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PLOS ONE  2014 

Premature CD4+ T Cell Aging and Its Contribution to Lymphopenia-Induced Proliferation of Memory Cells in Autoimmune-Prone Non-Obese Diabetic Mice

DOI: 10.1371/journal.pone.0089379

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Abstract:

Lymphopenia-induced proliferation (LIP), a mechanism to maintain a constant number of T cells in circulation, occurs in both normal aging and autoimmune disease. The incidence of most autoimmune diseases increases with age, and premature CD4+ T cell aging has been reported in several autoimmune diseases. In this study, we tested the hypothesis that premature CD4+ T cell aging can cause autoimmune disease by examining whether premature CD4+ T cell aging exists and causes LIP in our mouse model. Non-obese diabetic (NOD) mice were used because, in addition to Treg defects, the LIP of T cells has been shown to plays a causative role in the development of insulin-dependent diabetes mellitus (IDDM) in these mice. We found that with advancing age, NOD mice exhibited an accelerated decrease in the number of CD4+ T cells due to the loss of na?ve cells. This was accompanied by an increase in the percentage of memory cells, leading to a reduced na?ve/memory ratio. In addition, both the percentage of CD28+ cells in CD4+ T cells and IL-2 production decreased, while the percentage of FAS+CD44+ increased, suggesting that NOD mice exhibit premature CD4+ T cell aging. This process preferentially contributed to LIP of memory cells. Therefore, our results suggest that premature CD4+ T cell aging underlies the development of IDDM in NOD mice. Given that CD28 and IL-2 play important roles in Treg function, the relationships between premature CD4+ T cell aging and lymphopenia as well as Treg defects in autoimmune-prone NOD mice are proposed.

References

[1]  Naylor K, Li G, Vallejo AN, Lee WW, Koetz K, et al. (2005) The influence of age on T cell generation and TCR diversity. J Immunol 174: 7446–7452. doi: 10.4049/jimmunol.174.11.7446
[2]  Woods JA, Ceddia MA, Zack MD, Lowder TW, Lu Q (2003) Exercise training increases the naive to memory T cell ratio in old mice. Brain Behav Immun 17: 384–392. doi: 10.1016/s0889-1591(03)00030-8
[3]  King C, Ilic A, Koelsch K, Sarvetnick N (2004) Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117: 265–277. doi: 10.1016/s0092-8674(04)00335-6
[4]  Jang E, Kim HR, Cho SH, Paik DJ, Kim JM, et al. (2006) Prevention of spontaneous arthritis by inhibiting homeostatic expansion of autoreactive CD4+ T cells in the K/BxN mouse model. Arthritis Rheum 54: 492–498. doi: 10.1002/art.21567
[5]  Goronzy JJ, Weyand CM (2003) Aging, autoimmunity and arthritis: T-cell senescence and contraction of T-cell repertoire diversity - catalysts of autoimmunity and chronic inflammation. Arthritis Res Ther 5: 225–234.
