Infiltrating regulatory B cells control neuroinflammation following viral brain infection

Journal of Immunology

Volumn 193, Issue 12, 2014, Pages 6070-6080

  Mutnal, Manohar B ^a   Hu, Shuxian ^a   Schachtele, Scott J ^a   Lokensgard, James R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD1D ANTIGEN; CD4 ANTIGEN; CD5 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; B LYMPHOCYTE; BRAIN INFECTION; CD19+ CD1DHI CD5+ B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; CYTOMEGALOVIRUS INFECTION; FEMALE; FLOW CYTOMETRY; GAIN OF FUNCTION MUTATION; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTIC INFILTRATION; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE; WILD TYPE; ADOPTIVE TRANSFER; ANIMAL; BIOSYNTHESIS; BRAIN; DISEASE MODEL; ENCEPHALITIS; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; MUROMEGALOVIRUS; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; B-LYMPHOCYTES, REGULATORY; BRAIN; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FEMALE; HERPESVIRIDAE INFECTIONS; IMMUNOPHENOTYPING; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MICROGLIA; MUROMEGALOVIRUS; PHENOTYPE; T-LYMPHOCYTE SUBSETS;

EID: 84916886831     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400654     Document Type: Article

References (65)

1. González-Scarano, F., and J. Martín-García. 2005. The neuropathogenesis of AIDS. Nat. Rev. Immunol. 5: 69-81.
2. McGavern, D. B., and S. S. Kang. 2011. Illuminating viral infections in the nervous system. Nat. Rev. Immunol. 11: 318-329.
3. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
4. Kivisäkk, P., J. Imitola, S. Rasmussen, W. Elyaman, B. Zhu, R. M. Ransohoff, and S. J. Khoury. 2009. Localizing central nervous system immune surveillance: meningeal antigen-presenting cells activate T cells during experimental autoimmune encephalomyelitis. Ann. Neurol. 65: 457-469.
5. Hu, S., W. S. Sheng, S. J. Schachtele, and J. R. Lokensgard. 2011. Reactive oxygen species drive herpes simplex virus (HSV)-1-induced proinflammatory cytokine production by murine microglia. J. Neuroinflammation 8: 123.
6. Aravalli, R. N., S. Hu, T. N. Rowen, J. M. Palmquist, and J. R. Lokensgard. 2005. Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J. Immunol. 175: 4189-4193.
7. Phares, T. W., K. D. DiSano, D. R. Hinton, M. Hwang, A. J. Zajac, S. A. Stohlman, and C. C. Bergmann. 2013. IL-21 optimizes T cell and humoral responses in the central nervous system during viral encephalitis. J. Neuroimmunol. 263: 43-54.
8. Ransohoff, R. M., and M. A. Brown. 2012. Innate immunity in the central nervous system. J. Clin. Invest. 122: 1164-1171.
9. Stewart, B. S., V. L. Demarest, S. J. Wong, S. Green, and K. A. Bernard. 2011. Persistence of virus-specific immune responses in the central nervous system of mice after West Nile virus infection. BMC Immunol. 12: 6.
10. Anghelina, D., J. Zhao, K. Trandem, and S. Perlman. 2009. Role of regulatory T cells in coronavirus-induced acute encephalitis. Virology 385: 358-367.
11. Reuter, D., T. Sparwasser, T. Hünig, and J. Schneider-Schaulies. 2012. Foxp3+ regulatory T cells control persistence of viral CNS infection. PLoS ONE 7: e33989.
12. Graham, J. B., A. Da Costa, and J. M. Lund. 2014. Regulatory T cells shape the resident memory T cell response to virus infection in the tissues. J. Immunol. 192: 683-690.
13. Howard, M., and A. O'Garra. 1992. Biological properties of interleukin 10. Immunol. Today 13: 198-200.
14. Marques, C. P., S. Hu, W. Sheng, M. C. Cheeran, D. Cox, and J. R. Lokensgard. 2004. Interleukin-10 attenuates production of HSV-induced inflammatory mediators by human microglia. Glia 47: 358-366.
