IL-21 limits peripheral lymphocyte numbers through T cell homeostatic mechanisms

PLoS ONE

Volumn 3, Issue 9, 2008, Pages

  Datta, Shrimati ^a   Sarvetnick, Nora E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 21; ANTIGEN; INTERLEUKIN 21 RECEPTOR; INTERLEUKIN DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; C57BL 6 MOUSE; CELL SIZE; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; HOMEOSTASIS; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PERIPHERAL LYMPHOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL PROLIFERATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS; RODENTIA;

ANIMALS; ANTIGENS; AUTOIMMUNITY; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INTERLEUKINS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MODELS, BIOLOGICAL; RECEPTORS, INTERLEUKIN-21; T-LYMPHOCYTES;

EID: 52349088182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003118     Document Type: Article

References (63)

1. Leonard WJ, Spolski R (2005) Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat Rev Immunol 5: 688-698.
2. Coquet JM, Kyparissoudis K, Pellicci DG, Besra G, Berzins SP, et al. (2007) IL-21 is produced by NKT cells and modulates NKT cell activation and cytokine production. J Immunol 178: 2827-2834.
3. Nurieva R, Yang XO, Martinez G, Zhang Y, Panopoulos AD, et al. (2007) Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483.
4. Davis ID, Skak K, Smyth MJ, Kristjansen PE, Miller DM, et al. (2007) Interleukin-21 signaling: functions in cancer and autoimmunity. Clin Cancer Res 13: 6926-6932.
5. Wurster AL, Rodgers VL, Satoskar AR, Whitters MJ, Young DA, et al. (2002) Interleukin 21 is a T helper (Th) cell 2 cytokine that specifically inhibits the differentiation of naive Th cells into interferon gamma-producing Th1 cells. J Exp Med 196: 969-977.
6. Strengell M, Sareneva T, Foster D, Julkunen I, Matikainen S (2002) IL-21 up-regulates the expression of genes associated with innate immunity and Th1 response. J Immunol 169: 3600-3605.
7. Vollmer TL, Liu R, Price M, Rhodes S, La Cava A, et al. (2005) Differential effects of IL-21 during initiation and progression of autoimmunity against neuroantigen. J Immunol 174: 2696-2701.
8. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, et al. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487.
9. Li Y, Bleakley M, Yee C (2005) IL-21 influences the frequency, phenotype, and affinity of the antigen-specific CD8 T cell response. J Immunol 175: 2261-2269.
10. Zhou L, Ivanov II, Spolski R, Min R, Shenderov K, et al. (2007) IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8: 967-974.
11. 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.
12. 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.
13. Kasaian MT, Whitters MJ, Carter LL, Lowe LD, Jussif JM, et al. (2002) IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity 16: 559-569.
14. Mehta DS, Wurster AL, Whitters MJ, Young DA, Collins M, et al. (2003) IL-21 induces the apoptosis of resting and activated primary B cells. J Immunol 170: 4111-4118.
15. Ostiguy V, Allard EL, Marquis M, Leignadier J, Labrecque N (2007) IL-21 promotes T lymphocyte survival by activating the phosphatidylinositol-3 kinase signaling cascade. J Leukoc Biol 82: 645-656.
16. Zeng R, Spolski R, Finkelstein SE, Oh S, Kovanen PE, et al. (2005) Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med 201: 139-148.
17. King C, Ilic A, Koelsch K, Sarvemick N (2004) Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117: 265-277.
