Role of nuclear receptor NR4A2 in gastrointestinal inflammation and cancers

World Journal of Gastroenterology

Volumn 18, Issue 47, 2012, Pages 6865-6873

  Han, Yi Fang ^a   Cao, Guang Wen ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Gastrointestinal carcinoma; Immune cells; Inflammation; NR4A2; Signaling pathway

Indexed keywords

BETA CATENIN; CD133 ANTIGEN; COLLAGENASE 3; CORTICOTROPIN RELEASING FACTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN D1; CYCLOOXYGENASE 2; ENDOTHELIN 1; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; NONSTEROID ANTIINFLAMMATORY AGENT; NUCLEAR RECEPTOR NR4A3; NUCLEAR RECEPTOR NUR77; NUCLEAR RECEPTOR RELATED FACTOR 1; OSTEOPONTIN; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E2; RAS PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN;

APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; DIGESTIVE SYSTEM CANCER; DIGESTIVE SYSTEM INFLAMMATION; DISEASE COURSE; GENE MUTATION; HUMAN; MACROPHAGE; MULTIPLE SCLEROSIS; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; TH1 CELL;

EID: 84873896097     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v18.i47.6865     Document Type: Article

References (74)

1. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001; 357: 539-545
2. Ferrone C, Dranoff G. Dual roles for immunity in gastrointestinal cancers. J Clin Oncol 2010; 28: 4045-4051
3. Vannella L, Lahner E, Annibale B. Risk for gastric neoplasias in patients with chronic atrophic gastritis: a critical reappraisal. World J Gastroenterol 2012; 18: 1279-1285
4. Rizzo A, Pallone F, Monteleone G, Fantini MC. Intestinal inflammation and colorectal cancer: a double-edged sword? World J Gastroenterol 2011; 17: 3092-3100
5. Han YF, Zhao J, Ma LY, Yin JH, Chang WJ, Zhang HW, Cao GW. Factors predicting occurrence and prognosis of hepatitis-B-virus-related hepatocellular carcinoma. World J Gastroenterol 2011; 17: 4258-4270
6. Chang W, Ma L, Lin L, Gu L, Liu X, Cai H, Yu Y, Tan X, Zhai Y, Xu X, Zhang M, Wu L, Zhang H, Hou J, Wang H, Cao G. Identifcation of novel hub genes associated with liver metastasis of gastric cancer. Int J Cancer 2009; 125: 2844-2853
7. Li QX, Ke N, Sundaram R, Wong-Staal F. NR4A1, 2, 3--an orphan nuclear hormone receptor family involved in cell apoptosis and carcinogenesis. Histol Histopathol 2006; 21: 533-540
8. Winoto A, Littman DR. Nuclear hormone receptors in T lymphocytes. Cell 2002; 109 Suppl: S57-S66
9. Cheng LE, Chan FK, Cado D, Winoto A. Functional redundancy of the Nur77 and Nor-1 orphan steroid receptors in T-cell apoptosis. EMBO J 1997; 16: 1865-1875
10. Li H, Kolluri SK, Gu J, Dawson MI, Cao X, Hobbs PD, Lin B, Chen G, Lu J, Lin F, Xie Z, Fontana JA, Reed JC, Zhang X. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 2000; 289: 1159-1164
11. Ke N, Claassen G, Yu DH, Albers A, Fan W, Tan P, Grifman M, Hu X, Deffe K, Nguy V, Meyhack B, Brachat A, WongStaal F, Li QX. Nuclear hormone receptor NR4A2 is involved in cell transformation and apoptosis. Cancer Res 2004; 64: 8208-8212
12. Lin B, Kolluri SK, Lin F, Liu W, Han YH, Cao X, Dawson MI, Reed JC, Zhang XK. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/ TR3. Cell 2004; 116: 527-540
13. Sacchetti P, Carpentier R, Ségard P, Olivé-Cren C, Lefebvre P. Multiple signaling pathways regulate the transcriptional activity of the orphan nuclear receptor NURR1. Nucleic Acids Res 2006; 34: 5515-5527
14. Mullican SE, Zhang S, Konopleva M, Ruvolo V, Andreeff M, Milbrandt J, Conneely OM. Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat Med 2007; 13: 730-735
15. Ramirez-Herrick AM, Mullican SE, Sheehan AM, Conneely OM. Reduced NR4A gene dosage leads to mixed myelodysplastic/myeloproliferative neoplasms in mice. Blood 2011; 117: 2681-2690
16. Pei L, Waki H, Vaitheesvaran B, Wilpitz DC, Kurland IJ, Tontonoz P. NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat Med 2006; 12: 1048-1055