[6]  Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, et al. (2006) Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212: 8–27. doi: 10.1111/j.0105-2896.2006.00427.x
[7]  Sgouroudis E, Piccirillo CA (2009) Control of type 1 diabetes by CD4+Foxp3+ regulatory T cells: lessons from mouse models and implications for human disease. Diabetes Metab Res Rev 25: 208–218. doi: 10.1002/dmrr.945
[8]  Lin MH, Chou FC, Yeh LT, Fu SH, Chiou HY, et al. (2013) B lymphocyte-induced maturation protein 1 (BLIMP-1) attenuates autoimmune diabetes in NOD mice by suppressing Th1 and Th17 cells. Diabetologia 56: 136–146. doi: 10.1007/s00125-012-2722-y
[9]  Chang X, Zheng P, Liu Y (2008) Homeostatic proliferation in the mice with germline FoxP3 mutation and its contribution to fatal autoimmunity. J Immunol 181: 2399–2406. doi: 10.4049/jimmunol.181.4.2399
[10]  McHugh RS, Shevach EM (2002) Cutting edge: depletion of CD4+CD25+ regulatory T cells is necessary, but not sufficient, for induction of organ-specific autoimmune disease. J Immunol 168: 5979–5983. doi: 10.4049/jimmunol.168.12.5979
[11]  Goronzy JJ, Fujii H, Weyand CM (2006) Telomeres, immune aging and autoimmunity. Exp Gerontol 41: 246–251. doi: 10.1016/j.exger.2005.12.002
[12]  Thewissen M, Linsen L, Somers V, Geusens P, Raus J, et al. (2005) Premature immunosenescence in rheumatoid arthritis and multiple sclerosis patients. Ann N Y Acad Sci 1051: 255–262. doi: 10.1196/annals.1361.066
[13]  Goronzy JJ, Weyand CM (2005) Rheumatoid arthritis. Immunol Rev 204: 55–73. doi: 10.1111/j.0105-2896.2005.00245.x
[14]  Prelog M, Schwarzenbrunner N, Sailer-Hock M, Kern H, Klein-Franke A, et al. (2008) Premature aging of the immune system in children with juvenile idiopathic arthritis. Arthritis Rheum 58: 2153–2162. doi: 10.1002/art.23599
[15]  Zou JX, Rollison DE, Boulware D, Chen DT, Sloand EM, et al. (2009) Altered naive and memory CD4+ T-cell homeostasis and immunosenescence characterize younger patients with myelodysplastic syndrome. Leukemia 23: 1288–1296. doi: 10.1038/leu.2009.14
[16]  Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5: 133–139. doi: 10.1038/ni1033
[17]  Kovaiou RD, Grubeck-Loebenstein B (2006) Age-associated changes within CD4+ T cells. Immunol Lett 107: 8–14. doi: 10.1016/j.imlet.2006.07.006
[18]  Nikolich-Zugich J (2005) T cell aging: naive but not young. J Exp Med 201: 837–840. doi: 10.1084/jem.20050341
[19]  Weiskopf D, Weinberger B, Grubeck-Loebenstein B (2009) The aging of the immune system. Transpl Int 22: 1041–1050. doi: 10.1111/j.1432-2277.2009.00927.x
[20]  Lerner A, Yamada T, Miller RA (1989) Pgp-1hi T lymphocytes accumulate with age in mice and respond poorly to concanavalin A. Eur J Immunol. 19: 977–982. doi: 10.1002/eji.1830190604
[21]  Fulop T Jr, Larbi A, Dupuis G, Pawelec G (2003) Ageing, autoimmunity and arthritis: Perturbations of TCR signal transduction pathways with ageing - a biochemical paradigm for the ageing immune system. Arthritis Res Ther 5: 290–302.
[22]  Maue AC, Yager EJ, Swain SL, Woodland DL, Blackman MA, et al. (2009) T-cell immunosenescence: lessons learned from mouse models of aging. Trends in Immunology 30: 301–305. doi: 10.1016/j.it.2009.04.007
[23]  Pawelec G, Wagner W, Adibzadeh M, Engel A (1999) T cell immunosenescence in vitro and in vivo. Exp Gerontol 34: 419–429. doi: 10.1016/s0531-5565(99)00002-9
[24]  Wakikawa A, Utsuyama M, Hirokawa K (1997) Altered expression of various receptors on T cells in young and old mice after mitogenic stimulation: a flow cytometric analysis. Mechanisms of Ageing and Development 94: 113–122. doi: 10.1016/s0047-6374(97)01880-0
[25]  Potestio M, Pawelec G, Di Lorenzo G, Candore G, D'Anna C, et al. (1999) Age-related changes in the expression of CD95 (APO1/FAS) on blood lymphocytes. Exp Gerontol 34: 659–673. doi: 10.1016/s0531-5565(99)00041-8
[26]  Zhou T, Edwards CK 3rd, Mountz JD (1995) Prevention of age-related T cell apoptosis defect in CD2-fas-transgenic mice. J Exp Med 182: 129–137. doi: 10.1084/jem.182.1.129
[27]  Prelog M, Schonlaub J, Wurzner R, Koppelstaetter C, Almanzar G, et al. (2013) Lower CD28+ T cell proportions were associated with CMV-seropositivity in patients with Hashimoto's thyroiditis. BMC Endocr Disord 13: 34. doi: 10.1186/1472-6823-13-34
[28]  Fasth AE, Cao D, van Vollenhoven R, Trollmo C, Malmstrom V (2004) CD28nullCD4+ T cells—characterization of an effector memory T-cell population in patients with rheumatoid arthritis. Scand J Immunol 60: 199–208. doi: 10.1111/j.0300-9475.2004.01464.x
[29]  Koizumi T, Nakao Y, Matsui T, Katakami Y, Nakagawa T, et al. (1986) Synergistic induction by calcium ionophore and phorbol ester of interleukin-2 (IL-2) receptor expression, IL-2 production, and proliferation in autoimmune MRL/MP-lpr mice. Immunology 59: 43–49.
