Major histocompatibility complex haplotype determines hsp70-dependent protection against measles virus neurovirulence

Journal of Virology

Volumn 83, Issue 11, 2009, Pages 5544-5555

  Carsillo, Thomas ^a   Carsillo, Mary ^a   Traylor, Zachary ^a   Rajala Schultz, Päivi ^a   Popovich, Phillip ^a   Niewiesk, Stefan ^a   Oglesbee, Michael ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; HEAT SHOCK PROTEIN 72;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFECTION; C57BL 6 MOUSE; CELL POPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; FEMALE; FEVER; GENE EXPRESSION; GENE OVEREXPRESSION; HAPLOTYPE; HOST; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VITRO STUDY; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEASLES; MEASLES VIRUS; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; VIRUS ACTIVATION; VIRUS VIRULENCE; ANIMAL; BRAIN DISEASE; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PATHOLOGY; SURVIVAL RATE; VIRULENCE;

MEASLES VIRUS; MUS; MUS MUSCULUS;

ANIMALS; BRAIN DISEASES; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; HAPLOTYPES; HSP72 HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, INNATE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEASLES; MEASLES VIRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SURVIVAL RATE; T-LYMPHOCYTE SUBSETS; VIRULENCE;

EID: 66149143616     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02673-08     Document Type: Article

References (58)

1. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511. (Pubitemid 38931765)
2. Awad, H., Z. Suntres, J. Heijmans, D. Smeak, V. Bergdall-Costell, F. L. Christofi, C. Magro, and M. Oglesbee. 2008. Intracellular and extracellular expression of the major inducible 70kDa heat shock protein in experimental ischemia-reperfusion injury of the spinal cord. Exp. Neurol. 212:275-284.
3. Bieback, K., E. Lien, I. M. Klagge, E. Avota, J. Schneider-Schaulies, W. P. Duprex, H. Wagner, C. J. Kirschning, V. ter Meulen, and S. Schneider- Schaulies. 2002. Hemagglutinin protein of wild-type measles virus activates Toll-like receptor 2 signaling. J. Virol. 76:8729-8736.
4. Bourhis, J. M., B. Canard, and S. Longhi. 2006. Structural disorder within the replicative complex of measles virus: functional implications. Virology 344:94-110. (Pubitemid 41818949)
5. Brannan, C. A., and M. R. Roberts. 2004. Resident microglia from adult mice are refractory to nitric oxide-inducing stimuli due to impaired NOS2 gene expression. Glia 48:120-131. (Pubitemid 39545944)
6. Brooks, G. F., J. S. Butel, and S. A. Morse. 1998. Paramyxovirus and rubella virus, p. 507-527. In J. P. Butler, J. Ransom, and E. Ryan (ed.), Adelberg's microbiology. Appleton and Lange, Stamford, CT.
7. Carsillo, T., M. Carsillo, S. Niewiesk, D. Vasconcelos, and M. Oglesbee. 2004. Hyperthermic pre-conditioning promotes measles virus clearance from brain in a mouse model of persistent infection. Brain Res. 1004:73-82. (Pubitemid 38368063)
8. Carsillo, T., Z. Traylor, C. Choi, S. Niewiesk, and M. Oglesbee. 2006. Hsp72 - a host determinant of measles virus neurovirulence. J. Virol. 80:11031-11039. (Pubitemid 44706544)
9. Carsillo, T., X. Zhang, D. Vasconcelos, S. Niewiesk, and M. Oglesbee. 2006. A single codon in the nucleocapsid protein C terminus contributes to in vitro and in vivo fitness of Edmonston measles virus. J. Virol. 80:2904-2912. (Pubitemid 43346385)
10. Cattaneo, R., G. Rebmann, K. Baczko, V. ter Meulen, and M. A. Billeter. 1987. Altered ratios of measles virus transcripts in diseased human brains. Virology 160:523-526.
11. Cztonkowska, A., M. Klos, and B. Iwinska. 1986. Lack of relationship between the HLA system and subacute sclerosing panencephalitis. Acta Neurol. Scand. 73:304-305. (Pubitemid 16124056)
12. Esiri, M. M., and P. G. Kennedy. 1997. Viral diseases, p. 3-63. In D. I. Graham and P. L. Lantos (ed.), Greenfield's neuropathology. Arnold, New York, NY.
13. Esiri, M. M., D. R. Oppenheimer, B. Brownell, and M. Haire. 1982. Distribution of measles antigen and immunoglobulin-containing cells in the CNS in subacute sclerosing panencephalitis (SSPE) and atypical measles encephalitis. J. Neurol. Sci. 53:29-43. (Pubitemid 12237492)
14. Finke, D., U. G. Brinckmann, V. ter Meulen, and U. G. Liebert. 1995. Gamma interferon is a major mediator of antiviral defense in experimental measles virus-induced encephalitis. J. Virol. 69:5469-5474.
15. Finke, D., and U. G. Liebert. 1994. CD4+ T cells are essential in overcoming experimental murine measles encephalitis. Immunology 83:184-189. (Pubitemid 24315585)
16. Freeman, A. F., D. A. Jacobsohn, S. T. Shulman, W. J. Bellini, P. Jaggi, G. de Leon, G. F. Keating, F. Kim, L. M. Pachman, M. Kletzel, and R. E. Duerst. 2004. A new complication of stem cell transplantation: measles inclusion body encephalitis. Pediatrics 114:e657-e660. (Pubitemid 41647672)
17. Griffin, D. E., J. Mullinix, O. Narayan, and R. T. Johnson. 1974. Age dependence of viral expression: comparative pathogenesis of two rodentadapted strains of measles virus in mice. Infect. Immun. 9:690-695.
18. Haspel, M. V., and F. Rapp. 1975. Measles virus: an unwanted variant causing hydrocephalus. Science 187:450-451.
19. Hutchins, S. S., M. J. Papania, R. Amler, E. F. Maes, M. Grabowsky, K. Bromberg, V. Glasglow, T. Speed, W. J. Bellini, and W. A. Orenstein. 2004. Evaluation of the measles clinical case definition. J. Infect. Dis. 189(Suppl. 1):S153-S159. (Pubitemid 38639583)
