γ-Aminobutyric acid transporter 1 negatively regulates T cell-mediated immune responses and ameliorates autoimmune inflammation in the CNS

Journal of Immunology

Volumn 181, Issue 12, 2008, Pages 8226-8236

  Wang, Ying ^a   Feng, Dechun ^a   Liu, Guoxiang ^b   Luo, Qingqiong ^a   Xu, Yan ^a   Lin, Shuting ^a   Fei, Jian ^c   Xu, Lingyun ^a,d  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c TONGJI UNIVERSITY   (China)

^d Building I ^*  (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID CARRIER 1; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; STAT1 PROTEIN; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; EPITOPE; SLC6A1 PROTEIN, MOUSE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; MACROPHAGE; MONONUCLEAR CELL; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINAL CORD; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; DOWN REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; DOWN-REGULATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; EPITOPES, T-LYMPHOCYTE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MULTIPLE SCLEROSIS; T-LYMPHOCYTES;

EID: 58849132951     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.12.8226     Document Type: Article

References (50)

1. Andersson, P. B., and D. E. Goodkin. 1996. Current pharmacologic treatment of multiple sclerosis symptoms. West. J. Med. 165: 313-317. (Pubitemid 26425411)
2. Steinman, L. 1996. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 85: 299-302. (Pubitemid 26160700)
3. Lassmann, H., and H. M. Wisniewski. 1979. Chronic relapsing experimental allergic encephalomyelitis: clinicopathological comparison with multiple sclerosis. Arch. Neurol. 36: 490-497. (Pubitemid 9187999)
4. Selmaj, K. W. 2000. Tumour necrosis factor and anti-tumour necrosis factor approach to inflammatory demyelinating diseases of the central nervous system. Ann. Rheum. Dis. 59 (Suppl.): i94-i102. (Pubitemid 30824969)
5. Bettelli, E., and L. B. Nicholson. 2000. The role of cytokines in experimental autoimmune encephalomyelitis. Arch. Immunol. Ther. Exp. (Warsz). 48: 389-398.
6. Samoilova, E. B., J. L. Horton, B. Hilliard, T. S. Liu, and Y. Chen. 1998. IL-6- deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J. Immunol. 161: 6480-6486.
7. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573. (Pubitemid 43939170)
8. Touil, T., D. Fitzgerald, G. X. Zhang, A. M. Rostami, and B. Gran. 2006. Pathophysiology of interleukin-23 in experimental autoimmune encephalomyelitis. Drug News Perspect. 19: 77-83.
9. Hilliard, B. A., N. Mason, L. Xu, J. Sun, S. E. Lamhamedi-Cherradi, H. C. Liou, C. Hunter, and Y. H. Chen. 2002. Critical roles of c-Rel in autoimmune inflammation and helper T cell differentiation. J. Clin. Invest. 110: 843-850.
10. Bettelli, E., B. Sullivan, S. J. Szabo, R. A. Sobel, L. H. Glimcher, and V. K. Kuchroo. 2004. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200: 79-87. (Pubitemid 38924730)
11. Wilder, R. L. 1995. Neuroendocrine-immune system interactions and autoimmunity. Annu. Rev. Immunol. 13: 307-338.
12. Witting, A., L. Chen, E. Cudaback, A. Straiker, L. Walter, B. Rickman, T. Moller, C. Brosnan, and N. Stella. 2006. Experimental autoimmune encephalomyelitis disrupts endocannabinoid-mediated neuroprotection. Proc. Natl. Acad. Sci. USA 103: 6362-6367.
13. Kato, H., A. Ito, J. Kawanokuchi, S. Jin, T. Mizuno, K. Ojika, R. Ueda, and A. Suzumura. 2004. Pituitary adenylate cyclase-activating polypeptide (PACAP) ameliorates experimental autoimmune encephalomyelitis by suppressing the functions of antigen presenting cells. Mult. Scler. 10: 651-659. (Pubitemid 39585244)
