The sympathetic nervous system modulates CD4+FoxP3+ regulatory T cells via a TGF-β-dependent mechanism

Journal of Leukocyte Biology

Volumn 86, Issue 6, 2009, Pages 1275-1283

  Bhowmick, Sourojit ^a   Singh, Anurag ^a   Flavell, Richard A ^b   Clark, Robert B ^a   O'Rourke, James ^a   Cone, Robert E ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EAE; Neuroimmunology; Sympathectomy

Indexed keywords

OXIDOPAMINE; TRANSFORMING GROWTH FACTOR BETA;

ADRENERGIC SYSTEM; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CHEMICAL SYMPATHECTOMY; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; FEMALE; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SYMPATHETIC INNERVATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; LYMPH NODES; MICE; MICE, KNOCKOUT; OXIDOPAMINE; SPLEEN; STRESS, PHYSIOLOGICAL; SYMPATHETIC NERVOUS SYSTEM; SYMPATHOLYTICS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

MURINAE;

EID: 73149105743     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0209107     Document Type: Article

References (60)

1. Hogquist, K. A., Baldwin, T. A., Jameson, S. C. (2005) Central tolerance: learning self-control in the thymus. Nat. Rev. Immunol. 5, 772-782.
2. Goodnow, C. C., Sprent, J., Fazekas de St Groth, B., Vinuesa, C. G. (2005) Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435, 590-597.
3. Fontenot, J. D., Gavin, M. A., Rudensky, A. Y. (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336.
4. Sakaguchi, S. (2005) Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352.
5. Annacker, O., Pimenta-Araujo, R., Burlen-Defranoux, O., Barbosa, T. C., Cumano, A., Bandeira, A. (2001) CD25+ CD4+ T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J. Immunol. 166, 3008-3018.
6. Chen, W., Jin, W., Hardegen, N., Lei, K. J., Li, L., Marinos, N., McGrady, G., Wahl, S. M. (2003) Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886.
7. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A., Rudensky, A. Y. (2005) A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151.
8. Mills, K. H. (2004) Regulatory T cells: friend or foe in immunity to infection? Nat. Rev. Immunol. 4, 841-855.
9. O'Connor, R. A., Anderton, S. M. (2008) Foxp3+ regulatory T cells in the control of experimental CNS autoimmune disease. J. Neuroimmunol. 193, 1-11.
10. Huber, S., Schramm, C. (2006) TGF-β and CD4+CD25+ regulatory T cells. Front. Biosci. 11, 1014-1023.
11. Annacker, O., Pimenta-Araujo, R., Burlen-Defranoux, O., Bandeira, A. (2001) On the ontogeny and physiology of regulatory T cells. Immunol. Rev. 182, 5-17.
12. Liu, W., Putnam, A. L., Xu-Yu, Z., Szot, G. L., Lee, M. R., Zhu, S., Gottlieb, P. A., Kapranov, P., Gingeras, T. R., Fazekas de St Groth, B., Clayberger, C., Soper, D. M., Ziegler, S. F., Bluestone, J. A. (2006) CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203, 1701-1711.
13. Bellinger, D. L., Millar, B. A., Perez, S., Carter, J., Wood, C., ThyagaRajan, S., Molinaro, C., Lubahn, C., Lorton, D. (2008) Sympathetic modulation of immunity: relevance to disease. Cell. Immunol. 252, 27-56.
14. Elenkov, I. J., Wilder, R. L., Chrousos, G. P., Vizi, E. S. (2000) The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 52, 595-638.
15. Wrona, D. (2006) Neural-immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems. J. Neuroimmunol. 172, 38-58.
16. Weihe, E., Nohr, D., Michel, S., Muller, S., Zentel, H. J., Fink, T., Krekel, J. (1991) Molecular anatomy of the neuro-immune connection. Int. J. Neurosci. 59, 1-23.
17. Madden, K. S., Sanders, V. M., Felten, D. L. (1995) Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 35, 417-448.
18. Madden, K. S., Stevens, S. Y., Felten, D. L., Bellinger, D. L. (2000) Alterations in T lymphocyte activity following chemical sympathectomy in young and old Fischer 344 rats. J. Neuroimmunol. 103, 131-145.