15. Yanaba, K., J. D. Bouaziz, K. M. Haas, J. C. Poe, M. Fujimoto, and T. F. Tedder. 2008. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650.
16. Matsushita, T., K. Yanaba, J. D. Bouaziz, M. Fujimoto, and T. F. Tedder. 2008. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118: 3420-3430.
17. Matsushita, T., M. Horikawa, Y. Iwata, and T. F. Tedder. 2010. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J. Immunol. 185: 2240-2252.
18. Mauri, C., and A. Bosma. 2012. Immune regulatory function of B cells. Annu. Rev. Immunol. 30: 221-241.
19. Fillatreau, S., C. H. Sweenie, M. J. McGeachy, D. Gray, and S. M. Anderton. 2002. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3: 944-950.
20. Schioppa, T., R. Moore, R. G. Thompson, E. C. Rosser, H. Kulbe, S. Nedospasov, C. Mauri, L. M. Coussens, and F. R. Balkwill. 2011. B regulatory cells and the tumor-promoting actions of TNF-a during squamous carcinogenesis. Proc. Natl. Acad. Sci. USA 108: 10662-10667.
21. Ding, Q., M. Yeung, G. Camirand, Q. Zeng, H. Akiba, H. Yagita, G. Chalasani, M. H. Sayegh, N. Najafian, and D. M. Rothstein. 2011. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J. Clin. Invest. 121: 3645-3656.
22. Goenka, R., M. A. Parent, P. H. Elzer, and C. L. Baldwin. 2011. B cell-deficient mice display markedly enhanced resistance to the intracellular bacterium Brucella abortus. J. Infect. Dis. 203: 1136-1146.
23. Neves, P., V. Lampropoulou, E. Calderon-Gomez, T. Roch, U. Stervbo, P. Shen, A. A. Kühl, C. Loddenkemper, M. Haury, S. A. Nedospasov, et al. 2010. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity 33: 777-790.
24. Gray, M., K. Miles, D. Salter, D. Gray, and J. Savill. 2007. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. USA 104: 14080-14085.
25. Haas, K. M., R. Watanabe, T. Matsushita, H. Nakashima, N. Ishiura, H. Okochi, M. Fujimoto, and T. F. Tedder. 2010. Protective and pathogenic roles for B cells during systemic autoimmunity in NZB/W F1 mice. J. Immunol. 184: 4789-4800.
26. Yanaba, K., J. D. Bouaziz, T. Matsushita, T. Tsubata, and T. F. Tedder. 2009. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol. 182: 7459-7472.
27. Watanabe, R., N. Ishiura, H. Nakashima, Y. Kuwano, H. Okochi, K. Tamaki, S. Sato, T. F. Tedder, and M. Fujimoto. 2010. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J. Immunol. 184: 4801-4809.
28. Kamanaka, M., S. T. Kim, Y. Y. Wan, F. S. Sutterwala, M. Lara-Tejero, J. E. Galán, E. Harhaj, and R. A. Flavell. 2006. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25: 941-952.
29. Maseda, D., S. H. Smith, D. J. DiLillo, J. M. Bryant, K. M. Candando, C. T. Weaver, and T. F. Tedder. 2012. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J. Immunol. 188: 1036-1048.
30. Mutnal, M. B., S. Hu, M. R. Little, and J. R. Lokensgard. 2011. Memory T cells persisting in the brain following MCMV infection induce long-term microglial activation via interferon-g. J. Neurovirol. 17: 424-437.
31. Mutnal, M. B., S. Hu, and J. R. Lokensgard. 2012. Persistent humoral immune responses in the CNS limit recovery of reactivated murine cytomegalovirus. PLoS ONE 7: e33143.