[30]  Goudy KS, Johnson MC, Garland A, Li C, Samulski RJ, et al. (2011) Reduced IL-2 expression in NOD mice leads to a temporal increase in CD62Llo FoxP3+ CD4+ T cells with limited suppressor activity. Eur J Immunol 41: 1480–1490. doi: 10.1002/eji.201040890
[31]  Sansoni P, Cossarizza A, Brianti V, Fagnoni F, Snelli G, et al. (1993) Lymphocyte subsets and natural killer cell activity in healthy old people and centenarians. Blood 82: 2767–2773.
[32]  Utsuyama M, Hirokawa K, Kurashima C, Fukayama M, Inamatsu T, et al. (1992) Differential age-change in the numbers of CD4+CD45RA+ and CD4+CD29+ T cell subsets in human peripheral blood. Mech Ageing Dev 63: 57–68. doi: 10.1016/0047-6374(92)90016-7
[33]  Formby B, Miller N, Peterson CM (1988) Adoptive immunotherapy of diabetes in autologous nonobese diabetic mice with lymphoid cells ex vivo exposed to cyclosporin plus interleukin 2. Diabetes 37: 1305–1309. doi: 10.2337/diabetes.37.9.1305
[34]  Serreze DV, Chapman HD, Post CM, Johnson EA, Suarez-Pinzon WL, et al. (2001) Th1 to Th2 cytokine shifts in nonobese diabetic mice: sometimes an outcome, rather than the cause, of diabetes resistance elicited by immunostimulation. J Immunol 166: 1352–1359. doi: 10.4049/jimmunol.166.2.1352
[35]  Maehr R, Mintern JD, Herman AE, Lennon-Dumenil AM, Mathis D, et al. (2005) Cathepsin L is essential for onset of autoimmune diabetes in NOD mice. J Clin Invest 115: 2934–2943. doi: 10.1172/jci25485
[36]  Wong S, Guerder S, Visintin I, Reich EP, Swenson KE, et al. (1995) Expression of the co-stimulator molecule B7-1 in pancreatic beta-cells accelerates diabetes in the NOD mouse. Diabetes 44: 326–329. doi: 10.2337/diabetes.44.3.326
[37]  Lee N, Shin MS, Kang I (2012) T-cell biology in aging, with a focus on lung disease. J Gerontol A Biol Sci Med Sci 67: 254–263.
