Depletion of regulatory T-cells leads to moderate B-cell antigenicity in respiratory syncytial virus infection

International Journal of Infectious Diseases

Volumn 41, Issue , 2015, Pages 56-64

  Shao, Hsiao Yun ^a,b   Huang, Juo Yu ^a   Lin, Yi Wen ^a   Yu, Shu Ling ^a   Chitra, Ebenezer ^c   Chang, Ching Kun ^a,d   Sung, Wang Chou ^a   Chong, Pele ^a,e   Chow, Yen Hung ^a,e  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c INTERNATIONAL MEDICAL UNIVERSITY   (Malaysia)

^d NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^e CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Antigenicity; B cells; Regulatory T cells; Respiratory syncytial virus

Indexed keywords

ANTIBODY; CD25 ANTIBODY; FUSION ANTIBODY; IMMUNOGLOBULIN G2A; UNCLASSIFIED DRUG; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY TITER; ANTIGENICITY; ARTICLE; B LYMPHOCYTE; CD4+ CD25+ FOXP3+ T LYMPHOCYTE; CD45RA+ B LYMPHOCYTE; DENDRITIC CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL VIRUS INFECTION; ANIMAL; BAGG ALBINO MOUSE; CD8+ T LYMPHOCYTE; FEMALE; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; LUNG; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; SPLEEN; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; LUNG; MICE; MICE, INBRED BALB C; MICE, SCID; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 84948971944     PISSN: 12019712     EISSN: 18783511     Source Type: Journal    
DOI: 10.1016/j.ijid.2015.10.026     Document Type: Article

References (53)

