biol Chem 2004 Oct 29;279(44):45308-11.
                  pubmed: 15375157doi: 10.1074/jbc.c400333200google scholar: lookup
                6. Clement C, Tiwari V, Scanlan PM, Valyi-Nagy T, Yue BY, Shukla D. A novel role for phagocytosis-like uptake in herpes simplex virus entry.. J Cell Biol 2006 Sep 25;174(7):1009-21.
                  pmc: PMC2064392pubmed: 17000878doi: 10.1083/jcb.200509155google scholar: lookup
                7. Csellner H, Walker C, Wellington JE, McLure LE, Love DN, Whalley JM. EHV-1 glycoprotein D (EHV-1 gD) is required for virus entry and cell-cell fusion, and an EHV-1 gD deletion mutant induces a protective immune response in mice.. Arch Virol 2000;145(11):2371-85.
                  pubmed: 11205124doi: 10.1007/s007050070027google scholar: lookup
                8. Dhani SU, Mohammad-Panah R, Ahmed N, Ackerley C, Ramjeesingh M, Bear CE. Evidence for a functional interaction between the ClC-2 chloride channel and the retrograde motor dynein complex.. J Biol Chem 2003 May 2;278(18):16262-70.
                  pubmed: 12601004doi: 10.1074/jbc.m209828200google scholar: lookup
                9. Döhner K, Nagel CH, Sodeik B. Viral stop-and-go along microtubules: taking a ride with dynein and kinesins.. Trends Microbiol 2005 Jul;13(7):320-7.
                  pubmed: 15950476doi: 10.1016/j.tim.2005.05.010google scholar: lookup
                10. Döhner K, Wolfstein A, Prank U, Echeverri C, Dujardin D, Vallee R, Sodeik B. Function of dynein and dynactin in herpes simplex virus capsid transport.. Mol Biol Cell 2002 Aug;13(8):2795-809.
                  pmc: PMC117943pubmed: 12181347doi: 10.1091/mbc.01-07-0348google scholar: lookup
                11. Douglas MW, Diefenbach RJ, Homa FL, Miranda-Saksena M, Rixon FJ, Vittone V, Byth K, Cunningham AL. Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport.. J Biol Chem 2004 Jul 2;279(27):28522-30.
                  pubmed: 15117959doi: 10.1074/jbc.m311671200google scholar: lookup
                12. Elliott G, O'Hare P. Herpes simplex virus type 1 tegument protein VP22 induces the stabilization and hyperacetylation of microtubules.. J Virol 1998 Aug;72(8):6448-55.
                  pmc: PMC109805pubmed: 9658087doi: 10.1128/jvi.72.8.6448-6455.1998google scholar: lookup
                13. Florin L, Becker KA, Lambert C, Nowak T, Sapp C, Strand D, Streeck RE, Sapp M. Identification of a dynein interacting domain in the papillomavirus minor capsid protein l2.. J Virol 2006 Jul;80(13):6691-6.
                  pmc: PMC1488977pubmed: 16775357doi: 10.1128/jvi.00057-06google scholar: lookup
                14. Frampton AR Jr, Goins WF, Cohen JB, von Einem J, Osterrieder N, O'Callaghan DJ, Glorioso JC. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor.. J Virol 2005 Mar;79(5):3169-73.
                  pmc: PMC548480pubmed: 15709036doi: 10.1128/jvi.79.5.3169-3173.2005google scholar: lookup
                15. 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
                16. 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
                17. Jacob Y, Badrane H, Ceccaldi PE, Tordo N. Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein.. J Virol 2000 Nov;74(21):10217-22.
                  pmc: PMC102062pubmed: 11024152doi: 10.1128/jvi.74.21.10217-10222.2000google scholar: lookup
                18. Jouvenet N, Monaghan P, Way M, Wileman T. Transport of African swine fever virus from assembly sites to the plasma membrane is dependent on microtubules and conventional kinesin.. J Virol 2004 Aug;78(15):7990-8001.
                  pmc: PMC446130pubmed: 15254171doi: 10.1128/jvi.78.15.7990-8001.2004google scholar: lookup
                19. Kelkar SA, Pfister KK, Crystal RG, Leopold PL. Cytoplasmic dynein mediates adenovirus binding to microtubules.. J Virol 2004 Sep;78(18):10122-32.
