Marek's disease virus expresses multiple UL44 (gC) variants through mrna splicing that are all required for efficient horizontal transmission

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 7896-7906

  Jarosinski, Keith W ^a,b   Osterrieder, Nikolaus ^a,c  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN C 104; GLYCOPROTEIN C 145; MESSENGER RNA; PROTEIN C; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHICKEN; CONTROLLED STUDY; DISEASE TRANSMISSION; EMBRYO; IN VITRO STUDY; INTRON; MARDIVIRUS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; STOP CODON; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TRANSMISSION;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, VIRAL; CELL LINE; CELL MEMBRANE; CHICK EMBRYO; CHICKENS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 3, GALLID; MAREK DISEASE; POULTRY DISEASES; PROTEIN STRUCTURE, TERTIARY; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

GALLID HERPESVIRUS 2; GALLUS GALLUS;

EID: 84864392482     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00908-12     Document Type: Article

References (54)

1. Abramoff MD, Magalhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
2. Allen GP, Coogle LD. 1988. Characterization of an equine herpesvirus type 1 gene encoding a glycoprotein (gp13) with homology to herpes simplex virus glycoprotein C. J. Virol. 62:2850-2858.
3. Amor S, et al. 2011. ICP27 protein of Marek's disease virus interacts with SR proteins and inhibits the splicing of cellular telomerase chTERT and viral vIL8 transcripts. J. Gen. Virol. 92:1273-1278.
4. Arvin AM. 1996. Varicella-zoster virus: overview and clinical manifestations. Semin. Dermatol. 15:4-7.
5. Baines JD, Roizman B. 1991. The open reading frames UL3, UL4, UL10, and UL16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J. Virol. 65:938-944.
6. Balan P, et al. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75:1245-1258.
7. Black DL. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
8. Blondeau C, et al. 2007. A full UL13 open reading frame in Marek's disease virus (MDV) is dispensable for tumor formation and feather follicle tropism and cannot restore horizontal spread in rRB-1B in vivo. Vet. Res. 38:419-433.
9. Brunovskis P, Velicer LF. 1995. The Marek's disease virus (MDV) unique short region: alphaherpesvirus-homologous, fowlpox virus-homologous, and MDV-specific genes. Virology 206:324-338.
10. Bulow VV, Biggs PM. 1975. Differentiation between strains of Marek's disease virus and turkey herpesvirus by immunofluorescence assays. Avian Pathol. 4:133-146.
11. Burge CB, Padgett RA, Sharp PA. 1998. Evolutionary fates and origins of U12-type introns. Mol. Cell 2:773-785.
12. Calnek BW. 2001. Pathogenesis of Marek's disease virus infection, p 25-55. In Hirai K (ed), Marek's disease. Springer, Berlin, Germany.
13. Calnek BW, Adldinger HK, Kahn DE. 1970. Feather follicle epithelium: a source of enveloped and infectious cell-free herpesvirus from Marek's disease. Avian Dis. 14:219-233.
14. Churchill AE, Chubb RC, Baxendale W. 1969. The attenuation, with loss of oncogenicity, of the herpes-type virus of Marek's disease (strain HPRS-16) on passage in cell culture. J. Gen. Virol. 4:557-564.
15. Cohen JI, Nguyen H. 1997. Varicella-zoster virus glycoprotein I is essential for growth of virus in Vero cells. J. Virol. 71:6913-6920.
16. Cohen JI, Seidel K. 1994. Varicella-zoster virus (VZV) open reading frame 10 protein, the homolog of the essential herpes simplex virus protein VP16, is dispensable for VZV replication in vitro. J. Virol. 68:7850-7858.
17. Davison AJ, et al. 2009. The order Herpesvirales. Arch. Virol. 154:171-177.
18. Davison AJ, McGeoch DJ. 1986. Evolutionary comparisons of the S segments in the genomes of herpes simplex virus type 1 and varicellazoster virus. J. Gen. Virol. 67:597-611.
19. del Rio T, Werner HC, Enquist LW. 2002. The pseudorabies virus VP22 homologue (UL49) is dispensable for virus growth in vitro and has no effect on virulence and neuronal spread in rodents. J. Virol. 76:774-782.
20. Dijkstra JM, Visser N, Mettenleiter TC, Klupp BG. 1996. Identification and characterization of pseudorabies virus glycoprotein gM as a nonessential virion component. J. Virol. 70:5684-5688.
21. Dorange F, Tischer BK, Vautherot JF, Osterrieder N. 2002. Characterization of Marek's disease virus serotype 1 (MDV-1) deletion mutants that lack UL46 to UL49 genes: MDV-1 UL49, encoding VP22, is indispensable for virus growth. J. Virol. 76:1959-1970.
22. Eisenberg RJ, et al. 1987. Complement component C3B binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb. Pathog. 3:423-435.
23. Elliott G, Hafezi W, Whiteley A, Bernard E. 2005. Deletion of the herpes simplex virus VP22-encoding gene (UL49) alters the expression, localization, and virion incorporation of ICP0. J. Virol. 79:9735-9745.
24. Feenstra V, Hodaie M, Johnson DC. 1990. Deletions in herpes simplex virus glycoprotein D define nonessential and essential domains. J. Virol. 64:2096-2102.
25. Friedman HM, Cohen GH, Eisenberg RJ, Seidel CA, Cines DB. 1984. Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3B complement component on infected cells. Nature 309:633-635.
