The interplay between retinoic acid receptor-related orphan receptors and human diseases

Journal of Receptors and Signal Transduction

Volumn 32, Issue 4, 2012, Pages 181-189

  Ranhotra, Harmit S ^a  

^a St Edmunds College   (India)

Author keywords

Autoimmunity; Inflammation; Metabolic syndrome; Orphan nuclear receptors

Indexed keywords

CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME P450; FARNESOID X RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; ISOPROTEIN; LIVER X RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PREGNANE X RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR BETA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TUMOR NECROSIS FACTOR ALPHA; VITAMIN D RECEPTOR; XENOBIOTIC AGENT;

ACETYLATION; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; AUTOIMMUNE DISEASE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CYTOKINE PRODUCTION; DNA BINDING MOTIF; DOWN REGULATION; DRUG METABOLISM; GENE CONTROL; GENE SILENCING; IMMUNITY; INFLAMMATION; INTRACELLULAR SIGNALING; METABOLIC DISORDER; MOUSE; NEOPLASM; NONHUMAN; OXIDATIVE STRESS; PNEUMONIA; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; STOMACH CANCER; SUMOYLATION; UBIQUITINATION;

ANIMALS; DISEASE; GENE EXPRESSION REGULATION; HUMANS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1; OXIDATIVE STRESS; RECEPTORS, RETINOIC ACID; XENOBIOTICS;

ANIMALIA; MUS;

EID: 84864026646     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.3109/10799893.2012.692120     Document Type: Review

References (90)

