RAGE expression in human T cells: A link between environmental factors and adaptive immune responses

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Akirav, Eitan M ^a   Preston Hurlburt, Paula ^a   Garyu, Justin ^a   Henegariu, Octavian ^a   Clynes, Raphael ^b   Schmidt, Ann Marie ^c   Herold, Kevan C ^a  

^a YALE UNIVERSITY   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; GLUCOSE; HEMOGLOBIN A1C; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; LIGAND; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MOK PROTEIN, HUMAN; TUMOR ANTIGEN;

ADAPTIVE IMMUNITY; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETES CONTROL; DIABETES MELLITUS; ENDOSOME; ENVIRONMENTAL FACTOR; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION; ANTIGEN PRESENTING CELL; BLOOD; BYSTANDER EFFECT; CELL STRAIN HEK293; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LEUKEMIA CELL LINE; LYMPHOCYTE ACTIVATION; METABOLISM; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANTIGEN-PRESENTING CELLS; ANTIGENS, NEOPLASM; BYSTANDER EFFECT; DIABETES MELLITUS; ENDOSOMES; GENE EXPRESSION REGULATION; GLUCOSE; HEK293 CELLS; HUMANS; INTERLEUKIN-17; JURKAT CELLS; LIGANDS; LYMPHOCYTE ACTIVATION; MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84859590072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034698     Document Type: Article

References (71)