                  pmc: PMC515014pubmed: 15331745doi: 10.1128/jvi.78.18.10122-10132.2004google scholar: lookup
                20. Kobayashi T, Martensen T, Nath J, Flavin M. Inhibition of dynein ATPase by vanadate, and its possible use as a probe for the role of dynein in cytoplasmic motility.. Biochem Biophys Res Commun 1978 Apr 28;81(4):1313-8.
                  pubmed: 149544doi: 10.1016/0006-291x(78)91279-2google scholar: lookup
                21. Kristensson K, Lycke E, Röyttä M, Svennerholm B, Vahlne A. Neuritic transport of herpes simplex virus in rat sensory neurons in vitro. Effects of substances interacting with microtubular function and axonal flow [nocodazole, taxol and erythro-9-3-(2-hydroxynonyl)adenine].. J Gen Virol 1986 Sep;67 ( Pt 9):2023-8.
                  pubmed: 2427647doi: 10.1099/0022-1317-67-9-2023google scholar: lookup
                22. Lee GE, Murray JW, Wolkoff AW, Wilson DW. Reconstitution of herpes simplex virus microtubule-dependent trafficking in vitro.. J Virol 2006 May;80(9):4264-75.
                  pmc: PMC1472043pubmed: 16611885doi: 10.1128/jvi.80.9.4264-4275.2006google scholar: lookup
                23. Mabit H, Nakano MY, Prank U, Saam B, Döhner K, Sodeik B, Greber UF. Intact microtubules support adenovirus and herpes simplex virus infections.. J Virol 2002 Oct;76(19):9962-71.
                  pmc: PMC136514pubmed: 12208972doi: 10.1128/jvi.76.19.9962-9971.2002google scholar: lookup
                24. Naranatt PP, Krishnan HH, Smith MS, Chandran B. Kaposi's sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus.. J Virol 2005 Jan;79(2):1191-206.
                  pmc: PMC538527pubmed: 15613346doi: 10.1128/jvi.79.2.1191-1206.2005google scholar: lookup
                25. Nogales E. Structural insights into microtubule function.. Annu Rev Biochem 2000;69:277-302.
                  pubmed: 10966460doi: 10.1146/annurev.biochem.69.1.277google scholar: lookup
                26. O'CALLAGHAN DJ, GENTRY GA, RANDALL CC. The equine herpesviruses. In: ROIZMAN B, editor. The Herpesviruses, Comprehensive Virology. Plenum Press; New York: 1983.
                27. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant.. Virus Res 1999 Feb;59(2):165-77.
                  pubmed: 10082388doi: 10.1016/s0168-1702(98)00134-8google scholar: lookup
                28. Palazzo AF, Cook TA, Alberts AS, Gundersen GG. mDia mediates Rho-regulated formation and orientation of stable microtubules.. Nat Cell Biol 2001 Aug;3(8):723-9.
                  pubmed: 11483957doi: 10.1038/35087035google scholar: lookup
                29. Penningroth SM, Cheung A, Bouchard P, Gagnon C, Bardin CW. Dynein ATPase is inhibited selectively in vitro by erythro-9-[3-2-(hydroxynonyl)]adenine.. Biochem Biophys Res Commun 1982 Jan 15;104(1):234-40.
                  pubmed: 6462140doi: 10.1016/0006-291x(82)91964-7google scholar: lookup
                30. Petit C, Giron ML, Tobaly-Tapiero J, Bittoun P, Real E, Jacob Y, Tordo N, De The H, Saib A. Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8.. J Cell Sci 2003 Aug 15;116(Pt 16):3433-42.
                  pubmed: 12857789doi: 10.1242/jcs.00613google scholar: lookup
                31. Piperno G, LeDizet M, Chang XJ. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture.. J Cell Biol 1987 Feb;104(2):289-302.
                  pmc: PMC2114420pubmed: 2879846doi: 10.1083/jcb.104.2.289google scholar: lookup
                32. Raghu H, Sharma-Walia N, Veettil MV, Sadagopan S, Caballero A, Sivakumar R, Varga L, Bottero V, Chandran B. Lipid rafts of primary endothelial cells are essential for Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8-induced phosphatidylinositol 3-kinase and RhoA-GTPases critical for microtubule dynamics and nuclear delivery of viral DNA but dispensable for binding and entry.. J Virol 2007 Aug;81(15):7941-59.
