Hypoxia downregulates farnesoid X receptor via a hypoxia-inducible factor-independent but p38 mitogen-activated protein kinase-dependent pathway

FEBS Journal

Volumn 276, Issue 5, 2009, Pages 1319-1332

  Fujino, Tomofumi ^a   Murakami, Kaori ^a   Ozawa, Issei ^a   Minegishi, Yoshie ^a   Kashimura, Ryo ^a   Akita, Toshihiro ^a   Saitou, Susumu ^a   Atsumi, Takehisa ^a   Sato, Takashi ^a   Ando, Ken ^a   Hara, Shuntaro ^b   Kikugawa, Kiyomi ^a   Hayakawa, Makio ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b SHOWA UNIVERSITY   (Japan)

Author keywords

Cholestasis; Farnesoid X receptor; Hypoxia inducible factor; Ischemia; Mitogen activated protein kinase

Indexed keywords

BILE ACID; BILE SALT; FARNESOID X RECEPTOR; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; HYPOXIA INDUCIBLE FACTOR 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BILE FLOW; BILIARY EXCRETION; CELL STRAIN HEPG2; CHOLESTASIS; CONTROLLED STUDY; EVOKED RESPONSE; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPOXIA; LIVER; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUMP; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

BILE ACIDS AND SALTS; CELL HYPOXIA; CELLS, CULTURED; DNA-BINDING PROTEINS; DOWN-REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 60349116993     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.06867.x     Document Type: Article

References (63)

1. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835 839.
2. Forman BM, Goode E, Chen J, Oro AE, Bradley DJ, Perlmann T, Noonan DJ, Burka LT, McMorris T, Lamph WW et al. (1995) Identification of a nuclear receptor that is activated by farnesol metabolites. Cell 81, 687 693.
3. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ Shan B (1999) Identification of a nuclear receptor for bile acids. Science 284, 1362 1365.
4. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD et al. (1999) Bile acids: natural ligands for an orphan nuclear receptor. Science 284, 1365 1368.
5. Wang H, Chen J, Hollister K, Sowers LC Forman BM (1999) Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell 3, 543 553.
6. Seol W, Choi HS Moore DD (1995) Isolation of proteins that interact specifically with the retinoid X receptor: two novel orphan receptors. Mol Endocrinol 9, 72 85.
7. Glass CK (1994) Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr Rev 15, 391 407.
8. Huber RM, Murphy K, Miao B, Link JR, Cunningham MR, Rupar MJ, Gunyuzlu PL, Haws TF, Kassam A, Powell F et al. (2002) Generation of multiple farnesoid-X-receptor isoforms through the use of alternative promoters. Gene 290, 35 43.
9. Zhang Y, Kast-Woelbern HR Edwards PA (2003) Natural structural variants of the nuclear receptor farnesoid X receptor affect transcriptional activation. J Biol Chem 278, 104 110.
10. Rizzo G, Disante M, Mencarelli A, Renga B, Gioiello A, Pellicciari R Fiorucci S (2006) The farnesoid X receptor promotes adipocyte differentiation and regulates adipose cell function in vivo. Mol Pharmacol 70, 1164 1173.
11. Cariou B, van Harmelen K, Duran-Sandoval D, van Dijk TH, Grefhorst A, Abdelkarim M, Caron S, Torpier G, Fruchart JC, Gonzalez FJ et al. (2006) The farnesoid X receptor modulates adiposity and peripheral insulin sensitivity in mice. J Biol Chem 281, 11039 11049.
12. Fiorucci S, Rizzo G, Donini A, Distrutti E Santucci L (2007) Targeting farnesoid X receptor for liver and metabolic disorders. Trends Mol Med 13, 298 309.
13. Zhang Y Edwards PA (2008) FXR signaling in metabolic disease. FEBS Lett 582, 10 18.
14. Zollner G, Marschall HU, Wagner M Trauner M (2006) Role of nuclear receptors in the adaptive response to bile acids and cholestasis: pathogenetic and therapeutic considerations. Mol Pharm 3, 231 251.
15. Cutrin JC, Cantino D, Biasi F, Chiarpotto E, Salizzoni M, Andorno E, Massano G, Lanfranco G, Rizzetto M, Boveris A et al. (1996) Reperfusion damage to the bile canaliculi in transplanted human liver. Hepatology 24, 1053 1057.
16. Henley KS, Lucey MR, Appelman HD, Baliga P, Brown KA, Burtch GD, Campbell DA Jr., Ham JM, Merion RM Turcotte JG (1992) Biochemical and histopathological correlation in liver transplant: the first 180 days. Hepatology 16, 688 693.
17. Rosmorduc O, Wendum D, Corpechot C, Galy B, Sebbagh N, Raleigh J, Housset C Poupon R (1999) Hepatocellular hypoxia-induced vascular endothelial growth factor expression and angiogenesis in experimental biliary cirrhosis. Am J Pathol 155, 1065 1073.
18. Corpechot C, Barbu V, Wendum D, Kinnman N, Rey C, Poupon R, Housset C Rosmorduc O (2002) Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology 35, 1010 1021.
19. Bozova S Elpek GO (2007) Hypoxia-inducible factor-1α expression in experimental cirrhosis: correlation with vascular endothelial growth factor expression and angiogenesis. APMIS 115, 795 801.
20. Giaccia AJ, Simon MC Johnson R (2004) The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev 18, 2183 2194.
21. Lando D, Peet DJ, Whelan DA, Gorman JJ Whitelaw ML (2002) Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295, 858 861.
22. Maynard MA, Qi H, Chung J, Lee EH, Kondo Y, Hara S, Conaway RC, Conaway JW Ohh M (2003) Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 278, 11032 11040.
23. Fouassier L, Beaussier M, Schiffer E, Rey C, Barbu V, Mergey M, Wendum D, Callard P, Scoazec JY, Lasnier E et al. (2007) Hypoxia-induced changes in the expression of rat hepatobiliary transporter genes. Am J Physiol Gastrointest Liver Physiol 293, G25 G35.
24. Datta S, Wang L, Moore DD Osborne TF (2006) Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase promoter by nuclear receptors liver receptor homologue-1 and small heterodimer partner: a mechanism for differential regulation of cholesterol synthesis and uptake. J Biol Chem 281, 807 812.
25. De Fabiani E, Mitro N, Gilardi F, Caruso D, Galli G Crestani M (2003) Coordinated control of cholesterol catabolism to bile acids and of gluconeogenesis via a novel mechanism of transcription regulation linked to the fasted-to-fed cycle. J Biol Chem 278, 39124 39132.
26. Han SI, Studer E, Gupta S, Fang Y, Qiao L, Li W, Grant S, Hylemon PB Dent P (2004) Bile acids enhance the activity of the insulin receptor and glycogen synthase in primary rodent hepatocytes. Hepatology 39, 456 463.
27. Ono K Han J (2000) The p38 signal transduction pathway: activation and function. Cell Signal 12, 1 13.
28. Holt JA, Luo G, Billin AN, Bisi J, McNeill YY, Kozarsky KF, Donahee M, Wang DY, Mansfield TA, Kliewer SA et al. (2003) Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev 17, 1581 1591.
29. Stravitz RT, Rao YP, Vlahcevic ZR, Gurley EC, Jarvis WD Hylemon PB (1996) Hepatocellular protein kinase C activation by bile acids: implications for regulation of cholesterol 7 alpha-hydroxylase. Am J Physiol 271, G293 G303.
30. De Fabiani E, Mitro N, Anzulovich AC, Pinelli A, Galli G Crestani M (2001) The negative effects of bile acids and tumor necrosis factor-α on the transcription of cholesterol 7 α-hydroxylase gene (CYP7A1) converge to hepatic nuclear factor-4: a novel mechanism of feedback regulation of bile acid synthesis mediated by nuclear receptors. J Biol Chem 276, 30708 30716.
31. Fang Y, Han SI, Mitchell C, Gupta S, Studer E, Grant S, Hylemon PB Dent P (2004) Bile acids induce mitochondrial ROS, which promote activation of receptor tyrosine kinases and signaling pathways in rat hepatocytes. Hepatology 40, 961 971.
