Bile acids down-regulate caveolin-1 in esophageal epithelial cells through sterol responsive element-binding protein

Molecular Endocrinology

Volumn 26, Issue 5, 2012, Pages 819-832

  Prade, Elke ^a   Tobiasch, Moritz ^a   Hitkova, Ivana ^b   Schäffer, Isabell ^b   Lian, Fan ^c   Xing, Xiangbin ^c   Tänzer, Marc ^a   Rauser, Sandra ^d   Walch, Axel ^d   Feith, Marcus ^a   Post, Stefan ^b   Röcken, Christoph ^e   Schmid, Roland M ^a   Ebert, Matthias P A ^b   Burgermeister, Elke ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^d Research Unit Analytical Pathology   (Germany)

^e UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CAVEOLIN 1; CHENODEOXYCHOLIC ACID; CHOLESTEROL; FARNESOID X RECEPTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ANIMAL CELL; ARTICLE; BARRETT ESOPHAGUS; BILE ACID SYNTHESIS; C57BL 6 MOUSE; CELL JUNCTION; CONTROLLED STUDY; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS MUCOSA; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RISK FACTOR; SQUAMOUS CELL METAPLASIA;

ADENOCARCINOMA; ANIMALS; BARRETT ESOPHAGUS; BILE ACIDS AND SALTS; CAVEOLIN 1; CELL LINE, TUMOR; DOWN-REGULATION; ESOPHAGEAL NEOPLASMS; ESOPHAGITIS, PEPTIC; ESOPHAGUS; FEMALE; GASTROESOPHAGEAL REFLUX; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM PROTEINS; NEOPLASM RECURRENCE, LOCAL; RANDOM ALLOCATION; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

MUS;

EID: 84860340369     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1140     Document Type: Article

References (70)