32. Cheeran, M. C., G. Gekker, S. Hu, J. M. Palmquist, and J. R. Lokensgard. 2005. T cell-mediated restriction of intracerebral murine cytomegalovirus infection displays dependence upon perforin but not interferon-gamma. J. Neurovirol. 11: 274-280.
33. Stoddart, C. A., R. D. Cardin, J. M. Boname, W. C. Manning, G. B. Abenes, and E. S. Mocarski. 1994. Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J. Virol. 68: 6243-6253.
34. Nanton, M. R., S. S. Way, M. J. Shlomchik, and S. J. McSorley. 2012. Cutting edge: B cells are essential for protective immunity against Salmonella independent of antibody secretion. J. Immunol. 189: 5503-5507.
35. Chen, J., M. Trounstine, F. W. Alt, F. Young, C. Kurahara, J. F. Loring, and D. Huszar. 1993. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int. Immunol. 5: 647-656.
36. Cheeran, M. C., G. Gekker, S. Hu, X. Min, D. Cox, and J. R. Lokensgard. 2004. Intracerebral infection with murine cytomegalovirus induces CXCL10 and is restricted by adoptive transfer of splenocytes. J. Neurovirol. 10: 152-162.
37. Cheeran, M. C., S. Hu, J. M. Palmquist, T. Bakken, G. Gekker, and J. R. Lokensgard. 2007. Dysregulated interferon-gamma responses during lethal cytomegalovirus brain infection of IL-10-deficient mice. Virus Res. 130: 96-102.
38. Levine, B., J. M. Hardwick, B. D. Trapp, T. O. Crawford, R. C. Bollinger, and D. E. Griffin. 1991. Antibody-mediated clearance of alphavirus infection from neurons. Science 254: 856-860.
39. Marten, N. W., S. A. Stohlman, J. Zhou, and C. C. Bergmann. 2003. Kinetics of virus-specific CD8+ -T-cell expansion and trafficking following central nervous system infection. J. Virol. 77: 2775-2778.
40. Mutnal, M. B., M. C. Cheeran, S. Hu, M. R. Little, and J. R. Lokensgard. 2010. Excess neutrophil infiltration during cytomegalovirus brain infection of interleukin-10-deficient mice. J. Neuroimmunol. 227: 101-110.
41. Yoshizaki, A., T. Miyagaki, D. J. DiLillo, T. Matsushita, M. Horikawa, E. I. Kountikov, R. Spolski, J. C. Poe, W. J. Leonard, and T. F. Tedder. 2012. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491: 264-268.
42. Fantini, M. C., S. Dominitzki, A. Rizzo, M. F. Neurath, and C. Becker. 2007. In vitro generation of CD4+ CD25+ regulatory cells from murine naive T cells. Nat. Protoc. 2: 1789-1794.
43. Chao, C. C., S. Hu, W. S. Sheng, D. Bu, M. I. Bukrinsky, and P. K. Peterson. 1996. Cytokine-stimulated astrocytes damage human neurons via a nitric oxide mechanism. Glia 16: 276-284.
44. Suzumura, A., S. G. Mezitis, N. K. Gonatas, and D. H. Silberberg. 1987. MHC antigen expression on bulk isolated macrophage-microglia from newborn mouse brain: induction of Ia antigen expression by gamma-interferon. J. Neuroimmunol. 15: 263-278.
45. Giulian, D., T. J. Baker, L. C. Shih, and L. B. Lachman. 1986. Interleukin 1 of the central nervous system is produced by ameboid microglia. J. Exp. Med. 164: 594-604.
46. Hassan, N. F., S. Rifat, D. E. Campbell, L. J. McCawley, and S. D. Douglas. 1991. Isolation and flow cytometric characterization of newborn mouse brain-derived microglia maintained in vitro. J. Leukoc. Biol. 50: 86-92.