32. Xu Z, Tavares-Sanchez OL, Li Q, Fernando J, Rodriguez CM, Studer EJ, Pandak WM, Hylemon PB Gil G (2007) Activation of bile acid biosynthesis by the p38 mitogen-activated protein kinase (MAPK): hepatocyte nuclear factor-4α phosphorylation by the p38 MAPK is required for cholesterol 7α-hydroxylase expression. J Biol Chem 282, 24607 24614.
33. Kulisz A, Chen N, Chandel NS, Shao Z Schumacker PT (2002) Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol Lung Cell Mol Physiol 282, L1324 L1329.
34. Xu L, Pathak PS Fukumura D (2004) Hypoxia-induced activation of p38 mitogen-activated protein kinase and phosphatidylinositol 3′-kinase signaling pathways contributes to expression of interleukin 8 in human ovarian carcinoma cells. Clin Cancer Res 10, 701 707.
35. Eguchi R, Suzuki A, Miyakaze S, Kaji K Ohta T (2007) Hypoxia induces apoptosis of HUVECs in an in vitro capillary model by activating proapoptotic signal p38 through suppression of ERK1/2. Cell Signal 19, 1121 1131.
36. Song X, Kaimal R, Yan B Deng R (2008) Liver receptor homolog 1 transcriptionally regulates human bile salt export pump expression. J Lipid Res 49, 973 984.
37. Zagorska A Dulak J (2004) HIF-1: the knowns and unknowns of hypoxia sensing. Acta Biochim Pol 51, 563 585.
38. Bruegge K, Jelkmann W Metzen E (2007) Hydroxylation of hypoxia-inducible transcription factors and chemical compounds targeting the HIF-alpha hydroxylases. Curr Med Chem 14, 1853 1862.
39. Maynard MA Ohh M (2007) The role of hypoxia-inducible factors in cancer. Cell Mol Life Sci 64, 2170 2180.
40. Conrad PW, Rust RT, Han J, Millhorn DE Beitner-Johnson D (1999) Selective activation of p38α and p38γ by hypoxia. Role in regulation of cyclin D1 by hypoxia in PC12 cells. J Biol Chem 274, 23570 23576.
41. Cowan KJ Storey KB (2003) Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J Exp Biol 206, 1107 1115.
42. Lali FV, Hunt AE, Turner SJ Foxwell BM (2000) The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J Biol Chem 275, 7395 7402.
43. Hollenbach E, Vieth M, Roessner A, Neumann M, Malfertheiner P Naumann M (2005) Inhibition of RICK/nuclear factor-kappaB and p38 signaling attenuates the inflammatory response in a murine model of Crohn disease. J Biol Chem 280, 14981 14988.
44. Henklova P, Vrzal R, Papouskova B, Bednar P, Jancova P, Anzenbacherova E, Ulrichova J, Maurel P, Pavek P Dvorak Z (2008) SB203580, a pharmacological inhibitor of p38 MAP kinase transduction pathway activates ERK and JNK MAP kinases in primary cultures of human hepatocytes. Eur J Pharmacol 593, 16 23.
45. Birkenkamp KU, Tuyt LM, Lummen C, Wierenga AT, Kruijer W Vellenga E (2000) The p38 MAP kinase inhibitor SB203580 enhances nuclear factor-kappa B transcriptional activity by a non-specific effect upon the ERK pathway. Br J Pharmacol 131, 99 107.
46. Batts KP (1998) Ischemic cholangitis. Mayo Clin Proc 73, 380 385.
47. Beaussier M, Wendum D, Fouassier L, Rey C, Barbu V, Lasnier E, Lienhart A, Scoazec JY, Rosmorduc O Housset C (2005) Adaptative bile duct proliferative response in experimental bile duct ischemia. J Hepatol 42, 257 265.
48. Kim KR, Moon HE Kim KW (2002) Hypoxia-induced angiogenesis in human hepatocellular carcinoma. J Mol Med 80, 703 714.
49. Paumgartner G (2006) Medical treatment of cholestatic liver diseases: from pathobiology to pharmacological targets. World J Gastroenterol 12, 4445 4451.
50. Stedman C, Liddle C, Coulter S, Sonoda J, Alvarez JG, Evans RM Downes M (2006) Benefit of farnesoid X receptor inhibition in obstructive cholestasis. Proc Natl Acad Sci USA 103, 11323 11328.
51. Marschall HU, Wagner M, Bodin K, Zollner G, Fickert P, Gumhold J, Silbert D, Fuchsbichler A, Sjövall J Trauner M (2006) Fxr(-/-) mice adapt to biliary obstruction by enhanced phase I detoxification and renal elimination of bile acids. J Lipid Res 47, 582 592.
52. Alrefai WA Gill RK (2007) Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm Res 24, 1803 1823.
53. Trauner M Boyer JL (2003) Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83, 633 671.
54. König J, Rost D, Cui Y Keppler D (1999) Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology 29, 1156 1163.
55. Thompson R Strautnieks S (2001) BSEP: function and role in progressive familial intrahepatic cholestasis. Semin Liver Dis 21, 545 550.
56. Chen F, Ananthanarayanan M, Emre S, Neimark E, Bull LN, Knisely AS, Strautnieks SS, Thompson RJ, Magid MS, Gordon R et al. (2004) Progressive familial intrahepatic cholestasis, type 1, is associated with decreased farnesoid X receptor activity. Gastroenterology 126, 756 764.
57. Alvarez L, Jara P, Sánchez-Sabaté E, Hierro L, Larrauri J, Díaz MC, Camarena C, De la Vega A, Frauca E, López-Collazo E et al. (2004) Reduced hepatic expression of farnesoid X receptor in hereditary cholestasis associated to mutation in ATP8B1. Hum Mol Genet 13, 2451 2460.
58. Kubitz R, Sütfels G, Kühlkamp T, Kölling R Häussinger D (2004) Trafficking of the bile salt export pump from the Golgi to the canalicular membrane is regulated by the p38 MAP kinase. Gastroenterology 126, 541 553.
59. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65, 55 63.
60. Zhang Y, Castellani LW, Sinal CJ, Gonzalez FJ Edwards PA (2004) Peroxisome proliferator-activated receptor-gamma coactivator 1 α (PGC-1 α) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes Dev 18, 157 169.
61. Horii K, Suzuki Y, Kondo Y, Akimoto M, Nishimura T, Yamabe Y, Sakaue M, Sano T, Kitagawa T, Himeno S et al. (2007) Androgen-dependent gene expression of prostate-specific antigen is enhanced synergistically by hypoxia in human prostate cancer cells. Mol Cancer Res 5, 383 391.
62. Sowter HM, Raval RR, Moore JW, Ratcliffe PJ Harris AL (2003) Predominant role of hypoxia-inducible transcription factor (Hif)-1 α versus Hif-2 α in regulation of the transcriptional response to hypoxia. Cancer Res 63, 6130 6134.
63. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J Gleadle JM (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1α, HIF-2α, and other pathways. J Biol Chem 281, 15215 15226.