20. Jones, T. B., D. M. Basso, A. Sodhi, J. Z. Pan, R. P. Hart, R. C. MacCallum, S. Lee, C. C. Whitacre, and P. G. Popovich. 2002. Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J. Neurosci. 22:2690-2700. (Pubitemid 37465818)
21. Kakimura, J., Y. Kitamura, K. Takata, M. Umeki, S. Suzuki, K. Shibagaki, T. Taniguchi, Y. Nomura, P. J. Gebicke-Haerter, M. A. Smith, G. Perry, and S. Shimohama. 2002. Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins. FASEB J. 16:601-603. (Pubitemid 44793415)
22. Katayama, Y., H. Hotta, A. Nishimura, Y. Tatsuno, and M. Homma. 1995. Detection of measles virus nucleoprotein mRNA in autopsied brain tissues. J. Gen. Virol. 76:3201-3204. (Pubitemid 26003134)
23. Kawanokuchi, J., T. Mizuno, H. Takeuchi, H. Kato, J. Wang, N. Mitsuma, and A. Suzumura. 2006. Production of interferon-gamma by microglia. Mult. Scler. 12:558-564.
24. Kimura, T., and D. E. Griffin. 2003. Extensive immune-mediated hippocampal damage in mice surviving infection with neuroadapted Sindbis virus. Virology 311:28-39. (Pubitemid 36794207)
25. Lawrence, D. M., M. M. Vaughn, A. R. Belman, J. S. Cole, and G. F. Rall. 1999. Immune response-mediated protection of adult but not neonatal mice from neuron-restricted measles virus infection and central nervous system disease. J. Virol. 73:1795-1801. (Pubitemid 29098078)
26. Lemstra, A. W., J. C. Groen in't Woud, J. J. Hoozemans, E. S. van Haastert, A. J. Rozemuller, P. Eikelenboom, and W. A. van Gool. 2007. Microglia activation in sepsis: a case-control study. J. Neuroinflamm. 4:4.
27. Longbrake, E. E., W. Lai, D. P. Ankeny, and P. G. Popovich. 2007. Characterization and modeling of monocyte-derived macrophages after spinal cord injury. J. Neurochem. 102:1083-1094. (Pubitemid 47174229)
28. Matthews, V. B., F. T. Christiansen, and P. Price. 2000. Lymphocytes from H2 mice produce lower levels of several cytokines than congenic H2 or H2 mice. Immunol. Cell Biol. 78:247-253. (Pubitemid 30415460)
29. Matthews, V. B., and P. Price. 2000. The H2(b) haplotype modifies the production of pro-inflammatory cytokines: implications for immunopathology. Eur. Cytokine Netw. 11:640-646. (Pubitemid 32044249)
30. Mayer, M. P. 2005. Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev. Physiol. Biochem. Pharmacol. 153:1-46.
31. Milner, C. M., and R. D. Campbell. 1990. Structure and expression of the three MHC-linked HSP70 genes. Immunogenetics 32:242-251. (Pubitemid 20370377)
32. Moehler, M., M. Zeidler, J. Schede, J. Rommelaere, P. R. Galle, J. J. Cornelis, and M. Heike. 2003. Oncolytic parvovirus H1 induces release of heat-shock protein HSP72 in susceptible human tumor cells but may not affect primary immune cells. Cancer Gene Ther. 10:477-480. (Pubitemid 36667134)
33. Mori, A. 1968. Hereditary hydrocephalus in C57BL mouse. Brain Nerve 20:695-700.
34. Morrison-Bogorad, M., A. L. Zimmerman, and S. Pardue. 1995. Heat-shock 70 messenger RNA levels in human brain: correlation with agonal fever. J. Neurochem. 64:235-246.
35. Neumeister, C., and S. Niewiesk. 1998. Recognition of measles virus-infected cells by CD8+ T cells depends on the H-2 molecule. J. Gen. Virol. 79:2583-2591. (Pubitemid 28497610)
36. Niewiesk, S., U. Brinckmann, B. Bankamp, S. Sirak, U. G. Liebert, and V. ter Meulen. 1993. Susceptibility to measles virus-induced encephalitis in mice correlates with impaired antigen presentation to cytotoxic T lymphocytes. J. Virol. 67:75-81.
37. Oglesbee, M. 2007. Nucleocapsid protein interactions with the major inducible 70 kDa heat shock protein, p. 53-98. In S. Longhi (ed.), Measles virus nucleoprotein. Nova Science Publishers, Hauppauge, NY.
38. Oglesbee, M., S. Ringler, and S. Krakowka. 1990. Interaction of canine distemper virus nucleocapsid variants with 70K heat-shock proteins. J. Gen. Virol. 71:1585-1590. (Pubitemid 20225860)
39. Oglesbee, M. J., H. Kenney, T. Kenney, and S. Krakowka. 1993. Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persistent infection. Virology 192:556-567. (Pubitemid 23232029)
40. Oglesbee, M. J., Z. Liu, H. Kenney, and C. L. Brooks. 1996. The highly inducible member of the 70 kDa family of heat shock proteins increases canine distemper virus polymerase activity. J. Gen. Virol. 77:2125-2135. (Pubitemid 26316083)