1. Lagergren J 2005 Adenocarcinoma of oesophagus: what exactly is the size of the problem and who is at risk? Gut 54 Suppl 1:i1-5
2. Shaheen NJ 2005 Advances in Barrett's esophagus and esophageal adenocarcinoma. Gastroenterology 128:1554-1566
3. Anderson LA, Watson RG, Murphy SJ, Johnston BT, Comber H, Mc Guigan J, Reynolds JV, Murray LJ 2007 Risk factors for Barrett's oesophagus and oesophageal adenocarcinoma: results from the FINBAR study. World J Gastroenterol 13:1585-1594
4. Flook NW, Wiklund I 2007 Accounting for the effect of GERD symptoms on patients' health-related quality of life: supporting optimal disease management by primary care physicians. Int J Clin Pract 61:2071-2078
5. Perez MJ, Briz O 2009 Bile-acid-induced cell injury and protection. World J Gastroenterol 15:1677-1689
6. Berr F, Pratschke E, Fischer S, Paumgartner G 1992 Disorders of bile acid metabolism in cholesterol gallstone disease. J Clin Invest 90:859-868
7. Hansen CG, Nichols BJ 2010 Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20:177-186
8. Williams TM, Lisanti MP 2004 The caveolin genes: from cell biology to medicine. Ann Med 36:584-595
9. Goetz JG, Lajoie P, Wiseman SM, Nabi IR 2008 Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev 27:715-735
10. Burgermeister E, Liscovitch M, Röcken C, Schmid RM, Ebert MP 2008 Caveats of caveolin-1 in cancer progression. Cancer Lett 268: 187-201
11. Ando T, Ishiguro H, Kimura M, Mitsui A, Mori Y, Sugito N, Tomoda K, Mori R, Harada K, Katada T, Ogawa R, Fujii Y, Kuwabara Y 2007 The overexpression of caveolin-1 and caveolin-2 correlates with a poor prognosis and tumor progression in esophageal squamous cell carcinoma. Oncol Rep 18:601-609
12. Kato K, Hida Y, Miyamoto M, Hashida H, Shinohara T, Itoh T, Okushiba S, Kondo S, Katoh H 2002 Overexpression of caveolin-1 in esophageal squamous cell carcinoma correlates with lymph node metastasis and pathologic stage. Cancer 94:929-933
13. Watanabe M, Houten SM, Wang L, Moschetta A, Mangelsdorf DJ, Heyman RA, Moore DD, Auwerx J 2004 Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 113:1408-1418
14. Bist A, Fielding PE, Fielding CJ 1997 Two sterol regulatory element-like sequences mediate up-regulation of caveolin gene transcription in response to low density lipoprotein free cholesterol. Proc Natl Acad Sci USA 94:10693-10698
15. Raghow R, Yellaturu C, Deng X, Park EA, Elam MB 2008 SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol Metab 19:65-73
16. Bengoechea-Alonso MT, Ericsson J 2007 SREBP in signal transduction: cholesterol metabolism and beyond. Curr Opin Cell Biol 19:215-222
17. Cao S, Fernandez-Zapico ME, Jin D, Puri V, Cook TA, Lerman LO, Zhu XY, Urrutia R, Shah V 2005 KLF11-mediated repression antagonizes Sp1/sterol-responsive element-binding protein-induced transcriptional activation of caveolin-1 in response to cholesterol signaling. J Biol Chem 280:1901-1910
18. Yuan HY, Kuang SY, Zheng X, Ling HY, Yang YB, Yan PK, Li K, Liao DF 2008 Curcumin inhibits cellular cholesterol accumulation by regulating SREBP-1/caveolin-1 signaling pathway in vascular smooth muscle cells. Acta Pharmacol Sin 29:555-563
19. Luo DX, Xia CL, Li JM, Xiong Y, Yuan HY, Tang ZW, Zeng Y, Liao DF 2010 Static pressure accelerates ox-LDL-induced cholesterol accumulation via SREBP-1-mediated caveolin-1 downregulation in cultured vascular smooth muscle cells. Biochem Biophys Res Commun 403:52-58
20. Burgermeister E, Xing X, Röcken C, Juhasz M, Chen J, Hiber M, Mair K, Shatz M, Liscovitch M, Schmid RM, Ebert MP 2007 Differential expression and function of caveolin-1 in human gastric cancer progression. Cancer Res 67:8519-8526