1. Benoit G, Cooney A, Giguere v, Ingraham H, Lazar M, Muscat G, Perlmann T, Renaud JP, Schwabe J, Sladek F, Tsai MJ, Laudet V. International Union of Pharmacology. LXvI. Orphan nuclear receptors. Pharmacol Rev 2006, 58, 798-836.
2. Jetten AM. Retinoid-Related orphan receptors (RORs): Critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl Recept Signal 2009, 7, e003.
3. Sun Z, Unutmaz D, Zou YR, Sunshine MJ, Pierani A, Brenner- Morton S, Mebius RE, Littman DR. Requirement for RORγ in thymocyte survival and lymphoid organ development. Science 2000, 288, 2369-2373.
4. villey I, de Chasseval R, de villartay JP. RORγT, a thymus-Specific isoform of the orphan nuclear receptor RORγ/TOR, is up-Regulated by signaling through the pre-T cell receptor and binds to the TEA promoter. Eur J Immunol 1999, 29, 4072-4080.
5. Wada T, Kang HS, Jetten AM, Xie W. The emerging role of nuclear receptor RORα and its crosstalk with LXR in xeno- and endobiotic gene regulation. Exp Biol Med (Maywood) 2008, 233, 1191-1201.
6. Kang HS, Angers M, Beak JY, Wu X, Gimble JM, Wada T, Xie W, Collins JB, Grissom SF, Jetten AM. Gene expression profiling reveals a regulatory role for ROR α and ROR γ in phase I and phase II metabolism. Physiol Genomics 2007, 31, 281-294.
7. Lau P, Fitzsimmons RL, Raichur S, Wang SC, Lechtken A, Muscat GE. The orphan nuclear receptor, RORα, regulates gene expression that controls lipid metabolism: Staggerer (SG/SG) mice are resistant to diet-Induced obesity. J Biol Chem 2008, 283, 18411-18421.
8. Lau P, Bailey P, Dowhan DH, Muscat GE. Exogenous expression of a dominant negative RORα1 vector in muscle cells impairs differentiation: RORα1 directly interacts with p300 and myoD. Nucleic Acids Res 1999, 27, 411-420.
9. Nakagawa S, Watanabe M, Isobe T, Kondo H, Inoue Y. Cytological compartmentalization in the staggerer cerebellum, as revealed by calbindin immunohistochemistry for Purkinje cells. J Comp Neurol 1998, 395, 112-120.
10. Nakagawa Y, O'Leary DD. Dynamic patterned expression of orphan nuclear receptor genes RORα and RORβ in developing mouse forebrain. Dev Neurosci 2003, 25, 234-244.
11. Fujieda H, Bremner R, Mears AJ, Sasaki H. Retinoic acid receptorrelated orphan receptor α regulates a subset of cone genes during mouse retinal development. J Neurochem 2009, 108, 91-101.
12. Meyer T, Kneissel M, Mariani J, Fournier B. In vitro and in vivo evidence for orphan nuclear receptor RORα function in bone metabolism. Proc Natl Acad Sci USA 2000, 97, 9197-9202.
13. Gold DA, Gent PM, Hamilton BA. ROR α in genetic control of cerebellum development: 50 staggering years. Brain Res 2007, 1140, 19-25.
14. Dzhagalov I, Giguère v, He YW. Lymphocyte development and function in the absence of retinoic acid-Related orphan receptor α. J Immunol 2004, 173, 2952-2959.
15. Masana MI, Sumaya IC, Becker-Andre M, Dubocovich ML. Behavioral characterization and modulation of circadian rhythms by light and melatonin in C3H/HeN mice homozygous for the RORβ knockout. Am J Physiol Regul Integr Comp Physiol 2007, 292, R2357-R2367.
16. Srinivas M, Ng L, Liu H, Jia L, Forrest D. Activation of the blue opsin gene in cone photoreceptor development by retinoid-Related orphan receptor β. Mol Endocrinol 2006, 20, 1728-1741.
17. Raichur S, Lau P, Staels B, Muscat GE. Retinoid-Related orphan receptor γ regulates several genes that control metabolism in skeletal muscle cells: Links to modulation of reactive oxygen species production. J Mol Endocrinol 2007, 39, 29-44.
18. Chen Y, Coulter S, Jetten AM, Goldstein JA. Identification of human CYP2C8 as a retinoid-Related orphan nuclear receptor target gene. J Pharmacol Exp Ther 2009, 329, 192-201.
19. Jetten AM, Joo JH. Retinoid-Related orphan receptors (RORs): Roles in cellular differentiation and development. Adv Dev Biol 2006, 16, 313-355.
20. Pike AC, Brzozowski AM, Hubbard RE. A structural biologist's view of the oestrogen receptor. J Steroid Biochem Mol Biol 2000, 74, 261-268.
21. Steinmetz AC, Renaud JP, Moras D. Binding of ligands and activation of transcription by nuclear receptors. Annu Rev Biophys Biomol Struct 2001, 30, 329-359.
22. Popov vM, Wang C, Shirley LA, Rosenberg A, Li S, Nevalainen M, Fu M, Pestell RG. The functional significance of nuclear receptor acetylation. Steroids 2007, 72, 221-230.