47. Cheeran, M. C., J. R. Lokensgard, and M. R. Schleiss. 2009. Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clin. Microbiol. Rev. 22: 99-126.
48. + T cells during low-level Friend retrovirus infection. Retrovirology 10: 109.
49. Sungur, C. M., Y. J. Tang-Feldman, E. Ames, M. Alvarez, M. Chen, D. L. Longo, C. Pomeroy, and W. J. Murphy. 2013. Murine natural killer cell licensing and regulation by T regulatory cells in viral responses. Proc. Natl. Acad. Sci. USA 110: 7401-7406.
50. Qureshi, M. H., B. A. Garvy, C. Pomeroy, M. S. Inayat, and O. R. Oakley. 2005. A murine model of dual infection with cytomegalovirus and Pneumocystis carinii: effects of virus-induced immunomodulation on disease progression. Virus Res. 114: 35-44.
51. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147: 3815-3822.
52. Ray, A., S. Basu, C. B. Williams, N. H. Salzman, and B. N. Dittel. 2012. A novel IL-10-independent regulatory role for B cells in suppressing autoimmunity by maintenance of regulatory T cells via GITR ligand. J. Immunol. 188: 3188-3198.
53. Liu, Y., Y. Chen, Z. Li, Y. Han, Y. Sun, Q. Wang, B. Liu, and Z. Su. 2013. Role of IL-10-producing regulatory B cells in control of cerebral malaria in Plasmodium berghei infected mice. Eur. J. Immunol. 43: 2907-2918.
54. Gray, D., and M. Gray. 2010. What are regulatory B cells? Eur. J. Immunol. 40: 2677-2679.
55. DiLillo, D. J., T. Matsushita, and T. F. Tedder. 2010. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. N. Y. Acad. Sci. 1183: 38-57.
56. Mann, M. K., K. Maresz, L. P. Shriver, Y. Tan, and B. N. Dittel. 2007. B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol. 178: 3447-3456.
57. Miles, K., J. Heaney, Z. Sibinska, D. Salter, J. Savill, D. Gray, and M. Gray. 2012. A tolerogenic role for Toll-like receptor 9 is revealed by B-cell interaction with DNA complexes expressed on apoptotic cells. Proc. Natl. Acad. Sci. USA 109: 887-892.
58. Krug, A., A. R. French, W. Barchet, J. A. Fischer, A. Dzionek, J. T. Pingel, M. M. Orihuela, S. Akira, W. M. Yokoyama, and M. Colonna. 2004. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21: 107-119.
59. Marques, C. P., M. C. Cheeran, J. M. Palmquist, S. Hu, S. L. Urban, and J. R. Lokensgard. 2008. Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J. Immunol. 181: 6417-6426.
60. Ponomarev, E. D., L. P. Shriver, K. Maresz, and B. N. Dittel. 2005. Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J. Neurosci. Res. 81: 374-389.
61. Horikawa, M., E. T. Weimer, D. J. DiLillo, G. M. Venturi, R. Spolski, W. J. Leonard, M. T. Heise, and T. F. Tedder. 2013. Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice. J. Immunol. 190: 1158-1168.
62. Yang, M., J. Deng, Y. Liu, K. H. Ko, X. Wang, Z. Jiao, S. Wang, Z. Hua, L. Sun, G. Srivastava, et al. 2012. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am. J. Pathol. 180: 2375-2385.
63. Murphy, K. M., and B. Stockinger. 2010. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat. Immunol. 11: 674-680.
64. Amu, S., S. P. Saunders, M. Kronenberg, N. E. Mangan, A. Atzberger, and P. G. Fallon. 2010. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J. Allergy Clin. Immunol. 125: 1114-1124.e1118.
65. Hussaarts, L., L. E. van der Vlugt, M. Yazdanbakhsh, and H. H. Smits. 2011. Regulatory B-cell induction by helminths: implications for allergic disease. J. Allergy Clin. Immunol. 128: 733-739.