[38]  Effros RB, Dagarag M, Spaulding C, Man J (2005) The role of CD8+ T-cell replicative senescence in human aging. Immunol Rev 205: 147–157. doi: 10.1111/j.0105-2896.2005.00259.x
[39]  Vallejo AN, Weyand CM, Goronzy JJ (2004) T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends Mol Med 10: 119–124. doi: 10.1016/j.molmed.2004.01.002
[40]  Warrington KJ, Takemura S, Goronzy JJ, Weyand CM (2001) CD4+,CD28- T cells in rheumatoid arthritis patients combine features of the innate and adaptive immune systems. Arthritis Rheum 44: 13–20. doi: 10.1002/1529-0131(200101)44:1<13::aid-anr3>3.0.co;2-6
[41]  Groh V, Bruhl A, El-Gabalawy H, Nelson JL, Spies T (2003) Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc Natl Acad Sci U S A 100: 9452–9457. doi: 10.1073/pnas.1632807100
[42]  Yen JH, Moore BE, Nakajima T, Scholl D, Schaid DJ, et al. (2001) Major histocompatibility complex class I-recognizing receptors are disease risk genes in rheumatoid arthritis. J Exp Med 193: 1159–1167. doi: 10.1084/jem.193.10.1159
[43]  Snyder MR, Muegge LO, Offord C, O'Fallon WM, Bajzer Z, et al. (2002) Formation of the killer Ig-like receptor repertoire on CD4+CD28null T cells. J Immunol 168: 3839–3846. doi: 10.4049/jimmunol.168.8.3839
[44]  Azuma M, Phillips JH, Lanier LL (1993) CD28- T lymphocytes. Antigenic and functional properties. The Journal of Immunology 150: 1147–1159.
[45]  Boucher N, Dufeu-Duchesne T, Vicaut E, Farge D, Effros RB, et al. (1998) CD28 expression in T cell aging and human longevity. Exp Gerontol 33: 267–282. doi: 10.1016/s0531-5565(97)00132-0
[46]  Effros RB (1997) Loss of CD28 expression on T lymphocytes: a marker of replicative senescence. Dev Comp Immunol 21: 471–478. doi: 10.1016/s0145-305x(97)00027-x
[47]  Wakikawa A, Utsuyama M, Hirokawa K (1997) Altered expression of various receptors on T cells in young and old mice after mitogenic stimulation: a flow cytometric analysis. Mech Ageing Dev 94: 113–122. doi: 10.1016/s0047-6374(97)01880-0
[48]  Yu A, Olosz F, Choi CY, Malek TR (2000) Efficient internalization of IL-2 depends on the distal portion of the cytoplasmic tail of the IL-2R common gamma-chain and a lymphoid cell environment. J Immunol 165: 2556–2562. doi: 10.4049/jimmunol.165.5.2556
[49]  Stoffel B, Bauer P, Nix M, Deres K, Stoffel W (1998) Ceramide-independent CD28 and TCR signaling but reduced IL-2 secretion in T cells of acid sphingomyelinase-deficient mice. Eur J Immunol 28: 874–880. doi: 10.1002/(sici)1521-4141(199803)28:03<874::aid-immu874>3.0.co;2-t
[50]  Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, et al. (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133: 1710–1715.
[51]  Seddon B, Zamoyska R (2002) TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naive T cells. J Immunol 169: 3752–3759. doi: 10.4049/jimmunol.169.7.3752
[52]  Min B, Yamane H, Hu-Li J, Paul WE (2005) Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J Immunol 174: 6039–6044. doi: 10.4049/jimmunol.174.10.6039
[53]  Ernst B, Lee DS, Chang JM, Sprent J, Surh CD (1999) The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 11: 173–181. doi: 10.1016/s1074-7613(00)80092-8
[54]  Goldrath AW, Bevan MJ (1999) Low-affinity ligands for the TCR drive proliferation of mature CD8+ T cells in lymphopenic hosts. Immunity 11: 183–190. doi: 10.1016/s1074-7613(00)80093-x
[55]  Schluns KS, Kieper WC, Jameson SC, Lefrancois L (2000) Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 1: 426–432. doi: 10.1038/80868
[56]  Tan JT, Dudl E, LeRoy E, Murray R, Sprent J, et al. (2001) IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci U S A 98: 8732–8737. doi: 10.1073/pnas.161126098
[57]  Zipris D, Lazarus AH, Crow AR, Hadzija M, Delovitch TL (1991) Defective thymic T cell activation by concanavalin A and anti-CD3 in autoimmune nonobese diabetic mice. Evidence for thymic T cell anergy that correlates with the onset of insulitis. J Immunol 146: 3763–3771.