19. Kostrzewa, R. M., Jacobowitz, D. M. (1974) Pharmacological actions of 6-hydroxydopamine. Pharmacol. Rev. 26, 199-288.
20. Cross, R. J., Brooks, W. H., Roszman, T. L. (1987) Modulation of T-suppressor cell activity by central nervous system catecholamine depletion. J. Neurosci. Res. 18, 75-81.
21. Cross, R. J., Jackson, J. C., Brooks, W. H., Sparks, D. L., Markesbery, W. R., Roszman, T. L. (1986) Neuroimmunomodulation: impairment of humoral immune responsiveness by 6-hydroxydopamine treatment. Immunology 57, 145-152.
22. Karpus, W. J., Konkol, R. J., Killen, J. A. (1988) Central catecholamine neurotoxin administration. 1. Immunological changes associated with the suppression of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 18, 61-73.
23. Felten, D. L., Livnat, S., Felten, S. Y., Carlson, S. L., Bellinger, D. L., Yeh, P. (1984) Sympathetic innervation of lymph nodes in mice. Brain Res. Bull. 13, 693-699.
24. Leo, N. A., Bonneau, R. H. (2000) Mechanisms underlying chemical sympathectomy-induced suppression of herpes simplex virus-specific cytotoxic T lymphocyte activation and function. J. Neuroimmunol. 110, 45-56.
25. Li, X., Taylor, S., Zegarelli, B., Shen, S., O'Rourke, J., Cone, R. E. (2004) The induction of splenic suppressor T cells through an immune-privileged site requires an intact sympathetic nervous system. J. Neuroimmunol. 153, 40-49.
26. Minagawa, M., Oya, H., Yamamoto, S., Shimizu, T., Bannai, M., Kawamura, H., Hatakeyama, K., Abo, T. (2000) Intensive expansion of natural killer T cells in the early phase of hepatocyte regeneration after partial hepatectomy in mice and its association with sympathetic nerve activation. Hepatology 31, 907-915.
27. Sonoda, K. H., Exley, M., Snapper, S., Balk, S. P., Stein-Streilein, J. (1999) CD1-reactive natural killer T cells are required for development of systemic tolerance through an immune-privileged site. J. Exp. Med. 190, 1215-1226.
28. Lu, L., Cantor, H. (2008) Generation and regulation of CD8(+) regulatory T cells. Cell. Mol. Immunol. 5, 401-406.
29. Smith, T. R., Kumar, V. (2008) Revival of CD8+ Treg-mediated suppression. Trends Immunol. 29, 337-342.
30. Lee, Y. H., Ishida, Y., Rifa'i, M., Shi, Z., Isobe, K., Suzuki, H. (2008) Essential role of CD8+CD122+ regulatory T cells in the recovery from experimental autoimmune encephalomyelitis. J. Immunol. 180, 825-832.
31. Fontenot, J. D., Rasmussen, J. P., Williams, L. M., Dooley, J. L., Farr, A. G., Rudensky, A. Y. (2005) Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22, 329-341.
32. Gavin, M. A., Clarke, S. R., Negrou, E., Gallegos, A., Rudensky, A. (2002) Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 3, 33-41.
33. Gorelik, L., Flavell, R. A. (2000) Abrogation of TGFβ signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12, 171-181.
34. Wohlfert, E. A., Callahan, M. K., Clark, R. B. (2004) Resistance to CD4+CD25+ regulatory T cells and TGF-β in Cbl-b-/- mice. J. Immunol. 173, 1059-1065.
35. Kohm, A. P., Carpentier, P. A., Anger, H. A., Miller, S. D. (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.
36. Korn, T., Reddy, J., Gao, W., Bettelli, E., Awasthi, A., Petersen, T. R., Backstrom, B. T., Sobel, R. A., Wucherpfennig, K. W., Strom, T. B., Oukka, M., Kuchroo, V. K. (2007) Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13, 423-431.
37. Konkol, R. J., Wesselmann, U., Karpus, W. J., Leo, G. L., Killen, J. A., Roerig, D. L. (1990) Suppression of clinical weakness in experimental autoimmune encephalomyelitis associated with weight changes, and post-decapitation convulsions after intracisternal-ventricular administration of 6-hydroxydopamine. J. Neuroimmunol. 26, 25-34.
38. Chelmicka-Schorr, E., Checinski, M., Arnason, B. G. (1988) Chemical sympathectomy augments the severity of experimental allergic encephalomyelitis. J. Neuroimmunol. 17, 347-350.