14. Pryce, G., Z. Ahmed, D. J. Hankey, S. J. Jackson, J. L. Croxford, J. M. Pocock, C. Ledent, A. Petzold, A. J. Thompson, G. Giovannoni, et al. 2003. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 126: 2191-2202. (Pubitemid 37432364)
15. Pitt, D., P. Werner, and C. S. Raine. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6: 67-70. (Pubitemid 30048528)
16. 1A) receptor antagonist WAY100635 suppresses acute experimental allergic encephalomyelitis in Lewis rats. Neurosci. Lett. 342: 33-36. (Pubitemid 36513903)
17. D'Intino, G., M. Paradisi, M. Fernandez, A. Giuliani, L. Aloe, L. Giardino, and L. Calza. 2005. Cognitive deficit associated with cholinergic and nerve growth factor down-regulation in experimental allergic encephalomyelitis in rats. Proc. Natl. Acad. Sci. USA 102: 3070-3075. (Pubitemid 40299917)
18. Demakova, E. V., V. P. Korobov, and L. M. Lemkina. 2003. Determination of γ-aminobutyric acid concentration and activity of glutamate decarboxylase in blood serum of patients with multiple sclerosis. Klin. Lab. Diagn. 4: 15-17.
19. Gottesfeld, Z., D. Teitelbaum, C. Webb, and R. Arnon. 1976. Changes in the GABA system in experimental allergic encephalomyelitis-induced paralysis. J. Neurochem. 27: 695-699.
20. Rode, G., E. Maupas, J. Luaute, S. Courtois-Jacquin, and D. Boisson. 2003. Medical treatment of spasticity. Neurochirurgie 49: 247-255.
21. Chiu, C. S., S. Brickley, K. Jensen, A. Southwell, S. Mckinney, S. Cull-Candy, I. Mody, and H. A. Lester. 2005. GABA transporter deficiency causes tremor, ataxia, nervousness, and increased GABA-induced tonic conductance in cerebellum. J. Neurosci. 25: 3234-3245.
22. Chen, N. H., M. E. Reith, M. W. Quick. 2004. Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflügers Arch. 447: 519-531.
23. Guastella, J., N. Nelson, H. Nelson, L. Czyzyk, S. Keynan, M. C. Miedel, N. Davidson, H. A. Lester, and B. I. Kanner. 1990. Cloning and expression of a rat brain GABA transporter. Science 249: 1303-1306. (Pubitemid 20347672)
24. Cai, Y. Q., G. Q. Cai, G. X. Liu, Q. Cai, J. H. Shi, J. Shi, S. K. Ma, X. Sun, Z. J. Sheng, Z. T. Mei, et al. 2006. Mice with genetically altered GABA transporter subtype I (GAT1) expression show altered behavioral responses to ethanol. J. Neurosci. Res. 84: 255-267.
25. Becher, B., B. G. Durell, A. V. Miga, W. F. Hickey, and R. J. Noelle. 2001. The clinical course of experimental autoimmune encephalomyelitis and inflammation is controlled by the expression of CD40 within the central nervous system. J. Exp. Med. 193: 967-974. (Pubitemid 32525869)
26. Bright, J. J., C. Du, M. Coon, S. Sriram, and S. J. Klaus. 1998. Prevention of experimental allergic encephalomyelitis via inhibition of IL-12 signaling and IL-12-mediated Th1 differentiation: an effect of the novel anti-inflammatory drug lisofylline. J. Immunol. 161: 7015-7022.
27. Gonzalez-Rey, E., A. Fernandez-Martin, A. Chorny, J. Martin, D. Pozo, D. Ganea, and M. Delgado. 2006. Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am. J. Pathol. 168: 1179-1188.
28. Wang, Y., Y. Mei, S. Bao, and L. Xu. 2007. Vasoactive intestinal polypeptide enhances oral tolerance by regulating both cellular and humoral immune responses. Clin. Exp. Immunol. 148: 178-187.
29. Ruiz-Tachiquín, M. E., E. Sánchez-Lemus, L. E. Soria-Jasso, J. A. Arias- Montaño, and A. Ortega. 2002. γ-aminobutyric acid transporter (BGT-1) expressed in human astrocytoma U373 MG cells: pharmacological and molecular characterization and phorbol ester-induced inhibition. J. Neurosci. Res. 69: 125-132. (Pubitemid 34734173)
30. Kelly, D., J. I. Campbell, T. P. King, G. Grant, E. A. Jansson, A. G. Coutts, S. Pettersson, and S. Conway. 2004. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-γ and RelA. Nat. Immunol. 5: 104-112. (Pubitemid 38081475)