1. Nakayama T, Yamashita M, (2010) The TCR-mediated signaling pathways that control the direction of helper T cell differentiation. Semin Immunol 22: 303-309.
2. Schneider R, (2010) T cells with commitment issues. Sci Signal 3: jc3.
3. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, et al. (2002) The CD28 signaling pathway regulates glucose metabolism. Immunity 16: 769-777.
4. Frauwirth KA, Thompson CB, (2004) Regulation of T lymphocyte metabolism. J Immunol 172: 4661-4665.
5. Beverly B, Kang SM, Lenardo MJ, Schwartz RH, (1992) Reversal of in vitro T cell clonal anergy by IL-2 stimulation. Int Immunol 4: 661-671.
6. Caldwell CC, Kojima H, Lukashev D, Armstrong J, Farber M, et al. (2001) Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol 167: 6140-6149.
7. The Diabetes Control and Complications Trial Research Group (1998) Effect of intensive therapy on residual beta-cell function in patients with Type 1 diabetes in the Diabetes Control and Complications Trial. Annals of Internal Medicine 128: 517-523.
8. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, et al. (1999) RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97: 889-901.
9. Schmidt AM, Yan SD, Yan SF, Stern DM, (2000) The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 1498: 99-111.
10. Taguchi A, Blood DC, Del Toro G, Canet A, Lee DC, et al. (2000) Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 405: 354-360.
11. Schmidt AM, Yan SD, Yan SF, Stern DM, (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108: 949-955.
12. Feng L, Matsumoto C, Schwartz A, Schmidt AM, Stern DM, et al. (2005) Chronic vascular inflammation in patients with type 2 diabetes: endothelial biopsy and RT-PCR analysis. Diabetes Care 28: 379-384.
13. Goldin A, Beckman JA, Schmidt AM, Creager MA, (2006) Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114: 597-605.
14. Greten J, Kreis I, Wiesel K, Stier E, Schmidt AM, et al. (1996) Receptors for advance glycation end-products (AGE)- expression by endothelial cells in non-diabetic uraemic patients. Nephrol Dial Transplant 11: 786-790.
15. Kim W, Hudson BI, Moser B, Guo J, Rong LL, et al. (2005) Receptor for advanced glycation end products and its ligands: a journey from the complications of diabetes to its pathogenesis. Ann N Y Acad Sci 1043: 553-561.
16. Rong LL, Gooch C, Szabolcs M, Herold KC, Lalla E, et al. (2005) RAGE: a journey from the complications of diabetes to disorders of the nervous system- striking a fine balance between injury and repair. Restor Neurol Neurosci 23: 355-365.
17. Schmidt AM, Stern DM, (2000) RAGE: a new target for the prevention and treatment of the vascular and inflammatory complications of diabetes. Trends Endocrinol Metab 11: 368-375.
18. Hou FF, Ren H, Owen WF Jr, Guo ZJ, Chen PY, et al. (2004) Enhanced expression of receptor for advanced glycation end products in chronic kidney disease. J Am Soc Nephrol 15: 1889-1896.
19. Hudson BI, Carter AM, Harja E, Kalea AZ, Arriero M, et al. (2008) Identification, classification, and expression of RAGE gene splice variants. Faseb J 22: 1572-1580.
20. Kalea AZ, Reiniger N, Yang H, Arriero M, Schmidt AM, et al. (2009) Alternative splicing of the murine receptor for advanced glycation end-products (RAGE) gene. FASEB J 23: 1766-1774.
21. Kalea AZ, See F, Harja E, Arriero M, Schmidt AM, et al. (2010) Alternatively spliced RAGEv1 inhibits tumorigenesis through suppression of JNK signaling. Cancer Res 70: 5628-5638.
22. Basta G, Lazzerini G, Del Turco S, Ratto GM, Schmidt AM, et al. (2005) At least 2 distinct pathways generating reactive oxygen species mediate vascular cell adhesion molecule-1 induction by advanced glycation end products. Arterioscler Thromb Vasc Biol 25: 1401-1407.
23. Galkina E, Ley K, (2009) Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol 27: 165-197.
24. Ge J, Jia Q, Liang C, Luo Y, Huang D, et al. (2005) Advanced glycosylation end products might promote atherosclerosis through inducing the immune maturation of dendritic cells. Arterioscler Thromb Vasc Biol 25: 2157-2163.
25. Harja E, Bu DX, Hudson BI, Chang JS, Shen X, et al. (2008) Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J Clin Invest 118: 183-194.
26. Li W, Sama AE, Wang H, (2006) Role of HMGB1 in cardiovascular diseases. Curr Opin Pharmacol 6: 130-135.
27. Pollreisz A, Hudson BI, Chang JS, Qu W, Cheng B, et al. (2010) Receptor for advanced glycation endproducts mediates pro-atherogenic responses to periodontal infection in vascular endothelial cells. Atherosclerosis.
28. Schmidt AM, Yan SD, Wautier JL, Stern D, (1999) Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res 84: 489-497.
29. Xanthis A, Hatzitolios A, Fidani S, Befani C, Giannakoulas G, et al. (2009) Receptor of advanced glycation end products (RAGE) positively regulates CD36 expression and reactive oxygen species production in human monocytes in diabetes. Angiology 60: 772-779.
30. Yan SF, Ramasamy R, Bucciarelli LG, Wendt T, Lee LK, et al. (2004) RAGE and its ligands: a lasting memory in diabetic complications? Diab Vasc Dis Res 1: 10-20.
31. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ, (2010) HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol 28: 367-388.
32. Yan SF, Ramasamy R, Schmidt AM, (2010) The RAGE axis: a fundamental mechanism signaling danger to the vulnerable vasculature. Circ Res 106: 842-853.
33. Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, et al. (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96: 1395-1403.
34. Schmidt AM, Hori O, Cao R, Yan SD, Brett J, et al. (1996) RAGE: a novel cellular receptor for advanced glycation end products. Diabetes 45 (Suppl 3): S77-80.
35. Wautier JL, Zoukourian C, Chappey O, Wautier MP, Guillausseau PJ, et al. (1996) Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J Clin Invest 97: 238-243.
36. Yan SD, Chen X, Fu J, Chen M, Zhu H, et al. (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382: 685-691.
37. Zoukourian C, Wautier MP, Chappey O, Dosquet C, Rohban T, et al. (1996) Endothelial cell dysfunction secondary to the adhesion of diabetic erythrocytes. Modulation by iloprost. Int Angiol 15: 195-200.