21. Xing X, Burgermeister E, Geisler F, Einwächter H, Fan L, Hiber M, Rauser S, Walch A, Röcken C, Ebeling M, Wright MB, Schmid RM, Ebert MP 2009 Hematopoietically expressed homeobox is a target gene of farnesoid X receptor in chenodeoxycholic acid-induced liver hypertrophy. Hepatology 49:979-988
22. Fichter CD, Herz C, Münch C, Opitz OG, Werner M, Lassmann S 2011 Occurrence of multipolar mitoses and association with Aurora-A/-B kinases and p53 mutations in aneuploid esophageal carcinoma cells. BMC Cell Biol 12:13
23. Burgermeister E, Tencer L, Liscovitch M 2003 Peroxisome proliferator- activated receptor-gamma upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells. Oncogene 22: 3888-3900
24. Yu J, Leung WK, Ebert MP, Leong RW, Tse PC, Chan MW, Bai AH, To KF, Malfertheiner P, Sung JJ 2003 Absence of cyclin D2 expression is associated with promoter hypermethylation in gastric cancer. Br J Cancer 88:1560-1565
25. Rödel F, Capalbo G, Rödel C, Weiss C 2009 Caveolin-1 as a prognostic marker for local control after preoperative chemoradiation therapy in rectal cancer. Int J Radiat Oncol Biol Phys 73:846-852
26. Qin P, Borges-Marcucci LA, Evans MJ, Harnish DC 2005 Bile acid signaling through FXR induces intracellular adhesion molecule-1 expression in mouse liver and human hepatocytes. Am J Physiol Gastrointest Liver Physiol 289:G267-G273
27. Lian F, Xing X, Yuan G, Schäfer C, Rauser S, Walch A, Röcken C, Ebeling M, Wright MB, Schmid RM, Ebert MP, Burgermeister E 2011 Farnesoid X receptor protects human and murine gastric epithelial cells against inflammation-induced damage. Biochem J 438: 315-323
28. Bonuccelli G, Casimiro MC, Sotgia F, Wang C, Liu M, Katiyar S, Zhou J, Dew E, Capozza F, Daumer KM, Minetti C, Milliman JN, Alpy F, Rio MC, Tomasetto C, Mercier I, Flomenberg N, Frank PG, Pestell RG, Lisanti MP 2009 Caveolin-1 (P132L), a common breast cancer mutation, confers mammary cell invasiveness and defines a novel stem cell/metastasis-associated gene signature. Am J Pathol 174:1650-1662
29. Hayashi K, Matsuda S, Machida K, Yamamoto T, Fukuda Y, Nimura Y, Hayakawa T, Hamaguchi M 2001 Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res 61:2361-2364
30. Burgermeister E, Friedrich T, Hitkova I, Regel I, Einwächter H, Zimmermann W, Röcken C, Perren A, Wright MB, Schmid RM, Seger R, Ebert MP 2011 The Ras inhibitors caveolin-1 and docking protein 1 activate peroxisome proliferator-activated receptor gamma through spatial relocalization at helix 7 of its ligand-binding domain. Mol Cell Biol 31:3497-3510
31. Williams TM, Lisanti MP 2005 Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 288: C494-C506
32. Schlegel A, Arvan P, Lisanti MP 2001 Caveolin-1 binding to endoplasmic reticulum membranes and entry into the regulated secretory pathway are regulated by serine phosphorylation. Protein sorting at the level of the endoplasmic reticulum. J Biol Chem 276: 4398-4408
33. Tahir SA, Yang G, Ebara S, Timme TL, Satoh T, Li L, Goltsov A, Ittmann M, Morrisett JD, Thompson TC 2001 Secreted caveolin-1 stimulates cell survival/clonal growth and contributes to metastasis in androgen-insensitive prostate cancer. Cancer Res 61:3882-3885
34. Ayala GE, Dai H, Tahir SA, Li R, Timme T, Ittmann M, Frolov A, Wheeler TM, Rowley D, Thompson TC 2006 Stromal antiapoptotic paracrine loop in perineural invasion of prostatic carcinoma. Cancer Res 66:5159-5164
35. Lin SY, Yeh KT, Chen WT, Chen HC, Chen ST, Chang JG 2004 Promoter CpG methylation of caveolin-1 in sporadic colorectal cancer. Anticancer Res 24:1645-1650
36. Engelman JA, Zhang XL, Lisanti MP 1999 Sequence and detailed organization of the human caveolin-1 and -2 genes located near the D7S522 locus (7q31.1). Methylation of a CpG island in the 5′promoter region of the caveolin-1 gene in human breast cancer cell lines. FEBS Lett 448:221-230
