Investigating the Role for IL-21 in Rabies Virus Vaccine-induced Immunity

PLoS Neglected Tropical Diseases

Volumn 7, Issue 3, 2013, Pages

  Dorfmeier, Corin L ^a   Tzvetkov, Evgeni P ^a   Gatt, Anthony ^a   McGettigan, James P ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; INTERLEUKIN 21; INTERLEUKIN 21 RECEPTOR; NEUTRALIZING ANTIBODY; RABIES VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNIZATION; LOW DRUG DOSE; MEMORY CELL; MOUSE; NONHUMAN; POST EXPOSURE PROPHYLAXIS; RABIES;

EID: 84875977188     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002129     Document Type: Article

References (64)

1. Jackson AC, (2008) Rabies. Neurol Clin 26: 717-26.
2. Dodet B, Africa Rabies Expert B, Adjogoua EV, Aguemon AR, Amadou OH, et al. (2008) Fighting rabies in africa: The africa rabies expert bureau (AfroREB). Vaccine 26: 6295-8.
3. WHO (2007) Rabies and Envenomings: A neglected public health issue: Report of a Consultative Meeting. World Health Organization. 32 pp.
4. Blanton JD, Dyer J, McBrayer J, Rupprecht CE, (2012) Rabies surveillance in the united states during 2011. J Am Vet Med Assoc 241: 712-722 10.2460/javma.241.6.712.
5. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, et al. (2005) Re-evaluating the burden of rabies in africa and asia. Bull World Health Organ 83: 360-8.
6. CDC (2012) Cost of Rabies Prevention. Available: http://www.cdc.gov/rabies/location/usa/cost.html.
7. NIAID (2012) NIAID Category A, B, and C Priority Pathogens. Available: http://www.niaid.nih.gov/topics/biodefenserelated/biodefense/pages/cata.aspx.
8. Conzelmann KK, Cox JH, Schneider LG, Thiel HJ, (1990) Molecular cloning and complete nucleotide sequence of the attenuated rabies virus SAD B19. Virology 175: 485-99.
9. Cenna J, Hunter M, Tan GS, Papaneri AB, Ribka EP, et al. (2009) Replication-deficient rabies virus-based vaccines are safe and immunogenic in mice and nonhuman primates. Journal of Infectious Diseases 200: 1251-60.
10. Cenna J, Tan GS, Papaneri AB, Dietzschold B, Schnell MJ, et al. (2008) Immune modulating effect by a phosphoprotein-deleted rabies virus vaccine vector expressing two copies of the rabies virus glycoprotein gene. Vaccine 26: 6405-14.
11. Ito N, Sugiyama M, Yamada K, Shimizu K, Takayama-Ito M, et al. (2005) Characterization of M gene-deficient rabies virus with advantages of effective immunization and safety as a vaccine strain. Microbiol Immunol 49: 971-9.
12. Morimoto K, Shoji Y, Inoue K, (2005) Characterizatio of P gene-deficient rabies virus: Propagation, pathogenicity and antigenicity. Virus Research 111: 61-67.
13. McGettigan JP, Pomerantz RJ, Siler CA, McKenna PM, Foley HD, et al. (2003) Second-generation rabies virus-based vaccine vectors expressing human immunodeficiency virus type 1 gag have greatly reduced pathogenicity but are highly immunogenic. Journal of Virology 77: 237-44.
14. Johnson N, Cunningham AF, Fooks AR, (2010) The immune response to rabies virus infection and vaccination. Vaccine 28: 3896-3901 10.1016/j.vaccine.2010.03.039.
15. Turner GS, (1978) Immunoglobulin (IgG) and (IgM) antibody responses to rabies vaccine. J Gen Virol 40: 595-604.
16. Dorfmeier CL, Lytle AG, Dunkel AL, Gatt A, McGettigan JP, (2012) Protective vaccine-induced CD4+ T cell-independent B cell responses against rabies infection. J Virol 86: 11533-40 10.1128/JVI.00615-12.
17. Goenka R, Barnett LG, Silver JS, O'Neill PJ, Hunter CA, et al. (2011) Cutting edge: Dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J Immunol 187: 1091-1095 10.4049/jimmunol.1100853.
18. Ozaki K, Kikly K, Michalovich D, Young PR, Leonard WJ, (2000) Cloning of a type I cytokine receptor most related to the IL-2 receptor beta chain. Proc Natl Acad Sci U S A 97: 11439-11444 10.1073/pnas.200360997.
19. Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C, et al. (2000) Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408: 57-63 10.1038/35040504.
20. Yi JS, Cox MA, Zajac AJ, (2010) Interleukin-21: A multifunctional regulator of immunity to infections. Microbes Infect 12: 1111-1119 10.1016/j.micinf.2010.08.008.
21. Vogelzang A, McGuire HM, Yu D, Sprent J, Mackay CR, et al. (2008) A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29: 127-137 10.1016/j.immuni.2008.06.001.