38. Du Yan S, Zhu H, Fu J, Yan SF, Roher A, et al. (1997) Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: a proinflammatory pathway in Alzheimer disease. Proc Natl Acad Sci U S A 94: 5296-5301.
39. Schmidt AM, Stern D, (2000) Atherosclerosis and diabetes: the RAGE connection. Curr Atheroscler Rep 2: 430-436.
40. Yan SD, Zhu H, Zhu A, Golabek A, Du H, et al. (2000) Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med 6: 643-651.
41. Hofmann MA, Drury S, Hudson BI, Gleason MR, Qu W, et al. (2002) RAGE and arthritis: the G82S polymorphism amplifies the inflammatory response. Genes Immun 3: 123-135.
42. Yan SF, Ramasamy R, Naka Y, Schmidt AM, (2003) Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 93: 1159-1169.
43. Shang L, Ananthakrishnan R, Li Q, Quadri N, Abdillahi M, et al. (2010) RAGE modulates hypoxia/reoxygenation injury in adult murine cardiomyocytes via JNK and GSK-3beta signaling pathways. PLoS One 5: e10092.
44. Hofmann MA, Yang Q, Harja E, Kedia P, Gregersen PK, et al. (2005) The RAGE Gly82Ser polymorphism is not associated with cardiovascular disease in the Framingham offspring study. Atherosclerosis 182: 301-305.
45. Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, et al. (2008) Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J Biol Chem 283: 34457-34468.
46. Arumugam T, Simeone DM, Schmidt AM, Logsdon CD, (2004) S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem 279: 5059-5065.
47. Fang F, Lue LF, Yan S, Xu H, Luddy JS, et al. (2010) RAGE-dependent signaling in microglia contributes to neuroinflammation, Abeta accumulation, and impaired learning/memory in a mouse model of Alzheimer's disease. FASEB J 24: 1043-1055.
48. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, et al. (1999) N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem 274: 31740-31749.
49. Reddy MA, Li SL, Sahar S, Kim YS, Xu ZG, et al. (2006) Key role of Src kinase in S100B-induced activation of the receptor for advanced glycation end products in vascular smooth muscle cells. J Biol Chem 281: 13685-13693.
50. Yeh CH, Sturgis L, Haidacher J, Zhang XN, Sherwood SJ, et al. (2001) Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 50: 1495-1504.
51. Ohashi K, Takahashi HK, Mori S, Liu K, Wake H, et al. (2010) Advanced glycation end products enhance monocyte activation during human mixed lymphocyte reaction. Clin Immunol 134: 345-353.
52. Wang Y, Wang H, Piper MG, McMaken S, Mo X, et al. (2010) sRAGE induces human monocyte survival and differentiation. J Immunol 185: 1822-1835.
53. Dumitriu IE, Baruah P, Valentinis B, Voll RE, Herrmann M, et al. (2005) Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 174: 7506-7515.
54. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, et al. (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8: 487-496.
55. Urbonaviciute V, Furnrohr BG, Meister S, Munoz L, Heyder P, et al. (2008) Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 205: 3007-3018.
56. Lin L, (2006) RAGE on the Toll Road? Cell Mol Immunol 3: 351-358.
57. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, et al. (2006) High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 290: C917-924.
58. Chen Y, Akirav EM, Chen W, Henegariu O, Moser B, et al. (2008) RAGE ligation affects T cell activation and controls T cell differentiation. J Immunol 181: 4272-4278.
59. Chen Y, Yan SS, Colgan J, Zhang HP, Luban J, et al. (2004) Blockade of late stages of autoimmune diabetes by inhibition of the receptor for advanced glycation end products. J Immunol 173: 1399-1405.
60. Matsuoka N, Itoh T, Watarai H, Sekine-Kondo E, Nagata N, et al. (2010) High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J Clin Invest 120: 735-743.
61. Moser B, Desai DD, Downie MP, Chen Y, Yan SF, et al. (2007) Receptor for advanced glycation end products expression on T cells contributes to antigen-specific cellular expansion in vivo. J Immunol 179: 8051-8058.
62. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, et al. (2004) Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279: 7370-7377.
63. Qin YH, Dai SM, Tang GS, Zhang J, Ren D, et al. (2009) HMGB1 enhances the proinflammatory activity of lipopolysaccharide by promoting the phosphorylation of MAPK p38 through receptor for advanced glycation end products. J Immunol 183: 6244-6250.
64. Moser B, Hudson BI, Schmidt AM, (2005) Soluble RAGE: a hot new biomarker for the hot joint? Arthritis Res Ther 7: 142-144.
65. Liliensiek B, Weigand MA, Bierhaus A, Nicklas W, Kasper M, et al. (2004) Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 113: 1641-1650.
66. Dettoraki A, Gil AP, Spiliotis BE, (2009) Association between serum levels of the soluble receptor (sRAGE) for advanced glycation endproducts (AGEs) and their receptor (RAGE) in peripheral blood mononuclear cells of children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 22: 895-904.
67. Fuentes MK, Nigavekar SS, Arumugam T, Logsdon CD, Schmidt AM, et al. (2007) RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis Colon Rectum 50: 1230-1240.
68. Nakamura K, Yamagishi S, Adachi H, Matsui T, Kurita-Nakamura Y, et al. (2008) Circulating advanced glycation end products (AGEs) and soluble form of receptor for AGEs (sRAGE) are independent determinants of serum monocyte chemoattractant protein-1 (MCP-1) levels in patients with type 2 diabetes. Diabetes Metab Res Rev 24: 109-114.
69. The Diabetes Control and Complications Trial Research Group (1998) Effect of intensive therapy on residual beta-cell function in patients with type 1 diabetes in the diabetes control and complications trial. A randomized, controlled trial. Ann Intern Med 128: 517-523.
70. Sosenko JM, Palmer JP, Rafkin-Mervis L, Krischer JP, Cuthbertson D, et al. (2008) Glucose and C-peptide changes in the perionset period of type 1 diabetes in the Diabetes Prevention Trial-Type 1. Diabetes Care 31: 2188-2192.
71. Obermaier B, Dauer M, Herten J, Schad K, Endres S, et al. (2003) Development of a new protocol for 2-day generation of mature dendritic cells from human monocytes. Biol Proced Online 5: 197-203.