37. Dvorak K, Watts GS, Ramsey L, Holubec H, Payne CM, Bernstein C, Jenkins GJ, Sampliner RE, Prasad A, Garewal HS, Bernstein H 2009 Expression of bile acid transporting proteins in Barrett's esophagus and esophageal adenocarcinoma. Am J Gastroenterol 104:302-309
38. Hao Y, Sood S, Triadafilopoulos G, Kim JH, Wang Z, Sahbaie P, Omary MB, Lowe AW 2007 Gene expression changes associated with Barrett's esophagus and Barrett's-associated adenocarcinoma cell lines after acid or bile salt exposure. BMC Gastroenterol 7:24
39. Burnat G, Rau T, Elshimi E, Hahn EG, Konturek PC 2007 Bile acids induce overexpression of homeobox gene CDX-2 and vascular endothelial growth factor (VEGF) in human Barrett's esophageal mucosa and adenocarcinoma cell line. Scand J Gastroenterol 42:1460-1465
40. Kong J, Crissey MA, Funakoshi S, Kreindler JL, Lynch JP 2011 Ectopic Cdx2 expression in murine esophagus models an intermediate stage in the emergence of Barrett's esophagus. PLoS One 6:e18280.
41. Jean-Louis S, Akare S, Ali MA, Mash Jr EA, Meuillet E, Martinez JD 2006 Deoxycholic acid induces intracellular signaling through membrane perturbations. J Biol Chem 281:14948-14960
42. Hu Y, Williams VA, Gellersen O, Jones C, Watson TJ, Peters JH 2007 The pathogenesis of Barrett's esophagus: secondary bile acids upregulate intestinal differentiation factor CDX2 expression in esophageal cells. J Gastrointest Surg 11:827-834
43. Avissar NE, Toia L, Hu Y, Watson TJ, Jones C, Raymond DP, Matousek A, Peters JH 2009 Bile acid alone, or in combination with acid, induces CDX2 expression through activation of the epidermal growth factor receptor (EGFR). J Gastrointest Surg 13:212-222
44. Cronin J, McAdam E, Danikas A, Tselepis C, Griffiths P, Baxter J, Thomas L, Manson J, Jenkins G 2011 Epidermal growth factor receptor (EGFR) is overexpressed in high-grade dysplasia and adenocarcinoma of the esophagus and may represent a biomarker of histological progression in Barrett's esophagus (BE). Am J Gastroenterol 106:46-56
45. Lanuti M, Liu G, Goodwin JM, Zhai R, Fuchs BC, Asomaning K, Su L, Nishioka NS, Tanabe KK, Christiani DC 2008 A functional epidermal growth factor (EGF) polymorphism, EGF serum levels, and esophageal adenocarcinoma risk and outcome. Clin Cancer Res 14:3216-3222
46. Yeh M, Cole AL, Choi J, Liu Y, Tulchinsky D, Qiao JH, Fishbein MC, Dooley AN, Hovnanian T, Mouilleseaux K, Vora DK, Yang WP, Gargalovic P, Kirchgessner T, Shyy JY, Berliner JA 2004 Role for sterol regulatory element-binding protein in activation of endothelial cells by phospholipid oxidation products. Circ Res 95:780-788
47. Llaverias G, Vázquez-Carrera M, Sánchez RM, Noé V, Ciudad CJ, Laguna JC, Alegret M 2004 Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism. J Lipid Res 45:2015-2024
48. Sunaga N, Miyajima K, Suzuki M, Sato M, White MA, Ramirez RD, Shay JW, Gazdar AF, Minna JD 2004 Different roles for caveolin- 1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res 64:4277-4285
49. Engelman JA, Zhang XL, Lisanti MP 1998 Genes encoding human caveolin-1 and -2 are co-localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers. FEBS Lett 436:403-410
50. Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, Jin Z, Sato F, Berki AT, Kan T, Ito T, Mantzur C, Abraham JM, Meltzer SJ 2006 A genome-wide search identifies epigenetic silencing of somatostatin, tachykinin-1, and 5 other genes in colon cancer. Gastroenterology 131:797-808
51. Yamashita S, Tsujino Y, Moriguchi K, Tatematsu M, Ushijima T 2006 Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2′-deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 97:64-71
