The cystine/glutamate antiporter regulates dendritic cell differentiation and antigen presentation

Journal of Immunology

Volumn 185, Issue 6, 2010, Pages 3217-3226

  D'Angelo, June A ^a   Dehlink, Eleonora ^d   Platzer, Barbara ^d   Dwyer, Peter ^d   Circu, Magdalena L ^c   Garay, Jone ^a   Aw, Tak Yee ^c   Fiebiger, Edda ^d   Dickinson, Bonny L ^a,b  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL   (United States)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTER; CYSTINE; GLUTAMIC ACID; GLUTATHIONE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CROSS PRESENTATION; DENDRITIC CELL; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; MONOCYTE MACROPHAGE PRECURSOR CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; T LYMPHOCYTE;

AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIGEN PRESENTATION; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; CELLS, CULTURED; CROSS-PRIMING; CYSTINE; DENDRITIC CELLS; GLUTAMIC ACID; GLUTATHIONE; HOMEOSTASIS; HUMANS; INTRACELLULAR FLUID; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OVALBUMIN;

EID: 78649899334     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001199     Document Type: Article

References (64)

1. Meister, A., and M. E. Anderson. 1983. Glutathione. Annu. Rev. Biochem. 52: 711-760.
2. Reed, D. J. 1986. Regulation of reductive processes by glutathione. Biochem. Pharmacol. 35: 7-13.
3. Jones, D. P. 2002. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol. 348: 93-112.
4. Das, K. C., and C. W. White. 2002. Redox systems of the cell: possible links and implications. Proc. Natl. Acad. Sci. USA 99: 9617-9618.
5. Klebanoff, S. J. 1980. Oxygen metabolism and the toxic properties of phagocytes. Ann. Intern. Med. 93: 480-489.
6. Cook, J. A., D. Gius, D. A. Wink, M. C. Krishna, A. Russo, and J. B. Mitchell. 2004. Oxidative stress, redox, and the tumor microenvironment. Semin. Radiat. Oncol. 14: 259-266.
7. De la Fuente, M., A. Hernanz, and M. C. Vallejo. 2005. The immune system in the oxidative stress conditions of aging and hypertension: favorable effects of antioxidants and physical exercise. Antioxid. Redox Signal. 7: 1356-1366.
8. Richie, J. P., Jr. 1992. The role of glutathione in aging and cancer. Exp. Gerontol. 27: 615-626.
9. Hernanz, A., E. Fernández-Vivancos, C. Montiel, J. J. Vazquez, and F. Arnalich. 2000. Changes in the intracellular homocysteine and glutathione content associated with aging. Life Sci. 67: 1317-1324.
10. Hernanz, A., E. Fernández-Vivancos, R. M. Salazar, and F. Arnalich. 2000. Homocysteine and other thiol compounds in ageing. Biofactors 11: 47-49.
11. Dröge, W. 2002. Aging-related changes in the thiol/disulfide redox state: implications for the use of thiol antioxidants. Exp. Gerontol. 37: 1333-1345.
12. Bannai, S., and E. Kitamura. 1980. Transport interaction of L-cystine and L-glutamate in human diploid fibroblasts in culture. J. Biol. Chem. 255: 2372-2376.
13. Bannai, S., and N. Tateishi. 1986. Role of membrane transport in metabolism and function of glutathione in mammals. J. Membr. Biol. 89: 1-8.
14. Ishii, T., Y. Sugita, and S. Bannai. 1987. Regulation of glutathione levels in mouse spleen lymphocytes by transport of cysteine. J. Cell. Physiol. 133: 330-336.
15. Bannai, S., and E. Kitamura. 1981. Role of proton dissociation in the transport of cystine and glutamate in human diploid fibroblasts in culture. J. Biol. Chem. 256: 5770-5772.
16. Bannai, S., and T. Ishii. 1982. Transport of cystine and cysteine and cell growth in cultured human diploid fibroblasts: effect of glutamate and homocysteate. J. Cell. Physiol. 112: 265-272.
17. Christensen, H. N. 1990. Role of amino acid transport and countertransport in nutrition and metabolism. Physiol. Rev. 70: 43-77.
18. Sato, H., M. Tamba, T. Ishii, and S. Bannai. 1999. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J. Biol. Chem. 274: 11455-11458.
19. Verrey, F., C. Meier, G. Rossier, and L. C. Kühn. 2000. Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflugers Arch. 440: 503-512.
20. Bridges, C. C., R. Kekuda, H. Wang, P. D. Prasad, P. Mehta, W. Huang, S. B. Smith, and V. Ganapathy. 2001. Structure, function, and regulation of human cystine/glutamate transporter in retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 42: 47-54.