23. Faus H, Haendler B. Post-Translational modifications of steroid receptors. Biomed Pharmacother 2006, 60, 520-528.
24. Moraitis AN, Giguère V. The co-Repressor hairless protects RORα orphan nuclear receptor from proteasome-Nediated degradation. J Biol Chem 2003, 278, 52511-52518.
25. Jetten AM, Kurebayashi S, Ueda E. The ROR nuclear orphan receptor subfamily: Critical regulators of multiple biological processes. Prog Nucleic Acid Res Mol Biol 2001, 69, 205-247.
26. Moraitis AN, Giguère V. Transition from monomeric to homodimeric DNA binding by nuclear receptors: Identification of RevErbAα determinants required for RORα homodimer complex formation. Mol Endocrinol 1999, 13, 431-439.
27. vu-Dac N, Gervois P, Grötzinger T, De vos P, Schoonjans K, Fruchart JC, Auwerx J, Mariani J, Tedgui A, Staels B. Transcriptional regulation of apolipoprotein A-I gene expression by the nuclear receptor RORα. J Biol Chem 1997, 272, 22401-22404.
28. Stehlin-Gaon C, Willmann D, Zeyer D, Sanglier S, van Dorsselaer A, Renaud JP, Moras D, Sch?le R. All-Trans retinoic acid is a ligand for the orphan nuclear receptor ROR β. Nat Struct Biol 2003, 10, 820-825.
29. Harding HP, Atkins GB, Jaffe AB, Seo WJ, Lazar MA. Transcriptional activation and repression by RORα, an orphan nuclear receptor required for cerebellar development. Mol Endocrinol 1997, 11, 1737-1746.
30. Liu C, Li S, Liu T, Borjigin J, Lin JD. Transcriptional coactivator PGC- 1α integrates the mammalian clock and energy metabolism. Nature 2007, 447, 447-481.
31. Wolf IM, Heitzer MD, Grubisha M, DeFranco DB. Coactivators and nuclear receptor transactivation. J Cell Biochem 2008, 104, 1580-1586.
32. Xu W. Nuclear receptor coactivators: The key to unlock chromatin. Biochem Cell Biol 2005, 83, 418-428.
33. Hu X, Lazar MA. Transcriptional repression by nuclear hormone receptors. Trends Endocrinol Metab 2000, 11, 6-10.
34. Nagy L, Kao HY, Love JD, Li C, Banayo E, Gooch JT, Krishna v, Chatterjee K, Evans RM, Schwabe JW. Mechanism of corepressor binding and release from nuclear hormone receptors. Genes Dev 1999, 13, 3209-3216.
35. Kallen J, Schlaeppi JM, Bitsch F, Delhon I, Fournier B. Crystal structure of the human RORα Ligand binding domain in complex with cholesterol sulfate at 2.2 A. J Biol Chem 2004, 279, 14033-14038.
36. Kallen JA, Schlaeppi JM, Bitsch F, Geisse S, Geiser M, Delhon I, Fournier B. X-Ray structure of the hRORα LBD at 1.63 A: Structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORα. Structure 2002, 10, 1697-1707.
37. Wada T, Kang HS, Angers M, Gong H, Bhatia S, Khadem S, Ren S, Ellis E, Strom SC, Jetten AM, Xie W. Identification of oxysterol 7α-Hydroxylase (Cyp7b1) as a novel retinoid-Related orphan receptor alpha (RORα) (NR1F1) target gene and a functional crosstalk between RORα and liver X receptor (NR1H3). Mol Pharmacol 2008, 73, 891-899.
38. Zhu Y, McAvoy S, Kuhn R, Smith DI. RORA, a large common fragile site gene, is involved in cellular stress response. Oncogene 2006, 25, 2901-2908.
39. Smith DI, Zhu Y, McAvoy S, Kuhn R. Common fragile sites, extremely large genes, neural development and cancer. Cancer Lett 2006, 232, 48-57.
40. Lu Y, Yi Y, Liu P, Wen W, James M, Wang D, You M. Common human cancer genes discovered by integrated gene-Expression analysis. PLoS ONE 2007, 2, e1149.
41. Yamashita S, Tsujino Y, Moriguchi K, Tatematsu M, Ushijima T. Chemical genomic screening for methylation-Silenced genes in gastric cancer cell lines using 5-Aza-2'-Deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 2006, 97, 64-71.
42. Jetten AM, Ueda E. Retinoid-Related orphan receptors (RORs): Roles in cell survival, differentiation and disease. Cell Death Differ 2002, 9, 1167-1171.
43. Zhang F, Meng G, Strober W. Interactions among the transcription factors Runx1, RORγt and Foxp3 regulate the differentiation of interleukin 17-Producing T cells. Nat Immunol 2008, 9, 1297-1306.
44. Miyahara Y, Odunsi K, Chen W, Peng G, Matsuzaki J, Wang RF. Generation and regulation of human CD4+ IL-17-Producing T cells in ovarian cancer. Proc Natl Acad Sci USA 2008, 105, 15505-15510.
45. Pouysségur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441, 437-443.
46. Chauvet C, Bois-Joyeux B, Berra E, Pouyssegur J, Danan JL. The gene encoding human retinoic acid-Receptor-Related orphan receptor α is a target for hypoxia-Inducible factor 1. Biochem J 2004, 384, 79-85.