                  pmc: PMC1951274pubmed: 17507466doi: 10.1128/jvi.02848-06google scholar: lookup
                33. Raux H, Flamand A, Blondel D. Interaction of the rabies virus P protein with the LC8 dynein light chain.. J Virol 2000 Nov;74(21):10212-6.
                  pmc: PMC102061pubmed: 11024151doi: 10.1128/jvi.74.21.10212-10216.2000google scholar: lookup
                34. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, Brown SD, Rubinsztein DC. Dynein mutations impair autophagic clearance of aggregate-prone proteins.. Nat Genet 2005 Jul;37(7):771-6.
                  pubmed: 15980862doi: 10.1038/ng1591google scholar: lookup
                35. Sodeik B, Ebersold MW, Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus.. J Cell Biol 1997 Mar 10;136(5):1007-21.
                  pmc: PMC2132479pubmed: 9060466doi: 10.1083/jcb.136.5.1007google scholar: lookup
                36. Sugahara Y, Matsumura T, Kono Y, Honda E, Kida H, Okazaki K. Adaptation of equine herpesvirus 1 to unnatural host led to mutation of the gC resulting in increased susceptibility of the virus to heparin.. Arch Virol 1997;142(9):1849-56.
                  pubmed: 9672642doi: 10.1007/s007050050202google scholar: lookup
                37. Suikkanen S, Aaltonen T, Nevalainen M, Välilehto O, Lindholm L, Vuento M, Vihinen-Ranta M. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus.. J Virol 2003 Oct;77(19):10270-9.
                  pmc: PMC228505pubmed: 12970411doi: 10.1128/jvi.77.19.10270-10279.2003google scholar: lookup
                38. Ye GJ, Vaughan KT, Vallee RB, Roizman B. The herpes simplex virus 1 U(L)34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane.. J Virol 2000 Feb;74(3):1355-63.
                  pmc: PMC111470pubmed: 10627546doi: 10.1128/jvi.74.3.1355-1363.2000google scholar: lookup

                Citations

                This article has been cited 22 times.
                1. Black JB, Frampton AR. Anti-inflammatory compounds reduce equine herpesvirus type 1 replication and cell-to-cell spread.. Front Vet Sci 2023;10:1165917.
                  doi: 10.3389/fvets.2023.1165917pubmed: 37275614google scholar: lookup
                2. Song Y, Nguyen XN, Kumar A, da Silva C, Picard L, Etienne L, Cimarelli A. Trim69 is a microtubule regulator that acts as a pantropic viral inhibitor.. Proc Natl Acad Sci U S A 2022 Oct 25;119(43):e2211467119.
                  doi: 10.1073/pnas.2211467119pubmed: 36251989google 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. Kolyvushko O, Kelch MA, Osterrieder N, Azab W. Equine Alphaherpesviruses Require Activation of the Small GTPases Rac1 and Cdc42 for Intracellular Transport.. Microorganisms 2020 Jul 7;8(7).
                  doi: 10.3390/microorganisms8071013pubmed: 32645930google scholar: lookup
                5. Lee JS, Ismail AM, Lee JY, Zhou X, Materne EC, Chodosh J, Rajaiya J. Impact of dynamin 2 on adenovirus nuclear entry.. Virology 2019 Mar;529:43-56.
                  doi: 10.1016/j.virol.2019.01.008pubmed: 30660774google scholar: lookup
                6. Barber KA, Daugherty HC, Ander SE, Jefferson VA, Shack LA, Pechan T, Nanduri B, Meyer F. Protein Composition of the Bovine Herpesvirus 1.1 Virion.. Vet Sci 2017 Feb 20;4(1).
                  doi: 10.3390/vetsci4010011pubmed: 29056670google scholar: lookup
                7. Bai H, Lester GMS, Petishnok LC, Dean DA. Cytoplasmic transport and nuclear import of plasmid DNA.. Biosci Rep 2017 Dec 22;37(6).
                  doi: 10.1042/BSR20160616pubmed: 29054961google scholar: lookup
                8. Kobayashi R, Kato A, Sagara H, Watanabe M, Maruzuru Y, Koyanagi N, Arii J, Kawaguchi Y. Herpes Simplex Virus 1 Small Capsomere-Interacting Protein VP26 Regulates Nucleocapsid Maturation.. J Virol 2017 Sep 15;91(18).