31. Tischner, D., A. Weishaupt, J. van den Brandt, N. Müller, N. Beyersdorf, C. W. Ip, K. V. Toyka, T. Hünig, R. Gold, T. Kerkau, and H. M. Reichardt. 2006. Polyclonal expansion of regulatory T cells interferes with effector cell migration in a model of multiple sclerosis. Brain 129: 2635-2647. (Pubitemid 44522097)
32. Tian, J., Y. Lu, H. Zhang, C. H. Chau, H. N. Dang, and D. L. Kaufman. 2004. γ-aminobutyric acid inhibits T cell autoimmunity and the development of inflammatory responses in a mouse type 1 diabetes model. J. Immunol. 173: 5298-5304. (Pubitemid 39387814)
33. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18: 621-663. (Pubitemid 30365393)
34. O'Garra, A., and N. Arai. 2000. The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell Biol. 10: 542-550. (Pubitemid 30831454)
35. Lighvani, A. A., D. M. Frucht, D. Jankovic, H. Yamane, J. Aliberti, B. D. Hissong, B. V. Nguyen, M. Gadina, A. Sher, W. E. Paul, and J. J. O'Shea. 2001. T-bet is rapidly induced by interferon-γ in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98: 15137-15142.
36. + T cells. Nat. Immunol. 3: 549-557. (Pubitemid 34662307)
37. Bernard, C. C., J. Leydon, and I. R. Mackay. 1976. T cell necessity in the pathogenesis of experimental autoimmune encephalomyelitis in mice. Eur. J. Immunol. 6: 655-660.
38. Kuchroo, V. K., R. A. Sobel, T. Yamamura, E. Greenfield, M. E. Dorf, and M. B. Lees. 1991. Induction of experimental allergic encephalomyelitis by myelin proteolipid-protein-specific T cell clones and synthetic peptides. Pathobiology 59: 305-312.
39. Hilliard, B., E. Samoilova, T. S. Liu, A. Rostami, and Y. Chen. 1999. Experimental autoimmune encephalomyelitis in NF-κB-deficient mice: roles of NF-κB in the activation and differentiation of autoreactive T cells. J. Immunol. 163: 2937-2943. (Pubitemid 29399226)
40. Dasgupta, S., M. Jana, Y. Zhou, Y. K. Fung, S. Ghosh, and K. Pahan. 2004. Antineuroinflammatory effect of NF-κB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis. J. Immunol. 173: 1344-1354. (Pubitemid 38924314)
41. Hur, E. M., S. Youssef, M. E. Haws, S. Y. Zhang, R. A. Sobel, and L. Steinman. 2007. Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat. Immunol. 8: 74-83.
42. Martin, R., H. F. McFarland, and D. E. McFarlin. 1992. Immunological aspects of demyelinating diseases. Annu. Rev. Immunol. 10: 153-187.
43. Zamvil, S. S., and L. Steinman. 1990. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8: 579-621.
44. Kuchroo, V. K., A. C. Anderson, H., Waldner, M. Munder, E. Bettelli, and L. B. Nicholson. 2002. T cell response in experimental autoimmune encephalomyelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu. Rev. Immunol. 20: 101-123.
45. Lovett-Racke, A. E., A. E. Rocchini, J. Choy, S. C. Northrop, R. Z. Hussain, R. B. Ratts, D. Sikder, and M. K. Racke. 2004. Silencing T-bet defines a critical role in the differentiation of autoreactive T lymphocytes. Immunity 21: 719-731.
46. Mullen, A. C., F. A. High, A. S. Hutchins, H. W. Lee, A. V. Villarino, D. M. Livingston, A. L. Kung, N. Cereb, T. P. Yao, S. Y. Yang, and S. L. Reiner. 2001. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 292: 1907-1910.
47. Bettelli, E., and V. K. Kuchroo. 2005. IL-12- and IL-23-induced T helper cell subsets: birds of the same feather flock together. J. Exp. Med. 201: 169-171. (Pubitemid 40189424)
48. Mathur, A. N., H. C. Chang, D. G. Zisoulis, R. Kapur, M. L. Belladonna, G. S. Kansas, and M. H. Kaplan. 2006. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108: 1595-1601.
49. B receptors in the hippocampus. J. Neurophysiol. 90: 2690-2701. (Pubitemid 37266533)
50. A receptors mediate inhibition of T cell responses. J. Neuroimmunol. 96: 21-28. (Pubitemid 29179742)