Tauroursodeoxycholate inhibits human cholangiocarcinoma growth via Ca 2+-, PKC-, and MAPK-dependent pathways

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 286, Issue 6 49-6, 2004, Pages

  Alpini, Gianfranco ^a,c   Kanno, Noriatsu ^a   Phinizy, Jo Lynne ^b   Glaser, Shannon ^b   Francis, Healher ^b   Taffetani, Silvia ^b   LeSage, Gene ^a,d  

^a Department of Internal Medicine ^*  (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c Ctrl Texas Vet Health Care System   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Bile acids; Bile ducts; Cancer; Cyclic adenosine monophosphate; Mitosis

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; B RAF KINASE; CALCIUM CHELATING AGENT; CALCIUM ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C INHIBITOR; RAF PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TAUROURSOCHOLIC ACID; UNCLASSIFIED DRUG; CALCIUM; PRKCA PROTEIN, HUMAN; TAUROCHENODEOXYCHOLIC ACID; TAUROURSODEOXYCHOLIC ACID;

ARTICLE; BILE DUCT CARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION; TIME; BILE DUCT TUMOR; DRUG EFFECT; INTRACELLULAR MEMBRANE; INTRAHEPATIC BILE DUCT; METABOLISM; OSMOLARITY; PATHOLOGY; PHOSPHORYLATION; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE;

BILE DUCT NEOPLASMS; BILE DUCTS, INTRAHEPATIC; BIOLOGICAL TRANSPORT; CALCIUM; CELL LINE, TUMOR; CHOLANGIOCARCINOMA; HUMANS; INTRACELLULAR MEMBRANES; MITOGEN-ACTIVATED PROTEIN KINASES; OSMOLAR CONCENTRATION; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-RAF; TAUROCHENODEOXYCHOLIC ACID; TIME FACTORS;

EID: 2642548956     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00270.2003     Document Type: Article

References (68)

