The mouse cytomegalovirus immediate-early 1 gene is not required for establishment of latency or for reactivation in the lungs

Journal of Virology

Volumn 83, Issue 9, 2009, Pages 4030-4038

  Busche, Andreas ^a   Marquardt, Anja ^a   Bleich, Andre ^a   Ghazal, Peter ^b   Angulo, Ana ^c   Messerle, Martin ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; EXPLANT; FEMALE; GENETIC REGULATION; GENETIC TRANSCRIPTION; IMMEDIATE EARLY GENE; IN VIVO STUDY; INCIDENCE; LUNG; LUNG INFECTION; MEMORY T LYMPHOCYTE; MOUSE; MUTANT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RECURRENT INFECTION; TRANSCRIPTION INITIATION; VIRUS EXPRESSION; VIRUS GENOME; VIRUS LATENCY; VIRUS REACTIVATION; WILD TYPE;

ANIMALS; CELLS, CULTURED; FEMALE; GENE DELETION; GENOME, VIRAL; HERPESVIRIDAE INFECTIONS; IMMEDIATE-EARLY PROTEINS; LUNG; MICE; MICE, INBRED BALB C; MUROMEGALOVIRUS; MUTATION; TIME FACTORS; VIRUS ACTIVATION; VIRUS LATENCY;

CYTOMEGALOVIRUS; MAIZE CHLOROTIC MOTTLE VIRUS; MUS;

EID: 66149155356     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02520-08     Document Type: Article

References (64)