21. Bridges, R. J., and C. S. Esslinger. 2005. The excitatory amino acid transporters: pharmacological insights on substrate and inhibitor specificity of the EAAT subtypes. Pharmacol. Ther. 107: 271-285.
22. Sakakura, Y., H. Sato, A. Shiiya, M. Tamba, J. Sagara, M. Matsuda, N. Okamura, N. Makino, and S. Bannai. 2007. Expression and function of cystine/glutamate transporter in neutrophils. J. Leukoc. Biol. 81: 974-982.
23. Watanabe, H., and S. Bannai. 1987. Induction of cystine transport activity in mouse peritoneal macrophages. J. Exp. Med. 165: 628-640.
24. Eck, H. P., and W. Dröge. 1989. Influence of the extracellular glutamate concentration on the intracellular cyst(e)ine concentration in macrophages and on the capacity to release cysteine. Biol. Chem. Hoppe Seyler 370: 109-113.
25. Bevan, M. J. 1976. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143: 1283-1288.
26. Brossart, P., and M. J. Bevan. 1997. Presentation of exogenous protein antigens on major histocompatibility complex class I molecules by dendritic cells: pathway of presentation and regulation by cytokines. Blood 90: 1594-1599.
27. Brossart, P., A. W. Goldrath, E. A. Butz, S. Martin, and M. J. Bevan. 1997. Virus-mediated delivery of antigenic epitopes into dendritic cells as a means to induce CTL. J. Immunol. 158: 3270-3276.
28. Rodriguez, A., A. Regnault, M. Kleijmeer, P. Ricciardi-Castagnoli, and S. Amigorena. 1999. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1: 362-368.
29. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
30. Mellman, I., and R. M. Steinman. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106: 255-258.
31. Sallusto, F., P. Schaerli, P. Loetscher, C. Schaniel, D. Lenig, C. R. Mackay, S. Qin, and A. Lanzavecchia. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28: 2760-2769.
32. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779.
33. Steinman, R. M., D. Hawiger, K. Liu, L. Bonifaz, D. Bonnyay, K. Mahnke, T. Iyoda, J. Ravetch, M. Dhodapkar, K. Inaba, and M. Nussenzweig. 2003. Dendritic cell function in vivo during the steady state: a role in peripheral tolerance. Ann. N. Y. Acad. Sci. 987: 15-25.
34. Dhodapkar, M. V., R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj. 2001. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193: 233-238.
35. Ballatori, N., S. M. Krance, S. Notenboom, S. Shi, K. Tieu, and C. L. Hammond. 2009. Glutathione dysregulation and the etiology and progression of human diseases. Biol. Chem. 390: 191-214.
36. Reed, D. J., J. R. Babson, P. W. Beatty, A. E. Brodie, W. W. Ellis, and D. W. Potter. 1980. High-performance liquid chromatography analysis of nanomole levels of glutathione, glutathione disulfide, and related thiols and disulfides. Anal. Biochem. 106: 55-62.
37. Circu, M. L., C. Rodriguez, R. Maloney, M. P. Moyer, and T. Y. Aw. 2008. Contribution of mitochondrial GSH transport to matrix GSH status and colonic epithelial cell apoptosis. Free Radic. Biol. Med. 44: 768-778.
38. Circu, M. L., S. Stringer, C. A. Rhoads, M. P. Moyer, and T. Y. Aw. 2009. The role of GSH efflux in staurosporine-induced apoptosis in colonic epithelial cells. Biochem. Pharmacol. 77: 76-85.
39. Geiss, G. K., R. E. Bumgarner, B. Birditt, T. Dahl, N. Dowidar, D. L. Dunaway, H. P. Fell, S. Ferree, R. D. George, T. Grogan, et al. 2008. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26: 317-325.
40. +-dependent high-affinity glutamate transport in macrophages. J. Immunol. 164: 5430-5438.
41. Pacheco, R., H. Oliva, J. M. Martinez-Navío, N. Climent, F. Ciruela, J. M. Gatell, T. Gallart, J. Mallol, C. Lluis, and R. Franco. 2006. Glutamate released by dendritic cells as a novel modulator of T cell activation. J. Immunol. 177: 6695-6704.
42. Patel, S. A., B. A. Warren, J. F. Rhoderick, and R. J. Bridges. 2004. Differentiation of substrate and non-substrate inhibitors of transport system xc(-): an obligate exchanger of L-glutamate and L-cystine. Neuropharmacology 46: 273-284.
43. Bannai, S. 1986. Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J. Biol. Chem. 261: 2256-2263.