22. Linterman MA, Beaton L, Yu D, Ramiscal RR, Srivastava M, et al. (2010) IL-21 acts directly on B cells to regulate bcl-6 expression and germinal center responses. J Exp Med 207: 353-363 10.1084/jem.20091738.
23. Nurieva RI, Chung Y, Hwang D, Yang XO, Kang HS, et al. (2008) Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149 10.1016/j.immuni.2008.05.009.
24. King IL, Mohrs K, Mohrs M, (2010) A nonredundant role for IL-21 receptor signaling in plasma cell differentiation and protective type 2 immunity against gastrointestinal helminth infection. J Immunol 185: 6138-6145 10.4049/jimmunol.1001703.
25. Holm C, Nyvold CG, Paludan SR, Thomsen AR, Hokland M, (2006) Interleukin-21 mRNA expression during virus infections. Cytokine 33: 41-45 10.1016/j.cyto.2005.11.014.
26. Spolski R, Wang L, Wan CK, Bonville CA, Domachowske JB, et al. (2012) IL-21 promotes the pathologic immune response to pneumovirus infection. J Immunol 188: 1924-1932 10.4049/jimmunol.1100767.
27. Elsaesser H, Sauer K, Brooks DG, (2009) IL-21 is required to control chronic viral infection. Science 324: 1569-1572 10.1126/science.1174182.
28. Frohlich A, Kisielow J, Schmitz I, Freigang S, Shamshiev AT, et al. (2009) IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 324: 1576-1580 10.1126/science.1172815.
29. Yi JS, Du M, Zajac AJ, (2009) A vital role for interleukin-21 in the control of a chronic viral infection. Science 324: 1572-1576 10.1126/science.1175194.
30. Publicover J, Goodsell A, Nishimura S, Vilarinho S, Wang ZE, et al. (2011) IL-21 is pivotal in determining age-dependent effectiveness of immune responses in a mouse model of human hepatitis B. J Clin Invest 121: 1154-1162 10.1172/JCI44198.
31. Iannello A, Boulassel MR, Samarani S, Tremblay C, Toma E, et al. (2010) IL-21 enhances NK cell functions and survival in healthy and HIV-infected patients with minimal stimulation of viral replication. J Leukoc Biol 87: 857-867 10.1189/jlb.1009701.
32. Iannello A, Allam O, Samarani S, Ahmad A, (2012) Interleukin-21: A key cytokine for controlling HIV and other chronic viral infections. Med Sci (Paris) 28: 605-611 10.1051/medsci/2012286013.
33. Ruffin N, Lantto R, Pensieroso S, Sammicheli S, Hejdeman B, et al. (2012) Immune activation and increased IL-21R expression are associated with the loss of memory B cells during HIV-1 infection. J Intern Med 272: 492-503 10.1111/j.1365-2796.2012.02550.x; 10.1111/j.1365-2796.2012.02550.x.
34. Pallikkuth S, Pilakka Kanthikeel S, Silva SY, Fischl M, Pahwa R, et al. (2011) Upregulation of IL-21 receptor on B cells and IL-21 secretion distinguishes novel 2009 H1N1 vaccine responders from nonresponders among HIV-infected persons on combination antiretroviral therapy. J Immunol 186: 6173-6181 10.4049/jimmunol.1100264.
35. McGavern DB, (2010) A little 'help' from IL-21 during persistent viral infection. J Mol Cell Biol 2: 8-10 10.1093/jmcb/mjp021.
36. McGettigan JP, Naper K, Orenstein J, Koser M, McKenna PM, et al. (2003) Functional human immunodeficiency virus type 1 (HIV-1) gag-pol or HIV-1 gag-pol and env expressed from a single rhabdovirus-based vaccine vector genome. Journal of Virology 77: 10889-99.
37. Foley HD, McGettigan JP, Siler CA, Dietzschold B, Schnell MJ, (2000) A recombinant rabies virus expressing vesicular stomatitis virus glycoprotein fails to protect against rabies virus infection. Proceedings of the National Academy of Sciences of the United States of America 97: 14680-5.
38. Morimoto K, Hooper DC, Carbaugh H, Fu ZF, Koprowski H, et al. (1998) Rabies virus quasispecies: Implications for pathogenesis. Proceedings of the National Academy of Sciences of the United States of America 95: 3152-6.
39. Ozaki K, Spolski R, Feng CG, Qi CF, Cheng J, et al. (2002) A critical role for IL-21 in regulating immunoglobulin production. Science 298: 1630-1634 10.1126/science.1077002.
40. Cenna J, Hunter M, Tan GS, Papaneri AB, Ribka EP, et al. (2009) Replication-deficient rabies virus-based vaccines are safe and immunogenic in mice and nonhuman primates. J Infect Dis 200: 1251-1260 10.1086/605949.