1. Falsey A.R. Respiratory syncytial virus infection in elderly and high-risk adults. Exp Lung Res 2005, 31(Suppl 1):77.
2. Holzel A., Parker L., Patterson W.H., White L.L., Thompson K.M., Tobin J.O. The isolation of respiratory syncytial virus from children with acute respiratory disease. Lancet 1963, 1:295-298.
3. Chanock R, Finberg L, Recovery from infants with respiratory illness of a virus related to chimpanzee coryza agent (CCA). II. Epidemiologic aspects of infection in infants and young children. Am J Hyg 1957;66:291-300.
4. Hall C.B., Walsh E.E., Long C.E., Schnabel K.C. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991, 163:693-698.
5. Murata Y., Falsey A.R. Respiratory syncytial virus infection in adults. Antivir Ther 2007, 12:659-670.
6. Walsh E.E., Hall C.B., Briselli M., Brandriss M.W., Schlesinger J.J. Immunization with glycoprotein subunits of respiratory syncytial virus to protect cotton rats against viral infection. J Infect Dis 1987, 155:1198-1204.
7. Graham B.S., Bunton L.A., Wright P.F., Karzon D.T. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J Clin Invest 1991, 88:1026-1033.
8. Olson M.R., Varga S.M. Pulmonary immunity and immunopathology: lessons from respiratory syncytial virus. Expert Rev Vaccines 2008, 7:1239-1255.
9. Olson M.R., Hartwig S.M., Varga S.M. The number of respiratory syncytial virus (RSV)-specific memory CD8 T cells in the lung is critical for their ability to inhibit RSV vaccine-enhanced pulmonary eosinophilia. J Immunol 2008, 181:7958-7968.
10. Olson M.R., Varga S.M. CD8 T cells inhibit respiratory syncytial virus (RSV) vaccine-enhanced disease. J Immunol 2007, 179:5415-5424.
11. Isaacs D. Viral subunit vaccines. Lancet 1991, 337:1223-1224.
12. Shevach E.M. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002, 2:389-400.
13. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004, 22:531-562.
14. Scott-Browne J.P., Shafiani S., Tucker-Heard G., Ishida-Tsubota K., Fontenot J.D., Rudensky A.Y., et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 2007, 204:2159-2169.
15. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
16. Toka F.N., Suvas S., Rouse B.T. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J Virol 2004, 78:13082-13089.
17. Suvas S., Kumaraguru U., Pack C.D., Lee S., Rouse B.T. CD4+CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J Exp Med 2003, 198:889-901.
18. Fernandez M.A., Puttur F.K., Wang Y.M., Howden W., Alexander S.I., Jones C.A. T regulatory cells contribute to the attenuated primary CD8+ and CD4+ T cell responses to herpes simplex virus type 2 in neonatal mice. J Immunol 2008, 180:1556-1564.
19. Zhao D.M., Thornton A.M., DiPaolo R.J., Shevach E.M. Activated CD4+CD25+ T cells selectively kill B lymphocytes. Blood 2006, 107:3925-3932.
20. Lim H.W., Hillsamer P., Banham A.H., Kim C.H. Cutting edge: direct suppression of B cells by CD4+ CD25+ regulatory T cells. J Immunol 2005, 175:4180-4183.
21. Iikuni N., Lourenco E.V., Hahn B.H., La Cava A. Cutting edge: regulatory T cells directly suppress B cells in systemic lupus erythematosus. J Immunol 2009, 183:1518-1522.
22. Shao H.Y., Yu S.L., Sia C., Chen Y., Chitra E., Chen I.H., et al. Immunogenic properties of RSV-B1 fusion (F) protein gene-encoding recombinant adenoviruses. Vaccine 2009, 27(40):5460-5471.
23. Foster B., Prussin C., Liu F., Whitmire J.K., Whitton J.L. Detection of intracellular cytokines by flow cytometry. Curr Protoc Immunol 2007, Chapter 6:Unit 6.24.
24. Brincks E.L., Roberts A.D., Cookenham T., Sell S., Kohlmeier J.E., Blackman M.A., Woodland D.L. Antigen-specific memory regulatory CD4+Foxp3+ T cells control memory responses to influenza virus infection. J Immunol 2013, 190:3438-3446.
25. Paust H.J., Ostmann A., Erhardt A., Turner J.E., Velden J., Mittrucker H.W., et al. Regulatory T cells control the Th1 immune response in murine crescentic glomerulonephritis. Kidney Int 2011, 80:154-164.
26. Pier GB, Lyczak JB, Wetzler LM, Immunology, infection, and immunity. ASM Press; 2004.
27. Gupta N., LeGoff J., Chamat S., Mercier-Delarue S., Touzelet O., Power U.F., et al. Affinity-purified respiratory syncytial virus antibodies from intravenous immunoglobulin exert potent antibody-dependent cellular cytotoxicity. PLoS One 2013, 8:e69390.
28. Fulton R.B., Meyerholz D.K., Varga S.M. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J Immunol 2010, 185:2382-2392.
29. Ruckwardt T.J., Bonaparte K.L., Nason M.C., Graham B.S. Regulatory T cells promote early influx of CD8+ T cells in the lungs of respiratory syncytial virus-infected mice and diminish immunodominance disparities. J Virol 2009, 83:3019-3028.