17. Chao LC, Bensinger SJ, Villanueva CJ, Wroblewski K, Tontonoz P. Inhibition of adipocyte differentiation by Nur77, Nurr1, and Nor1. Mol Endocrinol 2008; 22: 2596-2608
18. Volakakis N, Joodmardi E, Perlmann T. NR4A orphan nuclear receptors influence retinoic acid and docosahexaenoic acid signaling via up-regulation of fatty acid binding protein 5. Biochem Biophys Res Commun 2009; 390: 1186-1191
19. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, Cheroutre H. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007; 317: 256-260
20. Zetterström RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T. Dopamine neuron agenesis in Nurr1-defcient mice. Science 1997; 276: 248-250
21. Bensinger SJ, Tontonoz P. A Nurr1 pathway for neuroprotection. Cell 2009; 137: 26-28
22. Chen YH, Tsai MT, Shaw CK, Chen CH. Mutation analysis of the human NR4A2 gene, an essential gene for midbrain dopaminergic neurogenesis, in schizophrenic patients. Am J Med Genet 2001; 105: 753-757
23. Buervenich S, Carmine A, Arvidsson M, Xiang F, Zhang Z, Sydow O, Jönsson EG, Sedvall GC, Leonard S, Ross RG, Freedman R, Chowdari KV, Nimgaonkar VL, Perlmann T, Anvret M, Olson L. NURR1 mutations in cases of schizo-
24. Phrenia and manic-depressive disorder. Am J Med Genet 2000; 96: 808-813
25. Le WD, Xu P, Jankovic J, Jiang H, Appel SH, Smith RG, Vassilatis DK. Mutations in NR4A2 associated with familial Parkinson disease. Nat Genet 2003; 33: 85-89
26. Chen L, Zhang Q, Chang W, Du Y, Zhang H, Cao G. Viral and host inflammation-related factors that can predict the prognosis of hepatocellular carcinoma. Eur J Cancer 2012; 48: 1977-1987
27. Sekiya T, Kashiwagi I, Inoue N, Morita R, Hori S, Waldmann H, Rudensky AY, Ichinose H, Metzger D, Chambon P, Yoshimura A. The nuclear orphan receptor Nr4a2 induces Foxp3 and regulates differentiation of CD4+ T cells. Nat Commun 2011; 2: 269
28. Barish GD, Downes M, Alaynick WA, Yu RT, Ocampo CB, Bookout AL, Mangelsdorf DJ, Evans RM. A Nuclear Receptor Atlas: macrophage activation. Mol Endocrinol 2005; 19: 2466-2477
29. Pei L, Castrillo A, Chen M, Hoffmann A, Tontonoz P. Induction of NR4A orphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J Biol Chem 2005; 280: 29256-29262
30. Ralph JA, Ahmed AU, Santos LL, Clark AR, McMorrow J, Murphy EP, Morand EF. Identification of NURR1 as a mediator of MIF signaling during chronic arthritis: effects on glucocorticoid-induced MKP1. Am J Pathol 2010; 177: 2366-2378
31. Doi Y, Oki S, Ozawa T, Hohjoh H, Miyake S, Yamamura T. Orphan nuclear receptor NR4A2 expressed in T cells from multiple sclerosis mediates production of infammatory cytokines. Proc Natl Acad Sci USA 2008; 105: 8381-8386
32. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009; 137: 47-59
33. Volakakis N, Kadkhodaei B, Joodmardi E, Wallis K, Panman L, Silvaggi J, Spiegelman BM, Perlmann T. NR4A orphan nuclear receptors as mediators of CREB-dependent neuroprotection. Proc Natl Acad Sci USA 2010; 107: 12317-12322
34. Mix KS, McMahon K, McMorrow JP, Walkenhorst DE, Smyth AM, Petrella BL, Gogarty M, Fearon U, Veale D, Attur MG, Abramson SB, Murphy EP. Orphan nuclear receptor NR4A2 induces synoviocyte proliferation, invasion, and matrix metalloproteinase 13 transcription. Arthritis Rheum 2012; 64: 2126-2136
35. McEvoy AN, Murphy EA, Ponnio T, Conneely OM, Bresnihan B, FitzGerald O, Murphy EP. Activation of nuclear orphan receptor NURR1 transcription by NF-kappa B and cyclic adenosine 5'-monophosphate response element-binding protein in rheumatoid arthritis synovial tissue. J Immunol 2002; 168: 2979-2987
36. Aherne CM, McMorrow J, Kane D, FitzGerald O, Mix KS, Murphy EP. Identification of NR4A2 as a transcriptional activator of IL-8 expression in human infammatory arthritis. Mol Immunol 2009; 46: 3345-3357
37. Burrage PS, Mix KS, Brinckerhoff CE. Matrix metalloproteinases: role in arthritis. Front Biosci 2006; 11: 529-543