[58]  Yamanouchi J, Rainbow D, Serra P, Howlett S, Hunter K, et al. (2007) Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat Genet 39: 329–337. doi: 10.1038/ng1958
[59]  Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, et al. (2008) Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28: 687–697. doi: 10.1016/j.immuni.2008.03.016
[60]  Wicker LS, Todd JA, Prins JB, Podolin PL, Renjilian RJ, et al. (1994) Resistance alleles at two non-major histocompatibility complex-linked insulin-dependent diabetes loci on chromosome 3, Idd3 and Idd10, protect nonobese diabetic mice from diabetes. J Exp Med 180: 1705–1713. doi: 10.1084/jem.180.5.1705
[61]  Dendrou CA, Wicker LS (2008) The IL-2/CD25 pathway determines susceptibility to T1D in humans and NOD mice. J Clin Immunol 28: 685–696. doi: 10.1007/s10875-008-9237-9
[62]  Wicker LS, Clark J, Fraser HI, Garner VE, Gonzalez-Munoz A, et al. (2005) Type 1 diabetes genes and pathways shared by humans and NOD mice. J Autoimmun 25 Suppl: 29?33 doi: 10.1016/j.jaut.2005.09.009
[63]  McGuire HM, Vogelzang A, Hill N, Flodstrom-Tullberg M, Sprent J, et al. (2009) Loss of parity between IL-2 and IL-21 in the NOD Idd3 locus. Proc Natl Acad Sci U S A 106: 19438–19443. doi: 10.1073/pnas.0903561106
[64]  Datta S, Sarvetnick NE (2008) IL-21 limits peripheral lymphocyte numbers through T cell homeostatic mechanisms. PLoS One 3: e3118. doi: 10.1371/journal.pone.0003118
[65]  Moralejo DH, Fuller JM, Rutledge EA, Van Yserloo B, Ettinger RA, et al. (2011) BB rat Gimap gene expression in sorted lymphoid T and B cells. Life Sci 89: 748–754. doi: 10.1016/j.lfs.2011.08.016
[66]  Rutledge EA, Fuller JM, Van Yserloo B, Moralejo DH, Ettinger RA, et al. (2009) Sequence variation and expression of the Gimap gene family in the BB rat. Exp Diabetes Res 2009: 835650. doi: 10.1155/2009/835650
[67]  Subra JF, Renier G, Reboul P, Tollis F, Boivinet R, et al. (2001) Lymphopenia in occupational pulmonary silicosis with or without autoimmune disease. Clin Exp Immunol 126: 540–544. doi: 10.1046/j.1365-2249.2001.01696.x
[68]  Koetz K, Bryl E, Spickschen K, O'Fallon WM, Goronzy JJ, et al. (2000) T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci U S A 97: 9203–9208. doi: 10.1073/pnas.97.16.9203
[69]  Marleau AM, Sarvetnick N (2005) T cell homeostasis in tolerance and immunity. J Leukoc Biol 78: 575–584. doi: 10.1189/jlb.0105050
[70]  van der Werf N, Kroese FG, Rozing J, Hillebrands JL (2007) Viral infections as potential triggers of type 1 diabetes. Diabetes Metab Res Rev 23: 169–183. doi: 10.1002/dmrr.695
[71]  Atkinson MA, Leiter EH (1999) The NOD mouse model of type 1 diabetes: as good as it gets? Nat Med 5: 601–604.