1. Ahn, J. H., E. J. Brignole, and G. S. Hayward. 1998. Disruption of PML subnuclear domains by the acidic IE1 protein of human cytomegalovirus is mediated through interaction with PML and may modulate a RING finger-dependent cryptic transactivator function of PML. Mol. Cell. Biol. 18:4899-4913. (Pubitemid 28343073)
2. Balthesen, M., M. Messerle, and M. J. Reddehase. 1993. Lungs are a major organ site of cytomegalovirus latency and recurrence. J. Virol. 67:5360-5366. (Pubitemid 23241369)
3. Bego, M., J. Maciejewski, S. Khaiboullina, G. Pari, and S. St. Jeor. 2005. Characterization of an antisense transcript spanning the UL81-82 locus of human cytomegalovirus. J. Virol. 79:11022-11034. (Pubitemid 41170643)
4. + cells from healthy subjects carry a circular conformation of latent cytomegalovirus genome. Blood 93:394-398.
5. Britt, W. 2006. Human cytomegalovirus infections and mechanisms of disease, p. 1-28. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, Norfolk, United Kingdom.
6. Brune, W., H. Hengel, and U. H. Koszinowski. 1999. A mouse model for cytomegalovirus infection, p. 19.7.1-19.7.13. In J. E. Coligan, B. E. Bierer, D. H. Margulies, E. M. Shevach, and W. Strober (ed.), Current protocols in immunology. John Wiley & Sons, New York, NY.
7. Busche, A., A. Angulo, P. Kay-Jackson, P. Ghazal, and M. Messerle. 2008. Phenotypes of major immediate-early gene mutants of mouse cytomegalovirus. Med. Microbiol. Immunol. 197:233-240.
8. Cook, C. H., J. Trgovcich, P. D. Zimmerman, Y. Zhang, and D. D. Sedmak. 2006. Lipopolysaccharide, tumor necrosis factor alpha, or interleukin-1β triggers reactivation of latent cytomegalovirus in immunocompetent mice. J. Virol. 80:9151-9158.
9. Gandhi, M. K., M. R. Wills, J. G. Sissons, and A. J. Carmichael. 2003. Human cytomegalovirus-specific immunity following haemopoietic stem cell transplantation. Blood Rev. 17:259-264. (Pubitemid 37356397)
10. Ghazal, P., A. E. Visser, M. Gustems, R. Garcia, E. M. Borst, K. Sullivan, M. Messerle, and A. Angulo. 2005. Elimination of ie1 significantly attenuates murine cytomegalovirus virulence but does not alter replicative capacity in cell culture. J. Virol. 79:7182-7194. (Pubitemid 40677348)
11. Gold, M. C., M. W. Munks, M. Wagner, C. W. McMahon, A. Kelly, D. G. Kavanagh, M. K. Slifka, U. H. Koszinowski, D. H. Raulet, and A. B. Hill. 2004. Murine cytomegalovirus interference with antigen presentation has little effect on the size or the effector memory phenotype of the CD8 T cell response. J. Immunol. 172:6944-6953. (Pubitemid 38669134)
12. Goodrum, F., M. Reeves, J. Sinclair, K. High, and T. Shenk. 2007. Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro. Blood 110:937-945.
13. Greaves, R. F., and E. S. Mocarski. 1998. Defective growth correlates with reduced accumulation of a viral DNA replication protein after low-multiplicity infection by a human cytomegalovirus ie1 mutant. J. Virol. 72:366-379. (Pubitemid 28048848)
14. Grzimek, N. K., D. Dreis, S. Schmalz, and M. J. Reddehase. 2001. Random, asynchronous, and asymmetric transcriptional activity of enhancer-flanking major immediate-early genes ie1/3 and ie2 during murine cytomegalovirus latency in the lungs. J. Virol. 75:2692-2705.
15. Gustems, M., A. Busche, M. Messerle, P. Ghazal, and A. Angulo. 2008. In vivo competence of murine cytomegalovirus under the control of the human cytomegalovirus major immediate-early enhancer in the establishment of latency and reactivation. J. Virol. 82:10302-10307.
16. lo memory-effector cell pool during latent murine cytomegalovirus infection of the lungs. J. Virol. 74:11495-11503.
17. Holtappels, R., D. Thomas, J. Podlech, and M. J. Reddehase. 2002. Two antigenic peptides from genes m123 and m164 of murine cytomegalovirus quantitatively dominate CD8 T-cell memory in the H-2d haplotype. J. Virol. 76:151-164. (Pubitemid 33139001)
18. Huh, Y. H., Y. E. Kim, E. T. Kim, J. J. Park, M. J. Song, H. Zhu, G. S. Hayward, and J. H. Ahn. 2008. Binding STAT2 by the acidic domain of human cytomegalovirus IE1 promotes viral growth and is negatively regulated by SUMO. J. Virol. 82:10444-10454. (Pubitemid 352691174)
