M94 is essential for the secondary envelopment of murine cytomegalovirus

Journal of Virology

Volumn 85, Issue 18, 2011, Pages 9254-9267

  Maninger, Silke ^a   Bosse, Jens Bernhard ^a   Lemnitzer, Frederic ^a   Pogoda, Madlen ^a   Mohr, Christian A ^a   von Einem, Jens ^c   Walther, Paul ^b   Koszinowski, Ulrich H ^a   Ruzsics, Zsolt ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN M99; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; CYTOMEGALOVIRUS; EMBRYO; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; LIFE CYCLE; M94 GENE; MOUSE; MUTAGENESIS; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TISSUE CULTURE; TRANSPOSON; VIROGENESIS; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS GENE; VIRUS GENOME; VIRUS MORPHOGENESIS; VIRUS REPLICATION;

DNA, VIRAL; GENE DELETION; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MUROMEGALOVIRUS; MUTAGENESIS; MUTANT PROTEINS; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS; VIRUS ASSEMBLY;

MAIZE CHLOROTIC MOTTLE VIRUS; MIRIDAE; MURID HERPESVIRUS 1;

EID: 80052507047     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00443-11     Document Type: Article

References (48)

1. Baines, J. D. 2007. Envelopment of herpes simplex virus nucleocapsids at the inner nuclear membrane, p. 144-150. In A. Arvin et al. (ed.), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
2. Baines, J. D., and B. Roizman. 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.
3. Baines, J. D., and B. Roizman. 1992. The UL11 gene of herpes simplex virus 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J. Virol. 66:5168-5174.
4. Biery, M. C., F. J. Stewart, A. E. Stellwagen, E. A. Raleigh, and N. L. Craig. 2000. A simple in vitro Tn7-based transposition system with low target site selectivity for genome and gene analysis. Nucleic Acids Res. 28:1067-1077.
5. Britt, B. 2007. Maturation and egress, p. 311-323. In A. Arvin et al. (ed.), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
6. Britt, W. J., M. Jarvis, J. Y. Seo, D. Drummond, and J. Nelson. 2004. Rapid genetic engineering of human cytomegalovirus by using a lambda phage linear recombination system: demonstration that pp28 (UL99) is essential for production of infectious virus. J. Virol. 78:539-543.
7. Bubeck, A., et al. 2004. Comprehensive mutational analysis of a herpesvirus gene in the viral genome context reveals a region essential for virus replication. J. Virol. 78:8026-8035.
8. Bubic, I., et al. 2004. Gain of virulence caused by loss of a gene in murine cytomegalovirus. J. Virol. 78:7536-7544.
9. Buser, C., P. Walther, T. Mertens, and D. Michel. 2007. Cytomegalovirus primary envelopment occurs at large infoldings of the inner nuclear membrane. J. Virol. 81:3042-3048.
10. Campadelli-Fiume, G., and L. Menotti. 2007. Entry of alphaherpesviruses into the cell, p. 93-111. In A. Arvin et al. (ed.), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
11. Cherepanov, P. P., and W. Wackernagel. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
12. Das, S., A. Vasanji, and P. E. Pellett. 2007. Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J. Virol. 81:11861-11869.
13. Davison, A. J. 2010. Herpesvirus systematics. Vet. Microbiol. 143:52-69.
14. Dunn, W., et al. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. U. S. A. 100:14223-14228.
15. Harper, A. L., et al. 2010. Interaction domains of the UL16 and UL21 tegument proteins of herpes simplex virus. J. Virol. 84:2963-2971.
16. Herskowitz, I. 1987. Functional inactivation of genes by dominant negative mutations. Nature 329:219-222.
17. Johnson, D. C., and J. D. Baines. 2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382-394.
18. Liu, Y., et al. 2009. The tegument protein UL94 of human cytomegalovirus as a binding partner for tegument protein pp28 identified by intracellular imaging. Virology 388:68-77.
19. Loomis, J. S., J. B. Bowzard, R. J. Courtney, and J. W. Wills. 2001. Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type J. Virol. 75:12209-12219.
20. Loomis, J. S., R. J. Courtney, and J. W. Wills. 2003. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 77:11417-11424.
21. Lotzerich, M., Z. Ruzsics, and U. H. Koszinowski. 2006. Functional domains of murine cytomegalovirus nuclear egress protein M53/p38. J. Virol. 80:73- 84.