[72]  Wetzel JD, Barton ES, Chappell JD, Baer GS, Mochow-Grundy M, et al. (2006) Reovirus delays diabetes onset but does not prevent insulitis in nonobese diabetic mice. J Virol 80: 3078–3082. doi: 10.1128/jvi.80.6.3078-3082.2006
[73]  Schulze-Koops H (2004) Lymphopenia and autoimmune diseases. Arthritis Res Ther 6: 178–180. doi: 10.1186/ar1208
[74]  Selmi C, Mackay IR, Gershwin ME (2011) The autoimmunity of primary biliary cirrhosis and the clonal selection theory. Immunol Cell Biol 89: 70–80. doi: 10.1038/icb.2010.126
[75]  Martin B, Becourt C, Bienvenu B, Lucas B (2006) Self-recognition is crucial for maintaining the peripheral CD4+ T-cell pool in a nonlymphopenic environment. Blood 108: 270–277. doi: 10.1182/blood-2006-01-0017
[76]  Kieper WC, Troy A, Burghardt JT, Ramsey C, Lee JY, et al. (2005) Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 174: 3158–3163. doi: 10.4049/jimmunol.174.6.3158
[77]  Tajima M, Wakita D, Noguchi D, Chamoto K, Yue Z, et al. (2008) IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J Exp Med 205: 1019–1027. doi: 10.1084/jem.20071133
[78]  Rocha B, Freitas AA, Coutinho AA (1983) Population dynamics of T lymphocytes. Renewal rate and expansion in the peripheral lymphoid organs. J Immunol 131: 2158–2164.
[79]  Tanchot C, Rosado MM, Agenes F, Freitas AA, Rocha B (1997) Lymphocyte homeostasis. Semin Immunol 9: 331–337.
[80]  Sprent J, Surh CD (2003) Cytokines and T cell homeostasis. Immunol Lett 85: 145–149. doi: 10.1016/s0165-2478(02)00221-3
[81]  Jameson SC (2005) T cell homeostasis: keeping useful T cells alive and live T cells useful. Semin Immunol 17: 231–237. doi: 10.1016/j.smim.2005.02.003
[82]  Hamilton SE, Wolkers MC, Schoenberger SP, Jameson SC (2006) The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells. Nat Immunol 7: 475–481. doi: 10.1038/ni1326
[83]  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. doi: 10.1084/jem.192.4.557
[84]  Cho BK, Rao VP, Ge Q, Eisen HN, Chen J (2000) Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 192: 549–556. doi: 10.1084/jem.192.4.549
[85]  Winstead CJ, Fraser JM, Khoruts A (2008) Regulatory CD4+CD25+Foxp3+ T cells selectively inhibit the spontaneous form of lymphopenia-induced proliferation of naive T cells. J Immunol 180: 7305–7317. doi: 10.4049/jimmunol.180.11.7305
[86]  Bourgeois C, Kassiotis G, Stockinger B (2005) A major role for memory CD4 T cells in the control of lymphopenia-induced proliferation of naive CD4 T cells. J Immunol 174: 5316–5323. doi: 10.4049/jimmunol.174.9.5316
[87]  Fry TJ, Mackall CL (2001) Interleukin-7: master regulator of peripheral T-cell homeostasis? Trends Immunol 22: 564–571. doi: 10.1016/s1471-4906(01)02028-2
[88]  Dummer W, Ernst B, LeRoy E, Lee D, Surh C (2001) Autologous regulation of naive T cell homeostasis within the T cell compartment. J Immunol 166: 2460–2468. doi: 10.4049/jimmunol.166.4.2460
[89]  Bosco N, Agenes F, Ceredig R (2005) Effects of increasing IL-7 availability on lymphocytes during and after lymphopenia-induced proliferation. J Immunol 175: 162–170. doi: 10.4049/jimmunol.175.1.162
[90]  Miller CN, Hartigan-O'Connor DJ, Lee MS, Laidlaw G, Cornelissen IP, et al. (2013) IL-7 production in murine lymphatic endothelial cells and induction in the setting of peripheral lymphopenia. Int Immunol 25: 471–483. doi: 10.1093/intimm/dxt012
[91]  den Braber I, Mugwagwa T, Vrisekoop N, Westera L, Mogling R, et al. (2012) Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity 36: 288–297. doi: 10.1016/j.immuni.2012.02.006
