Cytomegalovirus induces interferon-stimulated gene expression and is attenuated by interferon in the developing brain

Journal of Virology

Volumn 81, Issue 1, 2007, Pages 332-348

  Van Den Pol, Anthony N ^a   Robek, Michael D ^a   Ghosh, Prabhat K ^a   Ozduman, Koray ^a   Bandi, Prasanthi ^a   Whim, Matthew D ^a,b   Wollmann, Guido ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; POLYINOSINIC POLYCYTIDYLIC ACID; RNA;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; BRAIN; BRAIN CELL; CELL PROTECTION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE MODEL; EMBRYO; GENE; GENE EXPRESSION; GENE INDUCTION; GLIA; HOST RESISTANCE; HUMAN; HUMAN CELL; IFIT3 GENE; INNATE IMMUNITY; LMP2 GENE; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL CULTURE; NEUROLOGIC DISEASE; NEWBORN; NONHUMAN; OAS GENE; PATCH CLAMP; PRIORITY JOURNAL; RISK FACTOR; TGTP GENE; UPREGULATION; USP18 GENE; VIRUS REPLICATION; WHOLE CELL;

ANIMALS; ANTIVIRAL AGENTS; BRAIN; CELLS, CULTURED; CYTOMEGALOVIRUS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-ALPHA; INTERFERON-BETA; INTERFERONS; MICE; NEUROGLIA; NEURONS; PATCH-CLAMP TECHNIQUES; VIRUS REPLICATION;

CYTOMEGALOVIRUS;

EID: 33845776567     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01592-06     Document Type: Article

References (66)

1. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
2. Alford, C. A., and W. J. Britt. 1996. Cytomegalovirus, p. 2493-2534. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.) Fields virology. Lippincott-Raven Publishing, New York, NY.
3. Bakhramov, A., Y. S. Boriskin, J. C. Booth, and T. B. Bolton. 1995. Activation and deactivation of membrane currents in human fibroblasts following infection with human cytomegalovirus. Biochim. Biophys. Acta 1265:143-151.
4. Bale, J. F., Jr., P. F. Bray, and W. E. Bell. 1985. Neuroradiographic abnormalities in congenital cytomegalovirus infection. Pediatr. Neurol. 1:42-47.
5. Booss, J., P. R. Dann, B. P. Griffith, and J. H. Kim. 1989. Host defense response to cytomegalovirus in the central nervous system. Am. J. Pathol. 134:71-78.
6. Britt, W. J., and L. G. Vugler. 1990. Antiviral antibody responses in mothers and their newborn infants with clinical and subclinical congenital cytomegalovirus infections. J. Infect. Dis. 161:214-219.
7. Browne, E. P., B. Wing, D. Coleman, and T. Shenk. 2001. Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J. Virol. 75:12319-12330.
8. Brutkiewicz, R. R., and R. M. Welsh. 1995. Major histocompatibility complex class I antigens and the control of viral infections by natural killer cells. J. Virol. 69:3967-3971.
9. Brutkiewicz, R. R., J. R. Bennink, J. W. Yewdell, and A. Bendelac. 1995. TAP-independent, beta2-microglobulin-dependent surface expression of functional mouse CD1.1. J. Exp. Med. 182:1913-1919.
10. Bukowski, J. F., B. A. Woda, and R. M. Welsh. 1984. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52:119-128.
11. Cardin, R. D., G. B. Abenes, C. A. Stoddart, and E. S. Mocarski. 1995. Murine cytomegalovirus IE2, an activator of gene expression, is dispensible for growth and latency in mice. Virology 209:236-241.
12. Chesler, D. A., and C. S. Reiss. 2002. The role of IFN-gamma in immune responses to viral infections of the central nervous system. Cytokine Growth Factor Rev. 13:441-454.
13. Colton, C. A., J. Yao, J. E. Keri, and D. Gilbert. 1992. Regulation of microglial function by interferons. J. Neuroimmunol. 40:89-98.
14. + exchange in human fibroblasts. Am. J. Physiol. 42:C1739-C1748.
15. DeFilippis, V. R., B. Robinson, T. M. Keck, S. G. Hansen, J. A. Nelson, and K. J. Fruh. 2006. Interferon regulatory factor 3 is necessary for induction of antiviral genes during cytomegalovirus infection. J. Virol. 80:1032-1037.
16. Delale, T., A. Paquin, C. Asselin-Paturel, M. Dalod, G. Brizard, E. E. Bates, P. Kaster, S. Chan, S. Akira, A. Vicari, C. A. Biron, G. Trinchieri, and F. Briere. 2005. MyD88-dependent and -independent murine cytomegalovirus sensing for IFN-alpha release and initiation of immune responses in vivo. J. Immunol. 175:6723-6732.
17. Delhaye, S., S. Paul, G. Blakqori, M. Minet, F. Weber, P. Staeheli, and T. Michiels. 2006. Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. USA 103:7835-7840.
18. Ehrengruber, M. U., S. Hennou, H. Bueler, H. Y. Naim, N. Deglon, and K. Lundstrom. 2001. Gene transfer into neurons from hippocampal slices: comparison of recombinant Semliki Forest virus, adenovirus, adeno-associated virus, lentivirus, and measles virus. Mol. Cell Neurosci. 17:855-871.
19. Goodin, D. S. 2005. Treatment of multiple sclerosis with human beta interferon. Int. MS J. 12:96-108.
20. Grundy (Chandler), J. E., J. S. Mackenzie, and N. F. Stanley. 1981. Influence of H-2 and non-H-2 genes on resistance to murine cytomegalovirus infection. Infect. Immunol. 32:277-286.
21. Hicks, T., K. Fowler, M. Richardson, A. Dahle, L. Adams, and R. Pass. 1993. Congenital cytomegalovirus infection and neonatal auditory screening. J. Pediatr. 123:779-782.
22. Ho, K. L., C. Gottlieb, and R. J. Zarbo. 1991. Cytomegalovirus infection of cerebral astrocytoma in an AIDS patient. Clin. Neuropathol. 10:127-133.
23. Ho, M. 1982. Human cytomegalovirus infections in immunosuppressed patients, p. 171-204. In W. B. Greenough III and T. C. Merigan (ed.), Cytomegalovirus, biology and infection. Current topics in infectious disease. Plenum Medical Books, New York, NY.