30. Bosma G.C., Custer R.P., Bosma M.J. A severe combined immunodeficiency mutation in the mouse. Nature 1983, 301:527-530.
31. Ehlenfield D.R., Cameron K., Welliver R.C. Eosinophilia at the time of respiratory syncytial virus bronchiolitis predicts childhood reactive airway disease. Pediatrics 2000, 105:79-83.
32. Castilow E.M., Meyerholz D.K., Varga S.M. IL-13 is required for eosinophil entry into the lung during respiratory syncytial virus vaccine-enhanced disease. J Immunol 2008, 180:2376-2384.
33. Kim H.W., Canchola J.G., Brandt C.D., Pyles G., Chanock R.M., Jensen K., Parrott R.H. Respiratory syncytial virus disease in infants despite prior administration of antigenic inactivated vaccine. Am J Epidemiol 1969, 89:422-434.
34. Murphy B.R., Prince G.A., Walsh E.E., Kim H.W., Parrott R.H., Hemming V.G., Rodriguez W.J., Chanock R.M. Dissociation between serum neutralizing and glycoprotein antibody responses of infants and children who received inactivated respiratory syncytial virus vaccine. J Clin Microbiol 1986, 24:197-202.
35. Mongkolsapaya J., Dejnirattisai W., Xu X.N., Vasanawathana S., Tangthawornchaikul N., Chairunsri A., et al. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 2003, 9:921-927.
36. Crispin J.C. Regulatory T cells as modulators of B cell antibody production. Clin Immunol 2011, 140:216-217.
37. Ludwig-Portugall I., Hamilton-Williams E.E., Gotot J., Kurts C. CD25+ T(reg) specifically suppress auto-Ab generation against pancreatic tissue autoantigens. Eur J Immunol 2009, 39:225-233.
38. Ludwig-Portugall I., Hamilton-Williams E.E., Gottschalk C., Kurts C. Cutting edge: CD25+ regulatory T cells prevent expansion and induce apoptosis of B cells specific for tissue autoantigens. J Immunol 2008, 181:4447-4451.
39. Johnson S., Oliver C., Prince G.A., Hemming V.G., Pfarr D.S., Wang S.C., et al. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J Infect Dis 1997, 176:1215-1224.
40. Polack F.P., Teng M.N., Collins P.L., Prince G.A., Exner M., Regele H., et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J Exp Med 2002, 196:859-865.
41. Kruijsen D., Bakkers M.J., van Uden N.O., Viveen M.C., van der Sluis T.C., Kimpen J.L., et al. Serum antibodies critically affect virus-specific CD4+/CD8+ T cell balance during respiratory syncytial virus infections. J Immunol 2010, 185:6489-6498.
42. Marino E., Villanueva J., Walters S., Liuwantara D., Mackay F., Grey S.T. CD4(+)CD25(+) T-cells control autoimmunity in the absence of B-cells. Diabetes 2009, 58:1568-1577.
43. Hu C.Y., Rodriguez-Pinto D., Du W., Ahuja A., Henegariu O., Wong F.S., et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest 2007, 117:3857-3867.
44. Yu S., Maiti P.K., Dyson M., Jain R., Braley-Mullen H. B cell-deficient NOD.H-2h4 mice have CD4+CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. J Exp Med 2006, 203:349-358.
45. Amu S., Gjertsson I., Tarkowski A., Brisslert M. B-cell CD25 expression in murine primary and secondary lymphoid tissue. Scand J Immunol 2006, 64:482-492.
46. Brisslert M., Bokarewa M., Larsson P., Wing K., Collins L.V., Tarkowski A. Phenotypic and functional characterization of human CD25+ B cells. Immunology 2006, 117:548-557.
47. Amu S., Tarkowski A., Dorner T., Bokarewa M., Brisslert M. The human immunomodulatory CD25+ B cell population belongs to the memory B cell pool. Scand J Immunol 2007, 66:77-86.
48. Amu S., Gjertsson I., Brisslert M. Functional characterization of murine CD25 expressing B cells. Scand J Immunol 2010, 71:275-282.
49. Edinger M., Hoffmann P., Ermann J., Drago K., Fathman C.G., Strober S., Negrin R.S. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003, 9:1144-1150.
50. Mempel T.R., Pittet M.J., Khazaie K., Weninger W., Weissleder R., von Boehmer H., von Andrian U.H., Regulatory T. cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 2006, 25:129-141.
51. Amoah S., Holbrook B.C., Yammani R.D., Alexander-Miller M.A. High viral burden restricts short-lived effector cell number at late times postinfection through increased natural regulatory T cell expansion. J Immunol 2013, 190:5020-5029.
52. Bystry R.S., Aluvihare V., Welch K.A., Kallikourdis M., Betz A.G. B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol 2001, 2:1126-1132.
53. Leon B., Bradley J.E., Lund F.E., Randall T.D., Ballesteros-Tato A. FoxP3+ regulatory T cells promote influenza-specific Tfh responses by controlling IL-2 availability. Nat Commun 2014, 5:3495.