47. Miki N, Ikuta M, Matsui T. Hypoxia-Induced activation of the retinoic acid receptor-Related orphan receptor α4 gene by an interaction between hypoxia-Inducible factor-1 and Sp1. J Biol Chem 2004, 279, 15025-15031.
48. Joo JH, Liao G, Collins JB, Grissom SF, Jetten AM. Farnesolinduced apoptosis in human lung carcinoma cells is coupled to the endoplasmic reticulum stress response. Cancer Res 2007, 67, 7929-7936.
49. Besnard S, Silvestre JS, Duriez M, Bakouche J, Lemaigre-Dubreuil Y, Mariani J, Levy BI, Tedgui A. Increased ischemia-Induced angiogenesis in the staggerer mouse, a mutant of the nuclear receptor Rorα. Circ Res 2001, 89, 1209-1215.
50. Jaradat M, Stapleton C, Tilley SL, Dixon D, Erikson CJ, McCaskill JG, Kang HS, Angers M, Liao G, Collins J, Grissom S, Jetten AM. Modulatory role for retinoid-Related orphan receptor α in allergeninduced lung inflammation. Am J Respir Crit Care Med 2006, 174, 1299-1309.
51. Tilley SL, Jaradat M, Stapleton C, Dixon D, Hua X, Erikson CJ, McCaskill JG, Chason KD, Liao G, Jania L, Koller BH, Jetten AM. Retinoid-Related orphan receptor γ controls immunoglobulin production and Th1/Th2 cytokine balance in the adaptive immune response to allergen. J Immunol 2007, 178, 3208-3218.
52. Ivanov II, Zhou L, Littman DR. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 2007, 19, 409-417.
53. Yang XO, Chang SH, Park H, Nurieva R, Shah B, Acero L, Wang YH, Schluns KS, Broaddus RR, Zhu Z, Dong C. Regulation of inflammatory responses by IL-17F. J Exp Med 2008, 205, 1063-1075.
54. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, Kawakami K, Suda T, Sudo K, Nakae S, Iwakura Y, Matsuzaki G. IL-17-Nediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 2007, 178, 3786-3796.
55. Urry Z, Xystrakis E, Hawrylowicz CM. Interleukin-10-Secreting regulatory T cells in allergy and asthma. Curr Allergy Asthma Rep 2006, 6, 363-371.
56. Trenkner E, Hoffmann MK. Defective development of the thymus and immunological abnormalities in the neurological mouse mutation "staggerer". J Neurosci 1986, 6, 1733-1737.
57. He YW. The role of orphan nuclear receptor in thymocyte differentiation and lymphoid organ development. Immunol Res 2006, 22, 71-82.
58. Guo J, Hawwari A, Li H, Sun Z, Mahanta SK, Littman DR, Krangel MS, He YW. Regulation of the TCRα repertoire by the survival window of CD4(+)CD8(+) thymocytes. Nat Immunol 2002, 3, 469-476.
59. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126, 1121-1133.
60. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, Chung Y, Ma L, Shah B, Panopoulos AD, Schluns KS, Watowich SS, Tian Q, Jetten AM, Dong C. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR α and ROR γ. Immunity 2008, 28, 29-39.
61. Huang Z, Xie H, Wang R, Sun Z. Retinoid-Related orphan receptor γ t is a potential therapeutic target for controlling inflammatory autoimmunity. Expert Opin Ther Targets 2007, 11, 737-743.
62. Dong C. TH17 cells in development: An updated view of their molecular identity and genetic programming. Nat Rev Immunol 2008, 8, 337-348.
63. Furuzawa-Carballeda J, vargas-Rojas MI, Cabral AR. Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 2007, 6, 169-175.
64. Stockinger B, veldhoen M, Martin B. Th17 T cells: Linking innate and adaptive immunity. Semin Immunol 2007, 19, 353-361.
65. Leppkes M, Becker C, Ivanov II, Hirth S, Wirtz S, Neufert C, Pouly S, Murphy AJ, valenzuela DM, Yancopoulos GD, Becher B, Littman DR, Neurath MF. RORγ-Expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 2009, 136, 257-267.
66. Yamamoto T, Nakahata Y, Soma H, Akashi M, Mamine T, Takumi T. Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Mol Biol 2004, 5, 18.
67. Duguay D, Cermakian N. The crosstalk between physiology and circadian clock proteins. Chronobiol Int 2009, 26, 1479-1513.
68. Ellingsen T, Bener A, Gehani AA. Study of shift work and risk of coronary events. J R Soc Promot Health 2007, 127, 265-267.
69. Hermansson J, Gillander Gådin K, Karlsson B, Lindahl B, Stegmayr B, Knutsson A. Ischemic stroke and shift work. Scand J Work Environ Health 2007, 33, 435-439.
70. van Cauter E, Polonsky KS, Scheen AJ. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr Rev 2007, 18, 716-738.