24. Jacobs, L., J. A. O'Malley, A. Freeman, R. Ekes, and P. A. Reese. 1985. Intrathecal interferon in the treatment of multiple sclerosis. Patient follow-up. Arch. Neurol. 42:841-847.
25. Jarvis, M. A., C. E. Wang, H. L. Meyers, P. P. Smith, C. L. Corless, G. J. Henderson, J. Vieira, W. J. Britt, and J. A. Nelson. 1999. Human cytomegalovirus infection of caco-2 cells occurs at the basolateral membrane and is differentiation state dependent. J. Virol. 73:4552-4560.
26. Kalil, A. C., M. P. Devetten, S. Singh, B. Lesiak, D. P. Poage, K. Bargenquast, P. Fayad, and A. G. Freifeld. 2005. Use of interferon-alpha in patients with West Nile encephalitis: report of 2 cases. Clin. Infect. Dis. 40:764-766.
27. Kern, E. R., G. A. Olsen, J. C. Overall, Jr., and L. A. Glasgow. 1978. Treatment of a murine cytomegalovirus infection with exogenous interferon, polyinosinic-polycytidylic acid, and polyinosinic-polycytidylic acid-poly-L-lysine complex. Antimicrob. Agents Chemother. 13:344-346.
28. Kielian, T. 2006. Toll-like receptors in central nervous system glial inflammation and homeostasis. J. Neurosci. Res. 83:711-730.
29. Koedood, M., A. Fichtel, P. Meier, and P. J. Mitchell. 1995. Human cytomegalovirus (CMV) immediate-early enhancer/promoter specificity during embryogenesis defines target tissue of congenital HCMV infection. J. Virol. 69:2194-2207.
30. Loh, J., D. T. Chu, A. K. O'Guin, W. M. Yokoyama, and H. W. Virgin. 2005. Natural killer cells utilize both perform and gamma interferon to regulate murine cytomegalovirus infection in the spleen and liver. J. Virol. 79:661-667.
31. Mendoza-Fernandez, V., R. D. Andrew, and C. Barajas-Lopez. 2000. Interferon-alpha inhibits long-term potentiation and unmasks a long-term depression in the rat hippocampus. Brain Res. 885:14-24.
32. Mocarski, E. 1996. Cytomegaloviruses and their replication, p. 2447-2492. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven Publishing, New York, NY.
33. Navarro, L., K. Mowen, S. Rodems, B. Weaver, N. Reich, D. Spector, and M. David. 1998. Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon-stimulated response element binding complex. Mol. Cell. Biol. 18:3796-3802.
34. Nokta, M., M. P. Fons, D. C. Eaton, and T. Albrecht. 1988. Cytomegalovirus: sodium entry and development of cytomegaly in human fibroblasts. Virology 164:411-419.
35. Olson, J. K., and S. D. Miller. 2004. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 173:3916-3924.
36. Pahl-Seibert, M. F., M. Juelch, J. Podlech, D. Thomas, P. Deegen, M. J. Reddehase, and R. Holtappels. 2005. Highly protective in vivo function of cytomegalovirus IE1 epitope-specific memory CD8 T cells purified by T-cell receptor-based cell sorting. J. Virol. 79:5400-5413.
37. Perez-Jiminez, A., V. Colamaria, A. Franco, R. Grimau-Merino, R. Darra, E. Fontana, E. Zullini, A. Beltramello, and B. Dalla-Bernardina. 1998. Epilepsy and disorders of cortical development in children with congenital cytomegalovirus infection. Rev. Neurol. 26:42-49.
38. Prehaud, C., F. Megret, M. Lafage, and M. Lafon. 2005. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J. Virol. 79:12893-12904.
39. Reuter, J. D., J. H. Wilson, K. E. Idoko, and A. N. van den Pol. 2005. CD4+ T-cell reconstitution reduces cytomegalovirus in the immunocompromised brain. J. Virol. 79:9527-9539.
40. Rugolo, M., B. Baldassarri, and M. P. Landini. 1986. Changes in membrane permeability in cells infected by human cytomegalovirus. Arch. Virol. 89:203-212.
41. Salmaggi, A., A. Dufour, A. Silvani, E. Ciusani, A. Nespolo, and A. Boiardi. 1994. Immunological fluctuations during intrathecal immunotherapy in three patients affected by CNS tumours disseminating via CSF. Int. J. Neurosci. 77:117-125.
42. Samuel, M. A., K. Whitby, B. C. Keller, A. Marri, W. Barchet, B. R. Williams, R. H. Silverman, M. Gale, Jr., and M. S. Diamond. 2006. PKR and RNase L contribute to protection against lethal West Nile Virus infection by controlling early viral spread in the periphery and replication in neurons. J. Virol. 80:7009-7019.
43. Satoh, J., and Y. Kuroda. 2001. Differing effects of IFN beta vs IFN gamma in MS: gene expression in cultured astrocytes. Neurology 57:681-685.