44. Shimamoto, K., B. Lebrun, Y. Yasuda-Kamatani, M. Sakaitani, Y. Shigeri, N. Yumoto, and T. Nakajima. 1998. DL-threo-β-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol. Pharmacol. 53: 195-201.
45. Gmünder, H., H. P. Eck, B. Benninghoff, S. Roth, and W. Dröge. 1990. Macrophages regulate intracellular glutathione levels of lymphocytes: evidence for an immunoregulatory role of cysteine. Cell. Immunol. 129: 32-46.
46. Kanner, S. B., T. J. Kavanagh, A. Grossmann, S. L. Hu, J. B. Bolen, P. S. Rabinovitch, and J. A. Ledbetter. 1992. Sulfhydryl oxidation down-regulates T-cell signaling and inhibits tyrosine phosphorylation of phospholipase Cγ1. Proc. Natl. Acad. Sci. USA 89: 300-304.
47. Sido, B., J. Braunstein, R. Breitkreutz, C. Herfarth, and S. C. Meuer. 2000. Thiol-mediated redox regulation of intestinal lamina propria T lymphocytes. J. Exp. Med. 192: 907-912.
48. Yan, Z., S. K. Garg, J. Kipnis, and R. Banerjee. 2009. Extracellular redox modulation by regulatory T cells. Nat. Chem. Biol. 5: 721-723.
49. Sanlioglu, S., C. M. Williams, L. Samavati, N. S. Butler, G. Wang, P. B. McCray, Jr., T. C. Ritchie, G. W. Hunninghake, E. Zandi, and J. F. Engelhardt. 2001. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-α secretion through IKK regulation of NF-κB. J. Biol. Chem. 276: 30188-30198.
50. Carta, S., P. Castellani, L. Delfino, S. Tassi, R. Venè, and A. Rubartelli. 2009. DAMPs and inflammatory processes: the role of redox in the different outcomes. J. Leukoc. Biol. 86: 549-555.
51. Castellani, P., G. Angelini, L. Delfino, A. Matucci, and A. Rubartelli. 2008. The thiol redox state of lymphoid organs is modified by immunization: role of different immune cell populations. Eur. J. Immunol. 38: 2419-2425.
52. Masciarelli, S., and R. Sitia. 2008. Building and operating an antibody factory: redox control during B to plasma cell terminal differentiation. Biochim. Biophys. Acta 1783: 578-588.
53. Geijtenbeek, T. B., R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, G. J. Adema, Y. van Kooyk, and C. G. Figdor. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
54. León, B., and C. Ardavín. 2008. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 86: 320-324.
55. León, B., M. López-Bravo, and C. Ardavín. 2007. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26: 519-531.
56. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179: 1109-1118.
57. Kuppner, M. C., A. Scharner, V. Milani, C. Von Hesler, K. E. Tschop, O. Heinz, and R. D. Issels. 2003. Ifosfamide impairs the allostimulatory capacity of human dendritic cells by intracellular glutathione depletion. Blood 102: 3668-3674.
58. Yamada, H., T. Arai, N. Endo, K. Yamashita, K. Fukuda, M. Sasada, and T. Uchiyama. 2006. LPS-induced ROS generation and changes in glutathione level and their relation to thematuration of human monocyte-derived dendritic cells. Life Sci. 78: 926-933.
59. Peterson, J. D., L. A. Herzenberg, K. Vasquez, and C. Waltenbaugh. 1998. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc. Natl. Acad. Sci. USA 95: 3071-3076.
60. Rimaniol, A. C., P. Mialocq, P. Clayette, D. Dormont, and G. Gras. 2001. Role of glutamate transporters in the regulation of glutathione levels in human macrophages. Am. J. Physiol. Cell Physiol. 281: C1964-C1970.
61. James, S. J., S. Rose, S. Melnyk, S. Jernigan, S. Blossom, O. Pavliv, and D. W. Gaylor. 2009. Cellular and mitochondrial glutathione redox imbalance in lymphoblastoid cells derived from children with autism. FASEB J. 23: 2374-2383.
62. Franco, R., O. J. Schoneveld, A. Pappa, and M. I. Panayiotidis. 2007. The central role of glutathione in the pathophysiology of human diseases. Arch. Physiol. Biochem. 113: 234-258.
63. Arnalich, F., A. Hernanz, D. López-Maderuelo, M. De la Fuente, F. M. Arnalich, E. Andres-Mateos, C. Fernández-Capitán, and C. Montiel. 2001. Intracellular glutathione deficiency is associated with enhanced nuclear factor-κB activation in older non-insulin dependent diabetic patients. Free Radic. Res. 35: 873-884.
64. Eck, H. P., H. Gmünder, M. Hartmann, D. Petzoldt, V. Daniel, and W. Dröge. 1989. Low concentrations of acid-soluble thiol (cysteine) in the blood plasma of HIV-1-infected patients. Biol. Chem. Hoppe Seyler 370: 101-108.