19. Hummel, M., and M. M. Abecassis. 2002. A model for reactivation of CMV from latency. J. Clin. Virol. 25(Suppl. 2):S123-S136. (Pubitemid 35287198)
20. Hummel, M., Z. Zhang, S. Yan, I. DePlaen, P. Golia, T. Varghese, G. Thomas, and M. I. Abecassis. 2001. Allogeneic transplantation induces expression of cytomegalovirus immediate-early genes in vivo: a model for reactivation from latency. J. Virol. 75:4814-4822.
21. Jarvis, M. A., and J. A. Nelson. 2002. Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr. Opin. Microbiol. 5:403-407.
22. Jenkins, C., A. Abendroth, and B. Slobedman. 2004. A novel viral transcript with homology to human interleukin-10 is expressed during latent human cytomegalovirus infection. J. Virol. 78:1440-1447. (Pubitemid 38095854)
23. Jonjić, S., I. Pavić, B. Polić, I. Crnković, P. Lucin, and U. H. Koszinowski. 1994. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J. Exp. Med. 179:1713-1717. (Pubitemid 24129592)
24. + T cells over time. J. Immunol. 170:2022-2029.
25. Keil, G. M., K. A. Ebeling, and U. H. Koszinowski. 1987. Sequence and structural organization of murine cytomegalovirus immediate-early gene 1. J. Virol. 61:1901-1908. (Pubitemid 17080212)
26. Korioth, F., G. G. Maul, B. Plachter, T. Stamminger, and J. Frey. 1996. The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp. Cell Res. 229:155-158. (Pubitemid 26423944)
27. Kurz, S. K., M. Rapp, H. P. Steffens, N. K. Grzimek, S. Schmalz, and M. J. Reddehase. 1999. Focal transcriptional activity of murine cytomegalovirus during latency in the lungs. J. Virol. 73:482-494. (Pubitemid 28565393)
28. Lee, H. R., D. J. Kim, J. M. Lee, C. Y. Choi, B. Y. Ahn, G. S. Hayward, and J. H. Ahn. 2004. Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells. J. Virol. 78:6527-6542. (Pubitemid 38715951)
29. Lehming, N., A. Le Saux, J. Schuller, and M. Ptashne. 1998. Chromatin components as part of a putative transcriptional repressing complex. Proc. Natl. Acad. Sci. USA 95:7322-7326.
30. Maul, G. G. 2008. Initiation of cytomegalovirus infection at ND10. Curr. Top. Microbiol. Immunol. 325:117-132.
31. Maul, G. G., and D. Negorev. 2008. Differences between mouse and human cytomegalovirus interactions with their respective hosts at immediate early times of the replication cycle. Med. Microbiol. Immunol. 197:241-249.
32. Meier, J. L., and M. F. Stinski. 2006. Major immediate-early enhancer and its gene products, p. 151-166. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, Norfolk, United Kingdom.
33. Messerle, M., B. Bühler, G. M. Keil, and U. H. Koszinowski. 1992. Structural organization, expression, and functional characterization of the murine cytomegalovirus immediate-early gene 3. J. Virol. 66:27-36.
34. 491aa is replication defective due to a failure in autoregulation. Proc. Natl. Acad. Sci. USA 93:11321-11326.
35. Mocarski, E. S., T. Shenk, and R. F. Pass. 2007. Cytomegaloviruses, p. 2702-2772. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott Williams & Wilkins, Philadelphia, PA.
36. Munks, M. W., K. S. Cho, A. K. Pinto, S. Sierro, P. Klenerman, and A. B. Hill. 2006. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177:450-458. (Pubitemid 43939158)
37. Nevels, M., C. Paulus, and T. Shenk. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. USA 101:17234-17239.
38. Nicklas, W., P. Baneux, R. Boot, T. Decelle, A. A. Deeny, M. Fumanelli, and B. Illgen-Wilcke. 2002. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab. Anim. 36:20-42. (Pubitemid 34073119)
39. Paulus, C., S. Krauss, and M. Nevels. 2006. A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc. Natl. Acad. Sci. USA 103:3840-3845.
40. Polić, B., H. Hengel, A. Krmpotić, J. Trgovcich, I. Pavić, P. Luccaronin, S. Jonjić, and U. H. Koszinowski. 1998. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J. Exp. Med. 188:1047-1054. (Pubitemid 28443328)
41. Presti, R. M., J. L. Pollock, A. J. Dal Canto, A. K. O'Guin, and H. W. Virgin. 1998. Interferon gamma regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels. J. Exp. Med. 188:577-588. (Pubitemid 28369146)
42. Reddehase, M. J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2:831-844.