44. Scumpia, P. O., K. M. Kelley, W. H. Reeves, and B. R. Stevens. 2005. Double-stranded RNA signals antiviral and inflammatory programs and dysfunctional glutamate transport in TLR-3-expressing astrocytes. Glia 52:153-162.
45. Sedgwick, J. D., and W. F. Hickey. 1997. Antigen presentation in the nervous system, p. 364-418. In R. W. Keane and W. F. Mickey (ed.), Immunology of the nervous system. Oxford University Press, New York, NY.
46. Selgrade, M. J., and J. E. Osborn. 1974. Role of macrophages in resistance to murine cytomegalovirus. Infect. Immun. 10:1383-1390.
47. Servant, M. J., N. Grandvaux, and J. Hiscott. 2002. Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem. Pharmacol. 64:985-992.
48. Solomon, T. 2003. Recent advances in Japanese encephalitis. J. Neurovirol. 9:274-283.
49. Starr, S. E., and A. C. Allison. 1977. Role of T lymphocytes in recovery from murine cytomegalovirus infection. Infect. Immun. 17:458-462.
50. Stojdl, D. F., B. D. Lichty, B. R. tenOever, J. M. Paterson, A. T. Power, S. Knowles, R. Marius, J. Reynard, L. Poliquin, H. Atkins, E. G. Brown, R. K. Durbin, J. E. Durbin, J. Hiscott, and J. C. Bell. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
51. Tabeta, K., P. Georgel, E. Janssen, X. Du, K. Hoebe, K. Crozat, S. Mudd, L. Shamel, S. Sovath, J. Goode, L. Alexopoulou, R. A. Flavell, and B. Beutler. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 101:3516-3521.
52. Tedeschi, B., J. N. Barrett, and R. W. Keane. 1986. Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells. Cell Biol. 102:2244-2253.
53. Town, T., D. Jeng, L. Alexopoulou, J. Tan, and R. A. Flavell. 2006. Microglia recognize double-stranded RNA via TLR3. J. Immunol. 176:3804-3812.
54. Tsutsui, Y. 1995. Developmental disorders of the mouse brain induced by murine cytomegalovirus: animal models for congenital cytomegalovirus infection. Pathol. Int. 45:91-102.
55. Tsutsui, Y., A. Kashiwai, N. Kawamura, S. A. Aiba-Masago, and I. Kosugi. 1995. Prolonged infection of mouse brain neurons with murine cytomegalovirus after pre- and perinatal infection. Acta Virol. 140:1725-1736.
56. van den Pol, A. N., L. Kogelman, P. Ghosh, P. Liljelund, and C. Blackstone. 1994. Developmental regulation of the hypothalamic glutamate receptor mGluR1. J. Neurosci. 14:3816-3834.
57. van den Pol, A. N., E. Mocarski, N. Saederup, J. Vieira, and T. J. Meier. 1999. Cytomegalovirus cell tropism, replication, and gene transfer in brain. J. Neurosci. 19:10948-10965.
58. van den Pol, A. N., J. Vieira, D. D. Spencer, and J. G. Santarelli. 2000. Mouse cytomegalovirus in developing brain tissue-analysis of 11 species with GFP-expressing recombinant virus J. Comp. Neurol. 427:559-580.
59. van den Pol, A. N., K. Dalton, and J. Rose. 2002. Relative neurotropism of a recombinant rhabdovirus expressing a green fluorescent envelope glycoprotein. J. Virol. 76:1309-1327.
60. van den Pol, A. N., C. Acuna-Goycolea, R. Clark, and P. K. Ghosh. 2004. Physiological properties of hypothalamic MCH neurons identified with selective expression of reporter gene after recombinant virus infection. Neuron 42:635-652.
61. van den Pol, A. N., J. Reuter, and J. Santarelli. 2002. Enhanced cytomegalovirus infection of the developing brain independent of the adaptive immune system. J. Virol. 76:8842-8854.
62. White, D. O., and F. J. Fenner. 1994. Medical virology. Academic Press, New York, NY.
63. Wollmann, G., C. Acuna-Goycolea, and A. N. van den Pol. 2005. Direct excitation of hypocretin/orexin cells by extracellular ATP at P2X receptors. J. Neurophysiol. 94:2195-2206.
64. Yamada, T., M. A. Horisberger, N. Kawaguchi, I. Moroo, and T. Toyoda. 1994. Immunohistochemistry using antibodies to alpha-interferon and its induced protein, MxA, in Alzheimer's and Parkinson's disease brain tissues. Neurosci. Lett. 181:61-64.
65. Yang, S., J. Netterwald, W. Wang, and H. Zhu. 2005. Characterization of the elements and proteins responsible for interferon-stimulated gene induction by human cytomegalovirus. J. Virol. 79:5027-5034.
66. Yeow, W. S., C. M. Lawson, and M. W. Leilharz. 1998. Antiviral activities of individual murine IFN-alpha subtypes in vivo: intramuscular injection of IFN expression constructs reduces cytomegalovirus replication. J. Immunol. 160:2932-2939.