Persistent humoral immune responses in the CNS limit recovery of reactivated murine cytomegalovirus

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Mutnal, Manohar B ^a   Hu, Shuxian ^a   Lokensgard, James R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; VIRUS ANTIBODY; VIRUS ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BRAIN INFECTION; BRAIN TISSUE; CELL ISOLATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMORAL IMMUNITY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PLASMA CELL; VIRUS LATENCY; VIRUS REACTIVATION; ANIMAL; BAGG ALBINO MOUSE; BRAIN; CELL STRAIN 3T3; HERPES VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MUROMEGALOVIRUS; NERVE CELL; VIROLOGY; VIRUS ACTIVATION;

ANIMALIA; MAIZE CHLOROTIC MOTTLE VIRUS; MURID HERPESVIRUS 1; MURINAE; MUS;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; B-LYMPHOCYTES; BRAIN; CENTRAL NERVOUS SYSTEM; FEMALE; HERPESVIRIDAE INFECTIONS; IMMUNITY, HUMORAL; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MUROMEGALOVIRUS; NEURONS; NIH 3T3 CELLS; PLASMA CELLS; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84857824847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033143     Document Type: Article

References (46)

1. Mocarski ES Jr, Abenes GB, Manning WC, Sambucetti LC, Cherrington JM, (1990) Molecular genetic analysis of cytomegalovirus gene regulation in growth, persistence and latency. Curr Top Microbiol Immunol 154: 47-74.
2. Fields BN, Knipe DM, Howley PM, (2007) Fields' virology Philadelphia Wolters Kluwer Health/Lippincott Williams & Wilkins. 2 v pp. (xix, 3091, 3086 p.).
3. Cheeran MC, Jiang Z, Hu S, Ni HT, Palmquist JM, et al. (2008) Cytomegalovirus infection and interferon-gamma modulate major histocompatibility complex class I expression on neural stem cells. J Neurovirol 14: 437-447.
4. Mutnal MB, Cheeran MC, Hu S, Lokensgard JR, (2011) Murine cytomegalovirus infection of neural stem cells alters neurogenesis in the developing brain. PLoS One 6: e16211.
5. Cheeran MC, Gekker G, Hu S, Min X, Cox D, et al. (2004) Intracerebral infection with murine cytomegalovirus induces CXCL10 and is restricted by adoptive transfer of splenocytes. J Neurovirol 10: 152-162.
6. Arai Y, Ishiwata M, Baba S, Kawasaki H, Kosugi I, et al. (2003) Neuron-specific activation of murine cytomegalovirus early gene e1 promoter in transgenic mice. Am J Pathol 163: 643-652.
7. Roizman B, Sears AE, (1987) An inquiry into the mechanisms of herpes simplex virus latency. Annu Rev Microbiol 41: 543-571.
8. Reddehase MJ, Mutter W, Munch K, Buhring HJ, Koszinowski UH, (1987) CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J Virol 61: 3102-3108.
9. Reddehase MJ, Weiland F, Munch K, Jonjic S, Luske A, 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.
10. Mutnal MB, Hu S, Little MR, Lokensgard JR, (2011) Memory T cells persisting in the brain following MCMV infection induce long-term microglial activation via interferon-gamma. J Neurovirol 17: 424-437.
11. Irani DN, Griffin DE, (1991) Isolation of brain parenchymal lymphocytes for flow cytometric analysis. Application to acute viral encephalitis. J Immunol Methods 139: 223-231.
12. Metcalf TU, Griffin DE, (2011) Alphavirus-induced encephalomyelitis: antibody-secreting cells and viral clearance from the nervous system. J Virol 85: 11490-11501.
13. Phares TW, Marques CP, Stohlman SA, Hinton DR, Bergmann CC, (2011) Factors supporting intrathecal humoral responses following viral encephalomyelitis. J Virol 85: 2589-2598.
14. Binder GK, Griffin DE, (2001) Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293: 303-306.
15. Burdeinick-Kerr R, Wind J, Griffin DE, (2007) Synergistic roles of antibody and interferon in noncytolytic clearance of Sindbis virus from different regions of the central nervous system. J Virol 81: 5628-5636.
16. Franciotta D, Salvetti M, Lolli F, Serafini B, Aloisi F, (2008) B cells and multiple sclerosis. Lancet Neurol 7: 852-858.
17. Owens GP, Bennett JL, Gilden DH, Burgoon MP, (2006) The B cell response in multiple sclerosis. Neurol Res 28: 236-244.
18. Fragkoudis R, Ballany CM, Boyd A, Fazakerley JK, (2008) In Semliki Forest virus encephalitis, antibody rapidly clears infectious virus and is required to eliminate viral material from the brain, but is not required to generate lesions of demyelination. J Gen Virol 89: 2565-2568.
19. Griffin D, Levine B, Tyor W, Ubol S, Despres P, (1997) The role of antibody in recovery from alphavirus encephalitis. Immunol Rev 159: 155-161.
20. Hooper DC, Phares TW, Fabis MJ, Roy A, (2009) The production of antibody by invading B cells is required for the clearance of rabies virus from the central nervous system. PLoS Negl Trop Dis 3: e535.