18. Berzins SP, Venanzi ES, Benoist C, Mathis D (2003) T-cell compartments of prediabetic NOD mice. Diabetes 52: 327-334.
19. Barker BR, Parvani JG, Meyer D, Hey AS, Skak K, et al. (2007) IL-21 induces apoptosis of antigen-specific CD8+ T lymphocytes. J Immunol 179: 3596-3603.
20. Theofilopoulos AN, Dummer W, Kono DH (2001) T cell homeostasis and systemic autoimmunity. J Clin Invest 108: 335-340.
21. Baccala R, Theofilopoulos AN (2005) The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 26: 5-8.
22. Goldrath AW, Bogatzki LY, Bevan MJ (2000) Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 192: 557-564.
23. Clarke SR, Barnden M, Kurts C, Carbone FR, Miller JF, et al. (2000) Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol Cell Biol 78: 110-117.
24. Ge Q, Hu H, Eisen HN, Chen J (2002) Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proc Natl Acad Sci U S A 99: 2989-2994.
25. Vivien L, Benoist C, Mathis D (2001) T lymphocytes need IL-7 but not IL-4 or IL-6 to survive in vivo. Int Immunol 13: 763-768.
26. Akashi K, Kondo M, von Freeden-Jeffry U, Murray R, Weissman IL (1997) Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 89: 1033-1041.
27. Liu S, Lizee G, Lou Y, Liu C, Overwijk WW, et al. (2007) IL-21 synergizes with IL-7 to augment, expansion and anti-tumor function of cytotoxic T cells. Int Imnmnol 19: 1213-1221.
28. Gurlo T, Kawamura K, von Grafenstein H (1999) Role of inflammatory infiltrate in activation and effector function of cloned islet reactive nonobese diabetic CD8+ T cells: involvement of a nitric oxide-dependent pathway. J Immunol 163: 5770-5780.
29. Jameson SC (2002) Maintaining the norm: T-cell homeostasis. Nat Rev Immunol 2: 547-556.
30. Goldrath AW, Sivakumar PV, Glaccum M, Kennedy MK, Bevan MJ, et al. (2002) Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med 195:1515-1522.
31. 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.
32. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, et al. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556.
33. Qin JZ, Zhang CL, Kamarashev J, Dummer R, Burg G, et al. (2001) Interleukin-7 and interleukin-15 regulate the expression of the bcl-2 and c-myb genes in cutaneous T-cell lymphoma cells. Blood 98: 2778-2783.
34. Maraskovsky E, O'Reilly LA, Teepe M, Corcoran LM, Peschon JJ, et al. (1997) Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice. Cell 89:1011-1019.
35. Asao H, Okuyama C, Kumaki S, Ishii N, Tsuchiya S, et al. (2001) Cutting edge: the common gamma-chain is an indispensable subunit of the IL-21 receptor complex. J Immunol 167:1 5.
36. Abell K, Bilancio A, Clarkson RW, Tiffen PG, Altaparmakov AI, et al. (2005) Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition. Nat Cell Biol 7: 392-398.
37. Li WQ, Jiang Q, Khaled AR, Keller JR, Durum SK (2004) Interleukin-7 inactivates the pro-apoptotic protein Bad promoting T cell survival. J Biol Chem 279: 29160-29166.
38. Stephanou A, Brar BK, Knight RA, Latchman DS (2000) Opposing actions of STAT-1 and STAT-3 on the Bcl-2 and Bcl-x promoters. Cell Death Differ 7: 329-330.
39. Alves NL, Arosa FA, van Lier RA (2005) IL-21 sustains CD28 expression on IL-15-activated human naive CD8+ T cells. J Immunol 175: 755-762.
40. Habib T, Senadheera S, Weinberg K, Kaushansky K (2002) The common gamma chain (gamma c) is a required signaling component of the IL-21 receptor and supports IL-21-induced cell proliferation via JAK3. Biochemistry 41: 8725-8731.