                  doi: 10.1128/JVI.01068-17pubmed: 28679756google scholar: lookup
                9. Loftus MS, Verville N, Kedes DH. A Conserved Leucine Zipper Motif in Gammaherpesvirus ORF52 Is Critical for Distinct Microtubule Rearrangements.. J Virol 2017 Sep 1;91(17).
                  doi: 10.1128/JVI.00304-17pubmed: 28615210google scholar: lookup
                10. Van den Broeke C, Jacob T, Favoreel HW. Rho'ing in and out of cells: viral interactions with Rho GTPase signaling.. Small GTPases 2014;5:e28318.
                  doi: 10.4161/sgtp.28318pubmed: 24691164google scholar: lookup
                11. Słońska A, Cymerys J, Godlewski MM, Dzieciątkowski T, Tucholska A, Chmielewska A, Golke A, Bańbura MW. Equine herpesvirus type 1 (EHV-1)-induced rearrangements of actin filaments in productively infected primary murine neurons.. Arch Virol 2014 Jun;159(6):1341-9.
                  doi: 10.1007/s00705-013-1949-3pubmed: 24352436google scholar: lookup
                12. Sabo Y, Walsh D, Barry DS, Tinaztepe S, de Los Santos K, Goff SP, Gundersen GG, Naghavi MH. HIV-1 induces the formation of stable microtubules to enhance early infection.. Cell Host Microbe 2013 Nov 13;14(5):535-46.
                  doi: 10.1016/j.chom.2013.10.012pubmed: 24237699google scholar: lookup
                13. Naghavi MH, Gundersen GG, Walsh D. Plus-end tracking proteins, CLASPs, and a viral Akt mimic regulate herpesvirus-induced stable microtubule formation and virus spread.. Proc Natl Acad Sci U S A 2013 Nov 5;110(45):18268-73.
                  doi: 10.1073/pnas.1310760110pubmed: 24145430google scholar: lookup
                14. 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
                15. De Conto F, Di Lonardo E, Arcangeletti MC, Chezzi C, Medici MC, Calderaro A. Highly dynamic microtubules improve the effectiveness of early stages of human influenza A/NWS/33 virus infection in LLC-MK2 cells.. PLoS One 2012;7(7):e41207.
                  doi: 10.1371/journal.pone.0041207pubmed: 22911759google scholar: lookup
                16. Bosse JB, Bauerfeind R, Popilka L, Marcinowski L, Taeglich M, Jung C, Striebinger H, von Einem J, Gaul U, Walther P, Koszinowski UH, Ruzsics Z. A beta-herpesvirus with fluorescent capsids to study transport in living cells.. PLoS One 2012;7(7):e40585.
                  doi: 10.1371/journal.pone.0040585pubmed: 22792376google scholar: lookup
                17. Smith G. Herpesvirus transport to the nervous system and back again.. Annu Rev Microbiol 2012;66:153-76.
                  doi: 10.1146/annurev-micro-092611-150051pubmed: 22726218google scholar: lookup
                18. Street CA, Bryan BA. Rho kinase proteins--pleiotropic modulators of cell survival and apoptosis.. Anticancer Res 2011 Nov;31(11):3645-57.
                  pubmed: 22110183
                19. Zhang W, Greene W, Gao SJ. Microtubule- and dynein-dependent nuclear trafficking of rhesus rhadinovirus in rhesus fibroblasts.. J Virol 2012 Jan;86(1):599-604.
                  doi: 10.1128/JVI.06129-11pubmed: 22031929google scholar: lookup
                20. Van den Broeke C, Favoreel HW. Actin' up: herpesvirus interactions with Rho GTPase signaling.. Viruses 2011 Apr;3(4):278-92.
                  doi: 10.3390/v3040278pubmed: 21994732google scholar: lookup
                21. Bohannon KP, Sollars PJ, Pickard GE, Smith GA. Fusion of a fluorescent protein to the pUL25 minor capsid protein of pseudorabies virus allows live-cell capsid imaging with negligible impact on infection.. J Gen Virol 2012 Jan;93(Pt 1):124-129.
                  doi: 10.1099/vir.0.036145-0pubmed: 21976610google scholar: lookup
                22. Kurtz BM, Singletary LB, Kelly SD, Frampton AR Jr. Equus caballus major histocompatibility complex class I is an entry receptor for equine herpesvirus type 1.. J Virol 2010 Sep;84(18):9027-34.
                  doi: 10.1128/JVI.00287-10pubmed: 20610718google scholar: lookup
                Subscribe to our newsletter
                Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.