38. Mix KS, Attur MG, Al-Mussawir H, Abramson SB, Brinckerhoff CE, Murphy EP. Transcriptional repression of matrix metalloproteinase gene expression by the orphan nuclear receptor NURR1 in cartilage. J Biol Chem 2007; 282: 9492-9504
39. Ralph JA, Zocco D, Bresnihan B, Fitzgerald O, McEvoy AN, Murphy EP. A role for type 1alpha corticotropin-releasing hormone receptors in mediating local changes in chronically infamed tissue. Am J Pathol 2007; 170: 1121-1133
40. Puglisi MA, Barba M, Corbi M, Errico MF, Giorda E, Saulnier N, Boninsegna A, Piscaglia AC, Carsetti R, Cittadini A, Gasbarrini A, Sgambato A. Identification of Endothelin-1 and NR4A2 as CD133-regulated genes in colon cancer cells. J Pathol 2011; 225: 305-314
41. Li X, Tai HH. Activation of thromboxane A(2) receptors induces orphan nuclear receptor Nurr1 expression and stimulates cell proliferation in human lung cancer cells. Carcinogenesis 2009; 30: 1606-1613
42. Holla VR, Wu H, Shi Q, Menter DG, DuBois RN. Nuclear orphan receptor NR4A2 modulates fatty acid oxidation pathways in colorectal cancer. J Biol Chem 2011; 286: 30003-30009
43. Shadman M, Newcomb PA, Hampton JM, Wernli KJ, Trentham-Dietz A. Non-steroidal anti-inflammatory drugs and statins in relation to colorectal cancer risk. World J Gastroenterol 2009; 15: 2336-2339
44. Menter DG, Dubois RN. Prostaglandins in cancer cell adhesion, migration, and invasion. Int J Cell Biol 2012; 2012: 723419
45. Ji R, Sanchez CM, Chou CL, Chen XB, Woodward DF, Regan JW. Prostanoid EP1 receptors mediate up-regulation of the orphan nuclear receptor Nurr1 by cAMP-independent activation of protein kinase A, CREB and NF-κB. Br J Pharmacol 2012; 166: 1033-1046
46. Holla VR, Mann JR, Shi Q, DuBois RN. Prostaglandin E2 regulates the nuclear receptor NR4A2 in colorectal cancer. J Biol Chem 2006; 281: 2676-2682
47. Ji H, Zhang Y, Shen X, Gao F, Huang CY, Abad C, Busuttil RW, Waschek JA, Kupiec-Weglinski JW. Neuropeptide PACAP in mouse liver ischemia and reperfusion injury: immunomodulation via cAMP-PKA pathway. Hepatology 2012; Epub ahead of print
48. Palorini R, De Rasmo D, Gaviraghi M, Danna LS, Signorile A, Cirulli C, Chiaradonna F, Alberghina L, Papa S. Oncogenic K-ras expression is associated with derangement of the cAMP/PKA pathway and forskolin-reversible alterations of mitochondrial dynamics and respiration. Oncogene 2012; Epub ahead of print
49. Jones SE, Palmer TM. Protein kinase A-mediated phosphorylation of RhoA on serine 188 triggers the rapid induction of a neuroendocrine-like phenotype in prostate cancer epithelial cells. Cell Signal 2012; 24: 1504-1514
50. Li Y, Chen Y, Tao Y, Wang Y, Chen Y, Xu W. Fibronectin increases RhoA activity through inhibition of PKA in the human gastric cancer cell line SGC-7901. Mol Med Report 2011; 4: 65-69
51. Leone V, di Palma A, Ricchi P, Acquaviva F, Giannouli M, Di Prisco AM, Iuliano F, Acquaviva AM. PGE2 inhibits apoptosis in human adenocarcinoma Caco-2 cell line through Ras-PI3K association and cAMP-dependent kinase A activation. Am J Physiol Gastrointest Liver Physiol 2007; 293: G673-G681
52. Chan TA. Prostaglandins and the colon cancer connection. Trends Mol Med 2006; 12: 240-244
53. Kitagawa H, Ray WJ, Glantschnig H, Nantermet PV, Yu Y, Leu CT, Harada S, Kato S, Freedman LP. A regulatory circuit mediating convergence between Nurr1 transcriptional regulation and Wnt signaling. Mol Cell Biol 2007; 27: 7486-7496
54. Likui W, Hong W, Shuwen Z. Clinical significance of the unregulated osteopontin mRNA expression in human colorectal cancer. J Gastrointest Surg 2010; 14: 74-81
55. Lammi J, Huppunen J, Aarnisalo P. Regulation of the osteopontin gene by the orphan nuclear receptor NURR1 in osteoblasts. Mol Endocrinol 2004; 18: 1546-1557
56. Uede T. Osteopontin, intrinsic tissue regulator of intractable inflammatory diseases. Pathol Int 2011; 61: 265-280
57. Dai N, Bao Q, Lu A, Li J. Protein expression of osteopontin in tumor tissues is an independent prognostic indicator in gastric cancer. Oncology 2007; 72: 89-96