71. Holterhus PM, Odendahl R, Oesingmann S, Lepler R, Wagner v, Hiort O, Holl R; German/Austrian DPv Initiative; German Pediatric CSII Working Group. Classification of distinct baseline insulin infusion patterns in children and adolescents with type 1 diabetes on continuous subcutaneous insulin infusion therapy. Diabetes Care 2007, 30, 568-573.
72. Chopra AR, Louet JF, Saha P, An J, Demayo F, Xu J, York B, Karpen S, Finegold M, Moore D, Chan L, Newgard CB, O'Malley BW. Absence of the SRC-2 coactivator results in a glycogenopathy resembling von Gierke's disease. Science 2008, 322, 1395-1399.
73. Wang Y, Kumar N, Solt LA, Richardson TI, Helvering LM, Crumbley C, Garcia-Ordonez RD, Stayrook KR, Zhang X, Novick S, Chalmers MJ, Griffin PR, Burris TP. Modulation of retinoic acid receptorrelated orphan receptor α and γ activity by 7-Oxygenated sterol ligands. J Biol Chem 2010, 285, 5013-5025.
74. Brown AJ, Jessup W. Oxysterols and atherosclerosis. Atherosclerosis 1999, 142, 1-28.
75. Brown AJ, Leong SL, Dean RT, Jessup W. 7-Hydroperoxycholesterol and its products in oxidized low density lipoprotein and human atherosclerotic plaque. J Lipid Res 1997, 38, 1730-1745.
76. Gelissen IC, Brown AJ, Mander EL, Kritharides L, Dean RT, Jessup W. Sterol efflux is impaired from macrophage foam cells selectively enriched with 7-ketocholesterol. J Biol Chem 1996, 271, 17852-17860.
77. Sonoda J, Rosenfeld JM, Xu L, Evans RM, Xie W. A nuclear receptor-Nediated xenobiotic response and its implication in drug metabolism and host protection. Curr Drug Metab 2003, 4, 59-72.
78. Xie W, Uppal H, Saini SP, Mu Y, Little JM, Radominska-Pandya A, Zemaitis MA. Orphan nuclear receptor-Nediated xenobiotic regulation in drug metabolism. Drug Discov Today 2004, 9, 442-449.
79. Kliewer SA, Moore JT, Wade L, Staudinger JL, Watson MA, Jones SA, McKee DD, Oliver BB, Willson TM, Zetterström RH, Perlmann T, Lehmann JM. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell 1998, 92, 73-82.
80. Blumberg B, Sabbagh W Jr, Juguilon H, Bolado J Jr, van Meter CM, Ong ES, Evans RM. SXR, a novel steroid and xenobiotic-Sensing nuclear receptor. Genes Dev 1998, 12, 3195-3205.
81. Xie W, Barwick JL, Downes M, Blumberg B, Simon CM, Nelson MC, Neuschwander-Tetri BA, Brunt EM, Guzelian PS, Evans RM. Humanized xenobiotic response in mice expressing nuclear receptor SXR. Nature 2000, 406, 435-439.
82. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, Willson TM, Koller BH, Kliewer SA. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 2001, 98, 3369-3374.
83. Honkakoski P, Zelko I, Sueyoshi T, Negishi M. The nuclear orphan receptor CAR-Retinoid X receptor heterodimer activates the phenobarbital-Responsive enhancer module of the CYP2B gene. Mol Cell Biol 1998, 18, 5652-5658.
84. Wei P, Zhang J, Egan-Hafley M, Liang S, Moore DD. The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism. Nature 2000, 407, 920-923.
85. Makishima M, Lu TT, Xie W, Whitfield GK, Domoto H, Evans RM, Haussler MR, Mangelsdorf DJ. vitamin D receptor as an intestinal bile acid sensor. Science 2002, 296, 1313-1316.
86. Hayhurst GP, Lee YH, Lambert G, Ward JM, Gonzalez FJ. Hepatocyte nuclear factor 4α (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol 2001, 21, 1393-1403.
87. Ito O, Nakamura Y, Tan L, Ishizuka T, Sasaki Y, Minami N, Kanazawa M, Ito S, Sasano H, Kohzuki M. Expression of cytochrome P-450 4 enzymes in the kidney and liver: Regulation by PPAR and speciesdifference between rat and human. Mol Cell Biochem 2006, 284, 141-148.
88. Marschall HU, Wagner M, Bodin K, Zollner G, Fickert P, Gumhold J, Silbert D, Fuchsbichler A, Sjövall J, Trauner M. Fxr(-/-) mice adapt to biliary obstruction by enhanced phase I detoxification and renal elimination of bile acids. J Lipid Res 2006, 47, 582-592.
89. Uppal H, Saini SP, Moschetta A, Mu Y, Zhou J, Gong H, Zhai Y, Ren S, Michalopoulos GK, Mangelsdorf DJ, Xie W. Activation of LXRs prevents bile acid toxicity and cholestasis in female mice. Hepatology 2007, 45, 422-432.
90. Gong H, Guo P, Zhai Y, Zhou J, Uppal H, Jarzynka MJ, Song WC, Cheng SY, Xie W. Estrogen deprivation and inhibition of breast cancer growth in vivo through activation of the orphan nuclear receptor liver X receptor. Mol Endocrinol 2007, 21, 1781-1790.