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

Veterinary Microbiology

Volumn 141, Issue 1-2, 2010, Pages 12-21

  Frampton Jr , Arthur R ^a   Uchida, Hiroaki ^a   von Einem, Jens ^b   Goins, William F ^a   Grandi, Paola ^a   Cohen, Justus B ^a   Osterrieder, Nikolaus ^b,c   Glorioso, Joseph C ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Dynein; EHV 1; Microtubules; ROCK1; Trafficking

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MICROTUBULE PROTEIN; MOLECULAR MOTOR; PHOSPHOTRANSFERASE; PROTEIN ROCK1; TUBULIN; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DEPOLYMERIZATION; DISEASE COURSE; EQUINE HERPES VIRUS; EQUINE HERPESVIRUS 1; HORSE DISEASE; INTRACELLULAR TRANSPORT; MICROTUBULE; NONHUMAN; VIRUS CELL INTERACTION; VIRUS INFECTION;

ACETYLATION; ANIMALS; BLOTTING, WESTERN; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; DYNEINS; HERPESVIRUS 1, EQUID; HORSES; MICROSCOPY, CONFOCAL; MICROTUBULES; RABBITS; RHO-ASSOCIATED KINASES; TUBULIN;

EQUID HERPESVIRUS 1;

EID: 75149131559     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2009.07.035     Document Type: Article

References (38)