58. Zagani R, Hamzaoui N, Cacheux W, de Reyniès A, Terris B, Chaussade S, Romagnolo B, Perret C, Lamarque D. Cyclooxygenase-2 inhibitors down-regulate osteopontin and Nr4A2new therapeutic targets for colorectal cancers. Gastroenterology 2009; 137: 1358-66.e1-3
59. Zhao D, Desai S, Zeng H. VEGF stimulates PKD-mediated CREB-dependent orphan nuclear receptor Nurr1 expression: role in VEGF-induced angiogenesis. Int J Cancer 2011; 128: 2602-2612
60. Tayama M, Furuhata T, Inafuku Y, Okita K, Nishidate T, Mizuguchi T, Kimura Y, Hirata K. Vascular endothelial growth factor 165b expression in stromal cells and colorectal cancer. World J Gastroenterol 2011; 17: 4867-4874
61. Yin Y, Cao LY, Wu WQ, Li H, Jiang Y, Zhang HF. Blocking effects of siRNA on VEGF expression in human colorectal cancer cells. World J Gastroenterol 2010; 16: 1086-1092
62. Kamiyama T, Takahashi M, Nakanishi K, Yokoo H, Kamachi H, Kobayashi N, Ozaki M, Todo S. α-fetoprotein, vascular endothelial growth factor receptor-1 and early recurrence of hepatoma. World J Gastroenterol 2012; 18: 340-348
63. Tang H, Wang J, Bai F, Zhai H, Gao J, Hong L, Xie H, Zhang F, Lan M, Yao W, Liu J, Wu K, Fan D. Positive correlation of osteopontin, cyclooxygenase-2 and vascular endothelial growth factor in gastric cancer. Cancer Invest 2008; 26: 60-67
64. Coghill AE, Newcomb PA, Poole EM, Hutter CM, Makar KW, Duggan D, Potter JD, Ulrich CM. Genetic variation in inflammatory pathways is related to colorectal cancer survival. Clin Cancer Res 2011; 17: 7139-7147
65. Cheng HH, Tseng GY, Yang HB, Wang HJ, Lin HJ, Wang WC. Increased numbers of Foxp3-positive regulatory T cells in gastritis, peptic ulcer and gastric adenocarcinoma. World J Gastroenterol 2012; 18: 34-43
66. Liao G, Detre C, Berger SB, Engel P, de Waal Malefyt R, Herzog RW, Bhan AK, Terhorst C. Glucocorticoid-induced tumor necrosis factor receptor family-related protein regulates CD4(+)T cell-mediated colitis in mice. Gastroenterology 2012; 142: 582-591.e8
67. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR, Sargent DJ. Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 2009; 137: 1270-1279
68. Deng L, Zhang H, Luan Y, Zhang J, Xing Q, Dong S, Wu X, Liu M, Wang S. Accumulation of foxp3+ T regulatory cells in draining lymph nodes correlates with disease progression and immune suppression in colorectal cancer patients. Clin Cancer Res 2010; 16: 4105-4112
69. Chaput N, Louaf S, Bardier A, Charlotte F, Vaillant JC, Ménégaux F, Rosenzwajg M, Lemoine F, Klatzmann D, Taieb J. Identifcation of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue. Gut 2009; 58: 520-529
70. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pagès F, Galon J. Clinical impact of different classes of infltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res 2011; 71: 1263-1271
71. Maruyama T, Kono K, Mizukami Y, Kawaguchi Y, Mimura K, Watanabe M, Izawa S, Fujii H. Distribution of Th17 cells and FoxP3(+) regulatory T cells in tumor-infiltrating lymphocytes, tumor-draining lymph nodes and peripheral blood lymphocytes in patients with gastric cancer. Cancer Sci 2010; 101: 1947-1954
72. Yuan XL, Chen L, Li MX, Dong P, Xue J, Wang J, Zhang TT, Wang XA, Zhang FM, Ge HL, Shen LS, Xu D. Elevated expression of Foxp3 in tumor-infltrating Treg cells suppresses T-cell proliferation and contributes to gastric cancer progression in a COX-2-dependent manner. Clin Immunol 2010; 134: 277-288
73. Inamoto T, Papineni S, Chintharlapalli S, Cho SD, Safe S, Kamat AM. 1,1-Bis(3'-indolyl)-1-(p-chlorophenyl)methane activates the orphan nuclear receptor Nurr1 and inhibits bladder cancer growth. Mol Cancer Ther 2008; 7: 3825-3833
74. Inamoto T, Czerniak BA, Dinney CP, Kamat AM. Cytoplasmic mislocalization of the orphan nuclear receptor Nurr1 is a prognostic factor in bladder cancer. Cancer 2010; 116: 340-346