41. Cenna J, Tan GS, Papaneri AB, Dietzschold B, Schnell MJ, et al. (2008) Immune modulating effect by a phosphoprotein-deleted rabies virus vaccine vector expressing two copies of the rabies virus glycoprotein gene. Vaccine 26: 6405-6414 10.1016/j.vaccine.2008.08.069.
42. Lee SK, Rigby RJ, Zotos D, Tsai LM, Kawamoto S, et al. (2011) B cell priming for extrafollicular antibody responses requires bcl-6 expression by T cells. J Exp Med 208: 1377-1388 10.1084/jem.20102065.
43. Linterman MA, Rigby RJ, Wong RK, Yu D, Brink R, et al. (2009) Follicular helper T cells are required for systemic autoimmunity. J Exp Med 206: 561-576 10.1084/jem.20081886.
44. Linterman MA, Vinuesa CG, (2010) T follicular helper cells during immunity and tolerance. Prog Mol Biol Transl Sci 92: 207-248 10.1016/S1877-1173(10)92009-7.
45. Kuchen S, Robbins R, Sims GP, Sheng C, Phillips TM, et al. (2007) Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J Immunol 179: 5886-5896.
46. Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS, et al. (2005) IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 175: 7867-7879.
47. Ozaki K, Spolski R, Ettinger R, Kim HP, Wang G, et al. (2004) Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of blimp-1 and bcl-6. J Immunol 173: 5361-5371.
48. Metcalf TU, Griffin DE, (2011) Alphavirus-induced encephalomyelitis: Antibody-secreting cells and viral clearance from the nervous system. J Virol 85: 11490-11501 10.1128/JVI.05379-11.
49. Mathian A, Gallegos M, Pascual V, Banchereau J, Koutouzov S, (2011) Interferon-alpha induces unabated production of short-lived plasma cells in pre-autoimmune lupus-prone (NZBxNZW)F1 mice but not in BALB/c mice. Eur J Immunol 41: 863-872 10.1002/eji.201040649; 10.1002/eji.201040649.
50. Odegard JM, Marks BR, DiPlacido LD, Poholek AC, Kono DH, et al. (2008) ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity. J Exp Med 205: 2873-2886 10.1084/jem.20080840.
51. Rupprecht CE, Briggs D, Brown CM, Franka R, Katz SL, et al. (2010) Use of a reduced (4-dose) vaccine schedule for postexposure prophylaxis to prevent human rabies: Recommendations of the advisory committee on immunization practices. MMWR Recomm Rep 59: 1-9.
52. WHO (1997) WHO recommendations on rabies post-exposure treatment and the correct technique of intradermal immunization against rabies. World Health Organization. WHO/EMC/ZOO/96.6.
53. WHO (2009) Current WHO guidelines for rabies pre- and post-exposure treatment in humans. World Health Organization.
54. McGettigan JP, (2010) Experimental rabies vaccines for humans. Expert Rev Vaccines 9: 1177-1186 10.1586/erv.10.105.
55. Plotkin SA, (2008) Vaccines: Correlates of vaccine-induced immunity. Clin Infect Dis 47: 401-409 10.1086/589862.
56. Perry LL, Lodmell DL, (1991) Role of CD4+ and CD8+ T cells in murine resistance to street rabies virus. J Virol 65: 3429-3434.
57. Bunschoten H, Dietzschold B, Claassen I, Klapmuts R, Uytdehaag F, et al. (1990) Rabies virus cross-reactive murine T cell clones: Analysis of helper and delayed-type hypersensitivity function. Viral Immunol 3: 41-53.
58. Jackson AC, Wunner WH, editors (2007) Rabies. Elevier, Inc. 11-19 p.
59. Mifune K, Takeuchi E, Napiorkowski PA, Yamada A, Sakamoto K, (1981) Essential role of T cells in the postexposure prophylaxis of rabies in mice. Microbiol Immunol 25: 895-904.
60. Turner GS, (1976) Thymus dependence of rabies vaccine. J Gen Virol 33: 535-538.
61. Rankin AL, MacLeod H, Keegan S, Andreyeva T, Lowe L, et al. (2011) IL-21 receptor is critical for the development of memory B cell responses. J Immunol 186: 667-674 10.4049/jimmunol.0903207.
62. Zotos D, Coquet JM, Zhang Y, Light A, D'Costa K, et al. (2010) IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J Exp Med 207: 365-378 10.1084/jem.20091777.
63. Jin H, Carrio R, Yu A, Malek TR, (2004) Distinct activation signals determine whether IL-21 induces B cell costimulation, growth arrest, or bim-dependent apoptosis. J Immunol 173: 657-665.
64. Pelletier N, McHeyzer-Williams LJ, Wong KA, Urich E, Fazilleau N, et al. (2010) Plasma cells negatively regulate the follicular helper T cell program. Nat Immunol 11: 1110-1118 10.1038/ni.1954; 10.1038/ni.1954.