41. Young DA, Hegen M, Ma HL, Whitters MJ, Albert LM, et al. (2007) Blockade of the interleukin-21/interleukin-21 receptor pathway ameliorates disease in animal models of rheumatoid arthritis. Arthritis Rheum 56:1152-1163.
42. Li J, Shen W, Kong K, Liu Z (2006) Interleukin-21 induces T-cell activation and proinflammatory cytokine secretion in rheumatoid arthritis. Scand J Immunol 64: 515-522.
43. Cantor J, Haskins K (2005) Effector function of diabetogenic CD4 Th1 T cell clones: a central role for TNF-alpha. J Immunol 175: 7738-7745.
44. Haskins K (2005) Pathogenic T-cell clones in autoimmune diabetes: more lessons from the NOD mouse. Adv Immunol 87: 123-162.
45. Sarvetnick N, Shizuru J, Liggitt D, Martin L, McIntyre B, et al. (1990) Loss of pancreatic islet tolerance induced by beta-cell expression of interferon-gamma. Nature 346: 844-847.
46. Falcone M, Lee J, Patstone G, Yeung B, Sarvemick N (1998) B lymphocytes are crucial antigen-presenting cells in the pathogenic autoimmune response to GAD65 antigen in nonobese diabetic mice. J Immunol 161: 1163-1168.
47. Bour-Jordan H, Bluestone JA (2007) B cell depletion: a novel therapy for autoimmune diabetes? J Clin Invest 117: 3642-3645.
48. 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.
49. 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: 1270-137.
50. Luzina IG, Atamas SP, Storrer CE, daSilva LC, Kelsoe G, et al. (2001) Spontaneous formation of germinal centers in autoimmune-mice. J Leukoc Biol 70: 578-584.
51. Serreze DV, Post CM, Chapman HD, Johnson EA, Lu B, et al. (2000) Interferon-gamma receptor signaling is dispensable in the development of autoimmune type 1 diabetes in NOD mice. Diabetes 49: 2007-2011.
52. Rietz C, Screpanti V, Brenden N, Bohme J, Fernandez C (2003) Overexpression of bcl-2 in T cells affects insulitis in the nonobese diabetic mouse. Scand J Immunol 57: 342-349.
53. Giordano C, Stassi G, Todaro M, De Maria R, Richiusa P, et al. (1995) Low bcl-2 expression and increased spontaneous apoptosis in T-lymphocytes from newly-diagnosed IDDM patients. Diabetologia 38 :953-958.
54. Georgescu L, Vakkalanka RK, Elkon KB, Crow MK (1997) Interleukin-10 promotes activation-induced cell death of SLE lymphocytes mediated by Fas ligand. J Clin Invest 100: 2622-2633.
55. Schulze-Koops H (2004) Lymphopenia and autoimmune diseases. Arthritis Res Ther 6: 178-180.
56. Kohm AP, Carpentier PA, Anger HA, Miller SD (2002) Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol 169: 4712-4716.
57. Peluso I, Fantini MC, Fina D, Caruso R, Boirivant M, et al. (2007) IL-21 counteracts the regulatory T cell-mediated suppression of human CD4+ T lymphocytes. J Immunol 178: 732-739.
58. Khoruts A, Fraser JM (2005) A causal link between lymphopenia and autoimmunity. Immunol Lett 98: 23-31.
59. Goronzy JJ, Weyand CM (2001) Thymic function and peripheral T-cell homeostasis in rheumatoid arthritis. Trends Immunol 22: 251-255.
60. Brown IE, Blank C, Kline J, Kacha AK, Gajewski TF (2006) Homeostatic proliferation as an isolated variable reverses CD8+ T cell anergy and promotes tumor rejection. J Immunol 177: 4521-4529.
61. Smyth MJ, Teng MW, Sharkey J, Westwood JA, Haynes NM, et al. (2008) Interleukin 21 enhances antibody-mediated tumor rejection. Cancer Res 68: 3019-3025.
62. Krupica T Jr, Fry TJ, Mackall CL (2006) Autoimmunity during lymphopenia: a two-hit model. Clin Immunol 120: 121-128.
63. Yadav D, Judkowski V, Flodstrom-Tullberg M, Sterling L, Redmond WL, et al. (2004) B7-2 (CD86) controls the priming of autoreactive CD4 T cell response against pancreatic islets. J Immunol 173: 3631-3639.