26. Fries LF, et al. 1986. Glycoprotein C of herpes simplex virus 1 is an inhibitor of the complement cascade. J. Immunol. 137:1636-1641.
27. Fuchs W, Granzow H, Klupp BG, Kopp M, Mettenleiter TC. 2002. The UL48 tegument protein of pseudorabies virus is critical for intracytoplasmic assembly of infectious virions. J. Virol. 76:6729-6742.
28. Huemer HP, Larcher C, Coe NE. 1992. Pseudorabies virus glycoprotein III (gIII) derived from virions and infected cells binds to the 3rd component of complement. Virus Res. 23:271-280.
29. Huemer HP, Larcher C, van Drunen Littel-van den Hurk Babiuk LA. 1993. Species selective interaction of Alphaherpesvirinae with the "unspecific" immune system of the host. Arch. Virol. 130:353-364.
30. Huemer HP, Nowotny N, Crabb BS, Meyer H, Hubert PH. 1995. gp13 (EHV-gC): a complement receptor induced by equine herpesviruses. Virus Res. 37:113-126.
31. Ikuta K, Ueda S, Kato S, Hirai K. 1983. Monoclonal antibodies reactive with the surface and secreted glycoproteins of Marek's disease virus and herpesvirus of turkeys. J. Gen. Virol. 64:2597-2610.
32. Ikuta K, Ueda S, Kato S, Hirai K. 1983. Most virus-specific polypeptides in cells productively infected with Marek's disease virus or herpesvirus of turkeys possess cross-reactive determinants. J. Gen. Virol. 64:961-965.
33. Isfort RJ, Stringer RA, Kung HJ, Velicer LF. 1986. Synthesis, processing, and secretion of the Marek's disease herpesvirus A antigen glycoprotein. J. Virol. 57:464-474.
34. Jarosinski K, Kattenhorn L, Kaufer B, Ploegh H, Osterrieder N. 2007. A herpesvirus ubiquitin-specific protease is critical for efficient T cell lymphoma formation. Proc. Natl. Acad. Sci. U. S. A. 104:20025-20030.
35. Jarosinski KW, et al. 2007. Horizontal transmission of Marek's disease virus requires US2, the UL13 protein kinase, and gC. J. Virol. 81:10575-10587.
36. Jarosinski KW, O'Connell PH, Schat KA. 2003. Impact of deletions within the BamHI-L fragment of attenuated Marek's disease virus on vIL-8 expression and the newly identified transcript of open reading frame LORF4. Virus Genes 26:255-269.
37. Jarosinski KW, Osterrieder N. 2010. Further analysis of Marek's disease virus horizontal transmission confirms that UL44 (gC) and UL13 protein kinase activity are essential, while US2 is nonessential. J. Virol. 84:7911-7916.
38. Jarosinski KW, Osterrieder N, Nair VK, Schat KA. 2005. Attenuation of Marek's disease virus by deletion of open reading frame RLORF4 but not RLORF5a. J. Virol. 79:11647-11659.
39. Jarosinski KW, Tischer BK, Trapp S, Osterrieder N. 2006. Marek's disease virus: lytic replication, oncogenesis and control. Expert Rev. Vaccines 5:761-772.
40. Karger A, Mettenleiter TC. 1993. Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 194:654-664.
41. Kinchington PR, et al. 1990. A possible role for glycoprotein gpV in the pathogenesis of varicella-zoster virus, p 83-91. In Lopez C, et al (ed), Immunobiology and prophylaxis of human herpesvirus infections. Plenum Press, New York, NY.
42. Kostavasili I, et al. 1997. Mechanism of complement inactivation by glycoprotein C of herpes simplex virus. J. Immunol. 158:1763-1771.
43. Liang X, et al. 1995. Characterization of bovine herpesvirus 1 UL49 homolog gene and product: bovine herpesvirus 1 UL49 homolog is dispensable for virus growth. J. Virol. 69:3863-3867.
44. Liang X, Tang M, Manns B, Babiuk LA, Zamb TJ. 1993. Identification and deletion mutagenesis of the bovine herpesvirus 1 dUTPase gene and a gene homologous to herpes simplex virus UL49.5. Virology 195:42-50.
45. Liang XP, Pyne C, Li YH, Babiuk LA, Kowalski J. 1995. Delineation of the essential function of bovine herpesvirus-1 gD-an indication for the modulatory role of gD in virus entry. Virology 207:429-441.
46. Lubinski J, Nagashunmugam T, Friedman HM. 1998. Viral interference with antibody and complement. Semin. Cell Dev. Biol. 9:329-337.
47. Lubinski J, et al. 1999. In vivo role of complement-interacting domains of herpes simplex virus type 1 glycoprotein gC. J. Exp. Med. 190:1637-1646.
48. Lubinski JM, et al. 2002. Herpes simplex virus type 1 evades the effects of antibody and complement in vivo. J. Virol. 76:9232-9241.
49. Mallory S, Sommer M, Arvin AM. 1997. Mutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein E conformation and trafficking. J. Virol. 71:8279-8288.
50. Mallory S, Sommer M, Arvin AM. 1998. Analysis of the glycoproteins I and E of varicella-zoster virus (VZV) using deletional mutations of VZV cosmids. J. Infect. Dis. 178:S22-S26.
51. Mettenleiter TC. 1989. Glycoprotein gIII deletion mutants of pseudorabies virus are impaired in virus entry. Virology 171:623-625.
52. Mijnes JD, et al. 1996. Biosynthesis of glycoproteins E and I of feline herpesvirus: gE-gI interaction is required for intracellular transport. J. Virol. 70:5466-5475.
53. Moffat JF, et al. 1998. Attenuation of the vaccine Oka strain of varicellazoster virus and role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. J. Virol. 72:965-974.
54. Mossman KL, Sherburne R, Lavery C, Duncan J, Smiley JR. 2000. Evidence that herpes simplex virus VP16 is required for viral egress downstream of the initial envelopment event. J. Virol. 74:6287-6299.