39. Chelmicka-Schorr, E., Kwasniewski, M. N., Wollmann, R. L. (1992) Sympathectomy augments adoptively transferred experimental allergic encephalomyelitis. J. Neuroimmunol. 37, 99-103.
40. Pal, E., Yamamura, T., Tabira, T. (1999) Autonomic regulation of experimental autoimmune encephalomyelitis in IL-4 knockout mice. J. Neuroimmunol. 100, 149-155.
41. Lorton, D., Lubahn, C., Klein, N., Schaller, J., Bellinger, D. L. (1999) Dual role for noradrenergic innervation of lymphoid tissue and arthritic joints in adjuvant-induced arthritis. Brain Behav. Immun. 13, 315-334.
42. Chattopadhyay, S., O'Rourke, J., Cone, R. E. (2008) Implication for the CD94/NKG2A-Qa-1 system in the generation and function of ocular-induced splenic CD8+ regulatory T cells. Int. Immunol. 20, 509-516.
43. McCluskey, R. T., Benacerraf, B., McCluskey, J. W. (1963) Studies on the specificity of the cellular infiltrate in delayed hypersensitivity reactions. J. Immunol. 90, 466-477.
44. Khalil, Z., Helme, R. D. (1989) Sympathetic neurons modulate plasma extravasation in the rat through a non-adrenergic mechanism. Clin. Exp. Neurol. 26, 45-50.
45. Miao, F. J., Janig, W., Levine, J. (1996) Role of sympathetic postganglionic neurons in synovial plasma extravasation induced by bradykinin. J. Neurophysiol. 75, 715-724.
46. Wan, Y. Y., Flavell, R. A. (2006) The roles for cytokines in the generation and maintenance of regulatory T cells. Immunol. Rev. 212, 114-130.
47. Walker, L. S., Chodos, A., Eggena, M., Dooms, H., Abbas, A. K. (2003) Antigen-dependent proliferation of CD4+ CD25+ regulatory T cells in vivo. J. Exp. Med. 198, 249-258.
48. Liang, S., Alard, P., Zhao, Y., Parnell, S., Clark, S. L., Kosiewicz, M. M. (2005) Conversion of CD4+ CD25- cells into CD4+ CD25+ regulatory T cells in vivo requires B7 costimulation, but not the thymus. J. Exp. Med. 201, 127-137.
49. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C., von Boehmer, H. (2005) Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6, 1219-1227.
50. Knoechel, B., Lohr, J., Kahn, E., Bluestone, J. A., Abbas, A. K. (2005) Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J. Exp. Med. 202, 1375-1386.
51. Hori, S., Nomura, T., Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061.
52. Marie, J. C., Letterio, J. J., Gavin, M., Rudensky, A. Y. (2005) TGF-β1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 201, 1061-1067.
53. Fisher, S. A., Absher, M. (1995) Norepinephrine and ANG II stimulate secretion of TGF-β by neonatal rat cardiac fibroblasts in vitro. Am. J. Physiol. 268, C910-C917.
54. Ayache, N., Boumediene, K., Mathy-Hartert, M., Reginster, J. Y., Henrotin, Y., Pujol, J. P. (2002) Expression of TGF-βs and their receptors is differentially modulated by reactive oxygen species and nitric oxide in human articular chondrocytes. Osteoarthritis Cartilage 10, 344-352.
55. Liu, Y., Teige, I., Birnir, B., Issazadeh-Navikas, S. (2006) Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat. Med. 12, 518-525.
56. Yang, J., Brook, M. O., Carvalho-Gaspar, M., Zhang, J., Ramon, H. E., Sayegh, M. H., Wood, K. J., Turka, L. A., Jones, N. D. (2007) Allograft rejection mediated by memory T cells is resistant to regulation. Proc. Natl. Acad. Sci. USA 104, 19954-19959.
57. Morrissey, D. M., Brookes, V. S., Cooke, W. T. (1953) Sympathectomy in the treatment of hypertension; review of 122 cases. Lancet 1, 403-408.
58. Pope, J. E. (1996) Treatment of systemic sclerosis. Rheum. Dis. Clin. North Am. 22, 893-907.
59. Moak, J. P., Eldadah, B., Holmes, C., Pechnik, S., Goldstein, D. S. (2005) Partial cardiac sympathetic denervation after bilateral thoracic sympathectomy in humans. Heart Rhythm 2, 602-609.
60. Gordon, A., Zechmeister, K., Collin, J. (1994) The role of sympathectomy in current surgical practice. Eur. J. Vasc. Surg. 8, 129-137.