22. McVoy, M. A., and S. P. Adler. 1994. Human cytomegalovirus DNA replicates after early circularization by concatemer formation, and inversion occurs within the concatemer. J. Virol. 68:1040-1051.
23. Meckes, D. G., Jr., and J. W. Wills. 2007. Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J. Virol. 81:13028- 13036.
24. Meckes, D. G., Jr., and J. W. Wills. 2008. Structural rearrangement within an enveloped virus upon binding to the host cell. J. Virol. 82:10429-10435.
25. Menard, C., et al. 2003. Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J. Virol. 77:5557-5570.
26. Mocarski, E. D. J. 2007. Comparative analysis of herpesvirus-common proteins, p. 177-203. In A. Arvin et al. (ed.), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
27. Mohr, C. A., et al. 2010. A spread-deficient cytomegalovirus for assessment of first-target cells in vaccination. J. Virol. 84:7730-7742.
28. Mohr, C. A., et al. 2008. Engineering of cytomegalovirus genomes for recombinant live herpesvirus vaccines. Int. J. Med. Microbiol. 298:115-125.
29. Mühlbach, H., C. Mohr, Z. Ruzsics, and U. Koszinowski. 2009. Dominantnegative proteins in herpesviruses-from assigning gene function to intracellular immunization. Viruses 1:420-440.
30. Muranyi, W., J. Haas, M. Wagner, G. Krohne, and U. H. Koszinowski. 2002. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297:854-857.
31. Nalwanga, D., S. Rempel, B. Roizman, and J. D. Baines. 1996. The UL 16 gene product of herpes simplex virus 1 is a virion protein that colocalizes with intranuclear capsid proteins. Virology 226:236-242.
32. Oshima, S., et al. 1998. Characterization of the UL16 gene product of herpes simplex virus type 2. Arch. Virol. 143:863-880.
33. Popa, M., et al. 2010. Dominant negative mutants of the murine cytomegalovirus M53 gene block nuclear egress and inhibit capsid maturation. J. Virol. 84:9035-9046.
34. Reddehase, M. J., et al. 1985. Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J. Virol. 55:264-273.
35. Roizman, B., et al. 1981. Herpesviridae. Definition, provisional nomenclature, and taxonomy. The Herpesvirus Study Group, the International Committee on Taxonomy of Viruses. Intervirology 16:201-217.
36. Rupp, B., et al. 2007. Random screening for dominant-negative mutants of the cytomegalovirus nuclear egress protein M50. J. Virol. 81:5508-5517.
37. Rupp, B., Z. Ruzsics, T. Sacher, and U. H. Koszinowski. 2005. Conditional cytomegalovirus replication in vitro and in vivo. J. Virol. 79:486-494.
38. Ruzsics, Z., and U. H. Koszinowski. 2008. Mutagenesis of the cytomegalovirus genome. Curr. Top. Microbiol. Immunol. 325:41-61.
39. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Scrivano, L., et al. 2010. The m74 gene product of murine cytomegalovirus (MCMV) is a functional homolog of human CMV gO and determines the entry pathway of MCMV. J. Virol. 84:4469-4480.
41. Scrivano, L., C. Sinzger, H. Nitschko, U. H. Koszinowski, and B. Adler. 2011. HCMV spread and cell tropism are determined by distinct virus populations. PLoS Pathog. 7:e1001256.
42. Silva, M. C., J. Schroer, and T. Shenk. 2005. Human cytomegalovirus cellto-cell spread in the absence of an essential assembly protein. Proc. Natl. Acad. Sci. U. S. A. 102:2081-2086.
43. Silva, M. C., Q. C. Yu, L. Enquist, and T. Shenk. 2003. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J. Virol. 77:10594-10605.
44. Wagner, M., S. Jonjic, U. H. Koszinowski, and M. Messerle. 1999. Systematic excision of vector sequences from the BAC-cloned herpesvirus genome during virus reconstitution. J. Virol. 73:7056-7060.
45. Walther, P., and A. Ziegler. 2002. Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J. Microsc. 208:3-10.
46. Wing, B. A., G. C. Lee, and E. S. Huang. 1996. The human cytomegalovirus UL94 open reading frame encodes a conserved herpesvirus capsid/tegumentassociated virion protein that is expressed with true late kinetics. J. Virol. 70:3339-3345.
47. Yeh, P. C., D. G. Meckes, Jr., and J. W. Wills. 2008. Analysis of the interaction between the UL11 and UL16 tegument proteins of herpes simplex virus. J. Virol. 82:10693-10700.
48. Yu, D., M. C. Silva, and T. Shenk. 2003. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. U. S. A. 100:12396-12401.