41. Oglesbee, M. J., M. Pratt, and T. Carsillo. 2002. Role for heat shock proteins in the immune response to measles virus infection. Viral Immunol. 15:399-416.
42. Ovsyannikova, I. G., J. E. Ryan, R. A. Vierkant, V. S. Pankratz, R. M. Jacobson, and G. A. Poland. 2005. Immunologic significance of HLA class I genes in measles virus-specific IFN-gamma and IL-4 cytokine immune responses. Immunogenetics 57:828-836. (Pubitemid 41817941)
43. Pardue, S., S. Wang, M. M. Miller, and M. Morrison-Bogorad. 2007. Elevated levels of inducible heat shock 70 proteins in human brain. Neurobiol. Aging 28:314-324.
44. Patterson, C. E., D. M. Lawrence, L. A. Echols, and G. F. Rall. 2002. Immune-mediated protection from measles virus-induced central nervous system disease is noncytolytic and gamma interferon dependent. J. Virol. 76:4497-4506. (Pubitemid 34309585)
45. Sakae, H., M. Kohase, T. Kurata, and H. Yoshikura. 1997. Isolation of a measles virus variant: protection of newborn mice from measles encephalitis by 24 h prior intracerebral inoculation with the variant. Arch. Virol. 142:1937-1952. (Pubitemid 27510311)
46. Schell, J. B., C. A. Crane, M. F. Smith, Jr., and M. R. Roberts. 2007. Differential ex vivo nitric oxide production by acutely isolated neonatal and adult microglia. J. Neuroimmunol. 189:75-87. (Pubitemid 47379435)
47. Schubert, S., K. Moller-Ehrlich, K. Singethan, S. Wiese, W. P. Duprex, B. K. Rima, S. Niewiesk, and J. Schneider-Schaulies. 2006. A mouse model of persistent brain infection with recombinant Measles virus. J. Gen. Virol. 87:2011-2019. (Pubitemid 43985885)
48. Scorza, F. A., R. M. Cysneiros, R. M. Arida, C. A. Scorza, A. C. de Almeida, B. Schmidt, and E. A. Cavalheiro. 2008. Adult hippocampal neurogenesis and sudden unexpected death in epilepsy: reality or just an attractive history? Med. Hypotheses 71:914-922.
49. Spiller, S., G. Elson, R. Ferstl, S. Dreher, T. Mueller, M. Freudenberg, B. Daubeuf, H. Wagner, and C. J. Kirschning. 2008. TLR4-induced IFN-gamma production increases TLR2 sensitivity and drives Gram-negative sepsis in mice. J. Exp. Med. 205:1747-1754.
50. Tytell, M., W. R. Brown, D. M. Moody, and V. R. Challa. 1998. Immunohistochemical assessment of constitutive and inducible heat-shock protein 70 and ubiquitin in human cerebellum and caudate nucleus. Mol. Chem. Neuropathol. 35:97-117. (Pubitemid 128770284)
51. Uytdehaag, F. G., R. S. van Binnendijk, M. J. Kenter, and A. D. Osterhaus. 1994. Cytotoxic T lymphocyte responses against measles virus. Curr. Top. Microbiol. Immunol. 189:151-167. (Pubitemid 24170553)
52. Vasconcelos, D., E. Norrby, and M. Oglesbee. 1998. The cellular stress response increases measles virus-induced cytopathic effect. J. Gen. Virol. 79:1769-1773. (Pubitemid 28330682)
53. Vasconcelos, D. Y., X. H. Cai, and M. J. Oglesbee. 1998. Constitutive overexpression of the major inducible 70 kDa heat shock protein mediates large plaque formation by measles virus. J. Gen. Virol. 79:2239-2247. (Pubitemid 28423420)
54. Wang, X., and Y. Suzuki. 2007. Microglia produce IFN-gamma independently from T cells during acute toxoplasmosis in the brain. J. Interferon Cytokine Res. 27:599-605. (Pubitemid 47122719)
55. Weidinger, G., S. Czub, C. Neumeister, P. Harriott, V. ter Meulen, and S. Niewiesk. 2000. Role of CD4(+) and CD8(+) T cells in the prevention of measles virus-induced encephalitis in mice. J. Gen. Virol. 81:2707-2713.
56. Wells, A. D., S. K. Rai, M. S. Salvato, H. Band, and M. Malkovsky. 1998. Hsp72-mediated augmentation of MHC class I surface expression and endogenous antigen presentation. Int. Immunol. 10:609-617. (Pubitemid 28221462)
57. Zhang, X., J. M. Bourhis, S. Longhi, T. Carsillo, M. Buccellato, B. Morin, B. Canard, and M. Oglesbee. 2005. Hsp72 recognizes a P binding motif in the measles virus N protein. Virology 337:162-174. (Pubitemid 40725449)
58. Zhang, X., C. Glendening, H. Linke, C. L. Parks, C. Brooks, S. A. Udem, and M. Oglesbee. 2002. Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J. Virol. 76:8737-8746.