21. Levine B, Hardwick JM, Trapp BD, Crawford TO, Bollinger RC, et al. (1991) Antibody-mediated clearance of alphavirus infection from neurons. Science 254: 856-860.
22. Leonard WJ, Spolski R, (2005) Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat Rev Immunol 5: 688-698.
23. Belnoue E, Pihlgren M, McGaha TL, Tougne C, Rochat AF, et al. (2008) APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood 111: 2755-2764.
24. Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, et al. (2008) Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol 180: 3655-3659.
25. Shinmura Y, Aiba-Masago S, Kosugi I, Li RY, Baba S, et al. (1997) Differential expression of the immediate-early and early antigens in neuronal and glial cells of developing mouse brains infected with murine cytomegalovirus. Am J Pathol 151: 1331-1340.
26. Tsutsui Y, Kashiwai A, Kawamura N, Aiba-Masago S, Kosugi I, (1995) Prolonged infection of mouse brain neurons with murine cytomegalovirus after pre- and perinatal infection. Arch Virol 140: 1725-1736.
27. Jonjic S, Pavic I, Polic B, Crnkovic I, Lucin P, et al. (1994) Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J Exp Med 179: 1713-1717.
28. Reddehase MJ, Balthesen M, Rapp M, Jonjic S, Pavic I, et al. (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.
29. Polic B, Hengel H, Krmpotic A, Trgovcich J, Pavic I, et al. (1998) Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J Exp Med 188: 1047-1054.
30. Parrish-Novak J, Foster DC, Holly RD, Clegg CH, (2002) Interleukin-21 and the IL-21 receptor: novel effectors of NK and T cell responses. J Leukoc Biol 72: 856-863.
31. Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, et al. (2008) Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol 181: 6417-6426.
32. Cheeran MC, Gekker G, Hu S, Palmquist JM, Lokensgard JR, (2005) T cell-mediated restriction of intracerebral murine cytomegalovirus infection displays dependence upon perforin but not interferon-gamma. J Neurovirol 11: 274-280.
33. Greene IP, Lee EY, Prow N, Ngwang B, Griffin DE, (2008) Protection from fatal viral encephalomyelitis: AMPA receptor antagonists have a direct effect on the inflammatory response to infection. Proc Natl Acad Sci U S A 105: 3575-3580.
34. Marques CP, Kapil P, Hinton DR, Hindinger C, Nutt SL, et al. (2011) CXCR3-dependent plasma blast migration to the central nervous system during viral encephalomyelitis. J Virol 85: 6136-6147.
35. Stewart BS, Demarest VL, Wong SJ, Green S, Bernard KA, (2011) Persistence of virus-specific immune responses in the central nervous system of mice after West Nile virus infection. BMC Immunol 12: 6.
36. Jordan MC, Mar VL, (1982) Spontaneous activation of latent cytomegalovirus from murine spleen explants. Role of lymphocytes and macrophages in release and replication of virus. J Clin Invest 70: 762-768.
37. Jordan MC, Takagi JL, Stevens JG, (1982) Activation of latent murine cytomegalovirus in vivo and in vitro: a pathogenetic role for acute infection. J Infect Dis 145: 699-705.
38. Rabinovitch T, Oh JO, Minasi P, (1990) In vivo reactivation of latent murine cytomegalovirus in the eye by immunosuppressive treatment. Invest Ophthalmol Vis Sci 31: 657-663.
39. Hummel M, Zhang Z, Yan S, DePlaen I, Golia P, et al. (2001) Allogeneic transplantation induces expression of cytomegalovirus immediate-early genes in vivo: a model for reactivation from latency. J Virol 75: 4814-4822.
40. Busche A, Marquardt A, Bleich A, Ghazal P, Angulo A, et al. (2009) The mouse cytomegalovirus immediate-early 1 gene is not required for establishment of latency or for reactivation in the lungs. J Virol 83: 4030-4038.
41. Tessmer MS, Reilly EC, Brossay L, (2011) Salivary gland NK cells are phenotypically and functionally unique. PLoS Pathog 7: e1001254.
42. Stoddart CA, Cardin RD, Boname JM, Manning WC, Abenes GB, et al. (1994) Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J Virol 68: 6243-6253.
43. Cheeran MC, Hu S, Palmquist JM, Bakken T, Gekker G, et al. (2007) Dysregulated interferon-gamma responses during lethal cytomegalovirus brain infection of IL-10-deficient mice. Virus Res 130: 96-102.
44. Marten NW, Stohlman SA, Zhou J, Bergmann CC, (2003) Kinetics of virus-specific CD8+-T-cell expansion and trafficking following central nervous system infection. J Virol 77: 2775-2778.
45. Mutnal MB, Cheeran MC, Hu S, Little MR, Lokensgard JR, (2010) Excess neutrophil infiltration during cytomegalovirus brain infection of interleukin-10-deficient mice. J Neuroimmunol 227: 101-110.
46. Luker GD, Prior JL, Song J, Pica CM, Leib DA, (2003) Bioluminescence imaging reveals systemic dissemination of herpes simplex virus type 1 in the absence of interferon receptors. J Virol 77: 11082-11093.