1. Allen G.P., and Bryans J.T. Molecular epizootiology, pathogenesis, and prophylaxis of equine herpesvirus-1 infections. Prog. Vet. Microbiol. Immunol. 2 (1986) 78-144
2. Alonso C., Miskin J., Hernaez B., Fernandez-zapatero P., Soto L., Canto C., Rodriguez-crespo I., Dixon L., and Escribano J.M. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J. Virol. 75 (2001) 9819-9827
3. Bouchard P., Penningroth S.M., Cheung A., Gagnon C., and Bardin C.W. 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. 78 (1981) 1033-1036
4. Cheshenko N., Liu W., Satlin L.M., and Herold B.C. Focal adhesion kinase plays a pivotal role in herpes simplex virus entry. J. Biol. Chem. 280 (2005) 31116-31125
5. Cheung P.Y., Zhang Y., Long J., Lin S., Zhang M., Jiang Y., and Wu Z. p150(Glued), dynein, and microtubules are specifically required for activation of MKK3/6 and p38 MAPKs. J. Biol. Chem. 279 (2004) 45308-45311
6. Clement C., Tiwari V., Scanlan P.M., Valyi-nagy T., Yue B.Y., and Shukla D. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J. Cell Biol. 174 (2006) 1009-1021
7. Csellner H., Walker C., Wellington J.E., Mclure L.E., Love D.N., and Whalley J.M. 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. 145 (2000) 2371-2385
8. Dhani S.U., Mohammad-panah R., Ahmed N., Ackerley C., Ramjeesingh M., and Bear C.E. Evidence for a functional interaction between the ClC-2 chloride channel and the retrograde motor dynein complex. J. Biol. Chem. 278 (2003) 16262-16270
9. Dohner K., Nagel C.H., and Sodeik B. Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol. 13 (2005) 320-327
10. Dohner K., Wolfstein A., Prank U., Echeverri C., Dujardin D., Vallee R., and Sodeik B. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell. 13 (2002) 2795-2809
11. Douglas M.W., Diefenbach R.J., Homa F.L., Miranda-saksena M., Rixon F.J., Vittone V., Byth K., and Cunningham A.L. 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. 279 (2004) 28522-28530
12. Elliott G., and O'hare P. Herpes simplex virus type 1 tegument protein VP22 induces the stabilization and hyperacetylation of microtubules. J. Virol. 72 (1998) 6448-6455
13. Florin L., Becker K.A., Lambert C., Nowak T., Sapp C., Strand D., Streeck R.E., and Sapp M. Identification of a dynein interacting domain in the papillomavirus minor capsid protein l2. J. Virol. 80 (2006) 6691-6696
14. Frampton Jr. A.R., Goins W.F., Cohen J.B., Von Einem J., Osterrieder N., O'Callaghan D.J., and Glorioso J.C. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor. J. Virol. 79 (2005) 3169-3173
15. Frampton Jr. A.R., Smith P.M., Zhang Y., Matsumura T., Osterrieder N., and O'Callaghan D.J. Contribution of gene products encoded within the unique short segment of equine herpesvirus 1 to virulence in a murine model. Virus Res. 90 (2002) 287-301
16. Frampton Jr. A.R., Stolz D.B., Uchida H., Goins W.F., Cohen J.B., and Glorioso J.C. Equine herpesvirus 1 enters cells by two different pathways, and infection requires the activation of the cellular kinase ROCK1. J. Virol. 81 (2007) 10879-10889
17. Jacob Y., Badrane H., Ceccaldi P.E., and Tordo N. Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein. J. Virol. 74 (2000) 10217-10222
18. Jouvenet N., Monaghan P., Way M., and Wileman T. Transport of African swine fever virus from assembly sites to the plasma membrane is dependent on microtubules and conventional kinesin. J. Virol. 78 (2004) 7990-8001
19. Kelkar S.A., Pfister K.K., Crystal R.G., and Leopold P.L. Cytoplasmic dynein mediates adenovirus binding to microtubules. J. Virol. 78 (2004) 10122-10132
20. Kobayashi T., Martensen T., Nath J., and 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. 81 (1978) 1313-1318
21. Kristensson K., Lycke E., Roytta M., Svennerholm B., and 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. 67 Pt 9 (1986) 2023-2028
22. Lee G.E., Murray J.W., Wolkoff A.W., and Wilson D.W. Reconstitution of herpes simplex virus microtubule-dependent trafficking in vitro. J. Virol. 80 (2006) 4264-4275
23. Mabit H., Nakano M.Y., Prank U., Saam B., Dohner K., Sodeik B., and Greber U.F. Intact microtubules support adenovirus and herpes simplex virus infections. J. Virol. 76 (2002) 9962-9971
24. Naranatt P.P., Krishnan H.H., Smith M.S., and 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. 79 (2005) 1191-1206
25. Nogales E. Structural insights into microtubule function. Annu. Rev. Biochem. 69 (2000) 277-302
26. O'Callaghan D.J., Gentry G.A., and Randall C.C. The equine herpesviruses. In: Roizman B. (Ed). The Herpesviruses, Comprehensive Virology (1983), Plenum Press, New York
27. Osterrieder N. Construction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant. Virus Res. 59 (1999) 165-177
28. Palazzo A.F., Cook T.A., Alberts A.S., and Gundersen G.G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3 (2001) 723-729
29. Penningroth S.M., Cheung A., Bouchard P., Gagnon C., and Bardin C.W. Dynein ATPase is inhibited selectively in vitro by erythro-9-[3-2-(hydroxynonyl)]adenine. Biochem. Biophys. Res. Commun. 104 (1982) 234-240
30. Petit C., Giron M.L., Tobaly-Tapiero J., Bittoun P., Real E., Jacob Y., Tordo N., DE The H., and Saib A. Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116 (2003) 3433-3442
31. Piperno G., Ledizet M., and Chang X.J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 104 (1987) 289-302
32. Raghu H., Sharma-Walia N., Veettil M.V., Sadagopan S., Caballero A., Sivakumar R., VARGA L., Bottero V., and 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. 81 (2007) 7941-7959
33. Raux H., Flamand A., and Blondel D. Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74 (2000) 10212-10216
34. Ravikumar B., Acevedo-Arozena A., Imarisio S., Berger Z., Vacher C., O'kane C.J., Brown S.D., and Rubinsztein D.C. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet. 37 (2005) 771-776
35. Sodeik B., Ebersold M.W., and Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136 (1997) 1007-1021
36. Sugahara Y., Matsumura T., Kono Y., Honda E., Kida H., and 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. 142 (1997) 1849-1856
37. Suikkanen S., Aaltonen T., Nevalainen M., Valilehto O., Lindholm L., Vuento M., and Vihinen-Ranta M. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77 (2003) 10270-10279
38. Ye G.J., Vaughan K.T., Vallee R.B., and Roizman B. The herpes simplex virus 1 U(L)34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane. J. Virol. 74 (2000) 1355-1363