52. Buxman MM, Goodkin PE, Fahrenbach WH, Dimond RL 1979 Harlequin ichthyosis with epidermal lipid abnormality. Arch Dermatol 115:189-193
53. Jong MC, Gijbels MJ, Dahlmans VE, Gorp PJ, Koopman SJ, Ponec M, Hofker MH, Havekes LM 1998 Hyperlipidemia and cutaneous abnormalities in transgenic mice overexpressing human apolipoprotein C1. J Clin Invest 101:145-152
54. Evers BM, Farooqi MS, Shelton JM, Richardson JA, Goldstein JL, Brown MS, Liang G 2010 Hair growth defects in Insig-deficient mice caused by cholesterol precursor accumulation and reversed by simvastatin. J Invest Dermatol 130:1237-1248
55. Smyth I, Hacking DF, Hilton AA, Mukhamedova N, Meikle PJ, Ellis S, Satterley K, Collinge JE, de Graaf CA, Bahlo M, Sviridov D, Kile BT, Hilton DJ 2008 A mouse model of harlequin ichthyosis delineates a key role for Abca12 in lipid homeostasis. PLoS Genet 4:e1000192
56. Mirza R, Hayasaka S, Takagishi Y, Kambe F, Ohmori S, Maki K, Yamamoto M, Murakami K, Kaji T, Zadworny D, Murata Y, Seo H 2006 DHCR24 gene knockout mice demonstrate lethal dermopathy with differentiatin and maturation defects in the epidermis. J Invest Dermatol 126:638-647
57. Ishibashi S, Schwarz M, Frykman PK, Herz J, Russell DW 1996 Disruption of cholesterol 7alpha-hydroxylase gene in mice. I. Postnatal lethality reversed by bile acid and vitamin supplementation. J Biol Chem 271:18017-18023
58. Hamanaka S, Ujihara M, Serizawa S, Nakazawa S, Otsuka F 1997 A case of recessive X-linked ichthyosis: scale-specific abnormalities of lipid composition may explain the pathogenesis of the skin manifestation. J Dermatol 24:156-160
59. Mégarbané H, Mégarbané A 2011 Ichthyosis follicularis, alopecia, and photophobia (IFAP) syndrome. Orphanet J Rare Dis 6:29
60. Takahashi K, Folmer J, Coulombe PA 1994 Increased expression of keratin 16 causes anomalies in cytoarchitecture and keratinization in transgenic mouse skin. J Cell Biol 127:505-520
61. Schaaij-Visser TB, Bremmer JF, Braakhuis BJ, Heck AJ, Slijper M, van der Waal I, Brakenhoff RH 2010 Evaluation of cornulin, keratin 4, keratin 13 expression and grade of dysplasia for predicting malignant progression of oral leukoplakia. Oral Oncol 46:123-127
62. Yao D, Alexander CL, Quinn JA, Porter MJ, Wu H, Greenhalgh DA 2006 PTEN loss promotes rasHa-mediated papillomatogenesis via dual up-regulation of AKT activity and cell cycle deregulation but malignant conversion proceeds via PTEN-associated pathways. Cancer Res 66:1302-1312
63. van Baal JW, Bozikas A, Pronk R, Ten Kate FJ, Milano F, Rygiel AM, Rosmolen WD, Peppelenbosch MP, Bergman JJ, Krishnadath KK 2008 Cytokeratin and CDX-2 expression in Barrett's esophagus. Scand J Gastroenterol 43:132-140
64. Magin TM, Vijayaraj P, Leube RE 2007 Structural and regulatory functions of keratins. Exp Cell Res 313:2021-2032
65. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW 2010 The tumor-suppressive function of Connexin43 in keratinocytes is mediated in part via interaction with caveolin-1. Cancer Res 70:4222-4232
66. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW 2008 Caveolin- 1 and -2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol Biol Cell 19: 912-928
67. Kant P, Hull MA 2011 Excess body weight and obesity-the link with gastrointestinal and hepatobiliary cancer. Nat Rev Gastroenterol Hepatol 8:224-238
68. Abrams JA 2009 Obesity and Barrett's oesophagus: more than just reflux. Gut 58:1437-1438
69. Flegal KM 2000 Obesity, overweight, hypertension, and high blood cholesterol: the importance of age. Obes Res 8:676-677
70. 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