[92]  Arnold B, Schuler T, Hammerling GJ (2005) Control of peripheral T-lymphocyte tolerance in neonates and adults. Trends Immunol 26: 406–411. doi: 10.1016/j.it.2005.06.002
[93]  Dujardin HC, Burlen-Defranoux O, Boucontet L, Vieira P, Cumano A, et al. (2004) Regulatory potential and control of Foxp3 expression in newborn CD4+ T cells. Proc Natl Acad Sci U S A 101: 14473–14478. doi: 10.1073/pnas.0403303101
[94]  Adkins B, Leclerc C, Marshall-Clarke S (2004) Neonatal adaptive immunity comes of age. Nat Rev Immunol 4: 553–564. doi: 10.1038/nri1394
[95]  Alferink J, Tafuri A, Vestweber D, Hallmann R, Hammerling GJ, et al. (1998) Control of neonatal tolerance to tissue antigens by peripheral T cell trafficking. Science 282: 1338–1341. doi: 10.1126/science.282.5392.1338
[96]  Liston A, Rudensky AY (2007) Thymic development and peripheral homeostasis of regulatory T cells. Curr Opin Immunol 19: 176–185. doi: 10.1016/j.coi.2007.02.005
[97]  Boniface K, Blom B, Liu YJ, de Waal Malefyt R (2008) From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol Rev 226: 132–146. doi: 10.1111/j.1600-065x.2008.00714.x
[98]  Emamaullee JA, Davis J, Merani S, Toso C, Elliott JF, et al. (2009) Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 58: 1302–1311. doi: 10.2337/db08-1113
[99]  Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC (2006) A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 203: 1685–1691. doi: 10.1084/jem.20060285
[100]  Nakae S, Saijo S, Horai R, Sudo K, Mori S, et al. (2003) IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci U S A 100: 5986–5990. doi: 10.1073/pnas.1035999100
[101]  Yen D, Cheung J, Scheerens H, Poulet F, McClanahan T, et al. (2006) IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 116: 1310–1316. doi: 10.1172/jci21404
[102]  Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, et al. (2011) Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad Sci U S A 108: 11548–11553. doi: 10.1073/pnas.1108924108
[103]  Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, et al. (2008) Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455: 1109–1113. doi: 10.1038/nature07336
[104]  Calzascia T, Pellegrini M, Lin A, Garza KM, Elford AR, et al. (2008) CD4 T cells, lymphopenia, and IL-7 in a multistep pathway to autoimmunity. Proc Natl Acad Sci U S A 105: 2999–3004. doi: 10.1073/pnas.0712135105
[105]  Piccirillo CA, Tritt M, Sgouroudis E, Albanese A, Pyzik M, et al. (2005) Control of type 1 autoimmune diabetes by naturally occurring CD4+CD25+ regulatory T lymphocytes in neonatal NOD mice. Ann N Y Acad Sci 1051: 72–87. doi: 10.1196/annals.1361.048
[106]  Le Campion A, Gagnerault MC, Auffray C, Becourt C, Poitrasson-Riviere M, et al. (2009) Lymphopenia-induced spontaneous T-cell proliferation as a cofactor for autoimmune disease development. Blood 114: 1784–1793. doi: 10.1182/blood-2008-12-192120
[107]  Vallejo AN, Brandes JC, Weyand CM, Goronzy JJ (1999) Modulation of CD28 expression: distinct regulatory pathways during activation and replicative senescence. J Immunol 162: 6572–6579.
[108]  Monti P, Scirpoli M, Maffi P, Ghidoli N, De Taddeo F, et al. (2008) Islet transplantation in patients with autoimmune diabetes induces homeostatic cytokines that expand autoreactive memory T cells. J Clin Invest 118: 1806–1814. doi: 10.1172/jci35197
[109]  Rabinovitch A, Suarez-Pinzon WL (2007) Roles of cytokines in the pathogenesis and therapy of type 1 diabetes. Cell Biochem Biophys 48: 159–163. doi: 10.1007/s12013-007-0029-2

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