43. Reddehase, M. J., M. Balthesen, M. Rapp, S. Jonjić, I. Pavić, and U. H. Koszinowski. 1994. The conditions of primary infection define the load of latent viral genome in organs and the risk of recurrent cytomegalovirus disease. J. Exp. Med. 179:185-193. (Pubitemid 24012983)
44. Reddehase, M. J., J. Podlech, and N. K. Grzimek. 2002. Mouse models of cytomegalovirus latency: overview. J. Clin. Virol. 25(Suppl. 2):S23-S36. (Pubitemid 35287189)
45. Reddehase, M. J., C. O. Simon, C. K. Seckert, N. Lemmermann, and N. K. Grzimek. 2008. Murine model of cytomegalovirus latency and reactivation. Curr. Top. Microbiol. Immunol. 325:315-331.
46. Reddehase, M. J., F. Weiland, K. Munch, S. Jonjić, A. Luske, and U. H. Koszinowski. 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.
47. Reeves, M., and J. Sinclair. 2008. Aspects of human cytomegalovirus latency and reactivation. Curr. Top. Microbiol. Immunol. 325:297-313.
48. 491aa contains an acidic domain that plays a regulatory role and a chromatin-tethering domain that is dispensable during viral replication. J. Virol. 79:225-233.
49. Simon, C. O., R. Holtappels, H. M. Tervo, V. Bohm, T. Daubner, S. A. Oehrlein-Karpi, B. Kuhnapfel, A. Renzaho, D. Strand, J. Podlech, M. J. Reddehase, and N. K. Grzimek. 2006. CD8 T cells control cytomegalovirus latency by epitope-specific sensing of transcriptional reactivation. J. Virol. 80:10436-10456. (Pubitemid 44628891)
50. Simon, C. O., C. K. Seckert, D. Dreis, M. J. Reddehase, and N. K. Grzimek. 2005. Role for tumor necrosis factor alpha in murine cytomegalovirus transcriptional reactivation in latently infected lungs. J. Virol. 79:326-340. (Pubitemid 39648387)
51. Snyder, C. M., K. S. Cho, E. L. Bonnett, S. van Dommelen, G. R. Shellam, and A. B. Hill. 2008. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29:650-659.
52. Stenberg, R. M. 1996. The human cytomegalovirus major immediate-early gene. Intervirology 39:343-349.
53. Stinski, M. F., and H. Isomura. 2008. Role of the cytomegalovirus major immediate early enhancer in acute infection and reactivation from latency. Med. Microbiol. Immunol. 197:223-231.
54. Tanaka, K., S. Sawamura, T. Satoh, K. Kobayashi, and S. Noda. 2007. Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J. Immunol. 178:5209-5216. (Pubitemid 46595305)
55. Tang, Q., and G. G. Maul. 2003. Mouse cytomegalovirus immediate-early protein 1 binds with host cell repressors to relieve suppressive effects on viral transcription and replication during lytic infection. J. Virol. 77:1357-1367. (Pubitemid 36055558)
56. Tang, Q., and G. G. Maul. 2006. Immediate-early interactions and epigenetic defense mechanisms, p. 131-149. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, Norfolk, United Kingdom.
57. Tavalai, N., P. Papior, S. Rechter, M. Leis, and T. Stamminger. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018. (Pubitemid 44182301)
58. Tavalai, N., P. Papior, S. Rechter, and T. Stamminger. 2008. Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J. Virol. 82:126-137. (Pubitemid 350309130)
59. Wagner, M., S. Jonjić, 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. (Pubitemid 29327894)
60. Waller, E. C., E. Day, J. G. Sissons, and M. R. Wills. 2008. Dynamics of T cell memory in human cytomegalovirus infection. Med. Microbiol. Immunol. 197:83-96.
61. 2 arrest in murine cytomegalovirus-infected cells. J. Virol. 82: 10188-10198.
62. Wilhelmi, V., C. O. Simon, J. Podlech, V. Bohm, T. Daubner, S. Emde, D. Strand, A. Renzaho, N. A. Lemmermann, C. K. Seckert, M. J. Reddehase, and N. K. Grzimek. 2008. Transactivation of cellular genes involved in nucleotide metabolism by the regulatory IE1 protein of murine cytomegalovirus is not critical for viral replicative fitness in quiescent cells and host tissues. J. Virol. 82:9900-9916.
63. Wilkinson, G. W., C. Kelly, J. H. Sinclair, and C. Rickards. 1998. Disruption of PML-associated nuclear bodies mediated by the human cytomegalovirus major immediate early gene product. J. Gen. Virol. 79:1233-1245. (Pubitemid 28203865)
64. Wu, W. S., S. Vallian, E. Seto, W. M. Yang, D. Edmondson, S. Roth, and K. S. Chang. 2001. The growth suppressor PML represses transcription by functionally and physically interacting with histone deacetylases. Mol. Cell. Biol. 21:2259-2268. (Pubitemid 32222080)