1. Alpini G, Baiocchi L, Glaser S, Ueno Y, Marzioni M, Francis H, Phinizy JL, Angelico M, and LeSage G. Ursodeoxycholate and tauroursodeoxycholate inhibit cholangiocyte growth and secretion of BDL rats through activation of PKC alpha. Hepatology 35: 1041-1052, 2002.
2. Alpini G, Prall RT, and LaRusso NF. The pathobiology of biliary epithelia. In: The Liver: Biology and Pathobiology (4th ed), edited by Arias IM, Boyer JL, Chisari FV, Fausto N, Jakoby W, Schachter D, and Shafritz DA. Philadelphia, PA: Lippincott Williams & Wilkins, 2001, p. 421-435.
3. Alpini G, Ueno Y, Glaser SS, Marzioni M, Phinizy JL, Francis H, and LeSage G. Bile acid feeding increased proliferative activity and apical bile acid transporter expression in both small and large rat cholangiocytes. Hepatology 34: 868-876, 2001.
4. Alvarez E, Northwood IC, Gonzalez FA, Latour DA, Seth A, Abate C, Curran T, and Davis RJ. Pro-Leu-Ser/Trh-Pro is a consensus primary sequence for substrate protein phosphorylation: characterization of the phosphorylation of c-Myc and c-Jun proteins by an epidermal growth factor receptor threonine 669 protein kinase. J Biol Chem 266: 15277-15825, 1991.
5. Alvaro D, Della Guardia P, Bini A, Gigliozzi A, Furfaro S, La Rosa T, Piat C, and Capocaccia L. Effect of glucagon on intracellular pH regulation in isolated rat hepatocyte couplets. J Clin Invest 96: 665-674, 1995.
6. - exchange in cholangiocytes. Am J Physiol Gastrointest Liver Physiol 273: G303-G313, 1997.
7. André F, Rigot V, Remacle-Bonnet M, Luis J, Pommier G, and Marvaldi J. Protein kinase C-γ and -δ are involved in insulin-like growth factor-I migration of colonic epithelial cells. Gastroenterology 116: 64-77, 1999.
8. Batlle E, Verdù J, Dominguez D, del Mont Liosas M, Diaz V, Loukili N, Paciucci R, Alameda F, and Garcia de Herreros A. Protein kinase C-alpha activity inversely modulates invasion and growth of intestinal cells. J Biol Chem 273: 15091-15098, 1998.
9. Baumgartner U, Scholmerich J, Sellinger M, Reinhardt M, Ruf G, and Farthmann EH. Different protective effects of tauroursodeoxycholate, ursodeoxycholate, and 23-methyl-ursodeoxycholate against taurolithocholate-induced cholestasis. Dig Dis Sci 41: 250-255, 1996.
10. Benedetti A, Alvaro D, Bassotti C, Gigliozzi A, Ferretti G, La Rosa T, Di Sario A, Baiocchi L, and Jezequel AM. Cytotoxicity of bile salts against biliary epithelium: a study in isolated bile ductule fragments and isolated perfused rat liver. Hepatology 26: 9-21, 1997.
11. Benz C, Angermuller S, Otto G, Sauer P, Stremmel W, and Stiehl A. Effect of tauroursodeoxycholic acid on bile acid-induced apoptosis in primary human hepatocytes. Eur J Clin Invest 30: 203-209, 2000.
12. ++ mechanisms defective in cholestasis. J Clin Invest 92: 2984-2993, 1993.
13. Beuers U, Probst I, Soroka C, Boyer JL, Kullak-Ublick GA, and Paumgartner G. Modulation of protein kinase C by taurolithocholic acid in isolated rat hepatocytes. Hepatology 29: 477-482, 1999.
14. Boulton TG, Nye SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, and Yancopoulos GD. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65: 663-675, 1991.
15. Brewster JL, de Valoir T, Dwyer ND, Winter E, and Gustin MC. An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763, 1993.
16. Craven PA, Pfanstiel J, Saito R, and DeRubertis FR. Relationship between loss of rat colonic surface epithelium induced by deoxycholate and initiation of the subsequent proliferative response. Cancer Res 46: 5754-5759, 1986.
17. Degott C, Zafrani ES, Callard P, Balkau B, Poupon RE, and Poupon R. Histopathological study of primary biliary cirrhosis and the effect of ursodeoxycholic acid treatment on histology progression. Hepatology 29: 1007-1012, 1999.
18. DeRubertis FR, Craven PA, and Saito R. Bile salt stimulation of colonic epithelial proliferation. Evidence for involvement of lipoxygenase products. J Clin Invest 74: 1614-1624, 1984.
19. Dugan LL, Kim JS, Zhang Y, Bart RD, Sun Y, Holtzman DM, and Gutmann DH. Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem 274: 25842-25848, 1999.
20. Ejiri S, Eguchi Y, Kishida A, Ishigami F, Kurumi Y, Tani T, and Kodama M. Cellular distribution of thrombomodulin as an early marker for warm ischemic liver injury in porcine liver transplantation: protective effect of prostaglandin I2 analogue and tauroursodeoxycholic acid. Transplantation 71: 721-726, 2001.
21. Evers BM, Gomez G, Townsend CM Jr, Rajaraman S, and Thompson JC. Endogenous cholecystokinin regulates growth of human cholangiocarcinoma. Ann Surg 210: 317-323, 1989.
22. Fernandez M, Sanchez-Franco F, Palacios N, Sanchez I, Villuendas G, and Cacicedo L. Involvement of vasoactive intestinal peptide on insulin-like growth factor I-induced proliferation of rat pituitary lactotropes in primary culture: evidence for an autocrine and/or paracrine regulatory system. Neuroendocrinology 77: 341-352, 2003.
23. Fletcher MS, Brinkley D, Dawson JL, Nunnerley H, and Williams R. Treatment of hilar carcinoma by bile drainage combined with internal radiotherapy using 192iridium wire. Br J Surg 70: 733-735, 1983.
24. Gauthier ML, Torretto C, Ly J, Francescutti V, and O'Day DH. Protein kinase Cα negatively regulates cell spreading and motility in MDA-MB-231 human breast cancer cells downstream of epidermal growth factor receptor. Biochem Biophys Res Commun 307: 839-846, 2003.
25. Glaser S, Alvaro D, Roskams T, Phinizy JL, Stoica G, Francis H, Ueno Y, Barbaro B, Marzioni M, Mauldin J, Rashid S, Mancino MG, LeSage G, and Alpini G. Dopaminergic inhibition of secretin-stimulated choleresis by increased PKC-γ expression and decrease of PKA activity. Am J Physiol Gastrointest Liver Physiol 284: G683-G694, 2003.
26. 2+-dependent PKC isoforms. Liver Int 23: 78-88, 2003.
27. Glaser S, Benedetti A, Marucci L, Alvaro D, Baiocchi L, Kanno N, Caligiuri A, Phinizy JL, Chowdury U, Papa E, LeSage G, and Alpini G. Gastrin inhibits cholangiocyte growth in bile duct-ligated rats by interaction with cholecystokinin-B/gastrin receptors via d-myo-inositol 1,4,5-triphosphate-, Ca(2+)-, and protein kinase C alpha-dependent mechanisms. Hepatology 32: 17-25, 2000.
28. Heathcote EJ. Management of primary biliary cirrhosis. The American Association for the Study of Liver Diseases practice guidelines. Hepatology 31: 1005-1013, 2000.
29. Higuchi H, Yoon JH, Grambihler A, Werneburg N, Bronk SF, and Gores GJ. Bile acids stimulate cFLIP phosphorylation enhancing TRAIL-mediated apoptosis. J Biol Chem 278: 454-461, 2003.
30. Hovis JG, Meyer T, Teasdale RM, Albrecht BN, Yorek MA, and Lowe WLJ. Intracellular calcium regulates insulin-like growth factor-I messenger ribonucleic acid levels. Endocrinology 132: 1931-1938, 1993.
31. Invernizzi P, Setchell KD, Crosignani A, Battezzati PM, Larghi A, O'Connell NC, and Podda M. Differences in the metabolism and disposition of ursodeoxycholic acid and of its taurine-conjugated species in patients with primary biliary cirrhosis. Hepatology 29: 320-327, 1999.
32. Jones BA, Rao YP, Stravitz RT, and Gores GJ. Bile salt-induced apoptosis of hepatocytes involves activation of protein kinase C. Am J Physiol Gastrointest Liver Physiol 272: G1109-G1115, 1997.
33. 2+-dependent protein kinase C-alpha. J Hepatol 34: 284-291, 2001.
34. Kanno N, LeSage G, Phinizy JL, Glaser S, Francis H, and Alpini G. Stimulation of alpha2-adrenergic receptor inhibits cholangiocarcinoma growth through modulation of Raf-1 and B-Raf activities. Hepatology 35: 1329-1340, 2002.
35. Kato A, Gores GJ, and LaRusso NF. Secretin stimulates exocytosis in isolated bile duct epithelial cells by a cyclic AMP-mediated mechanism. J Biol Chem 267: 15523-15529, 1992.
36. Knuth A, Gabbert H, Dippold W, Klein O, Sachsse W, Bitter-Suermann D, Prellwitz W, and Meyer zum Buschenfelde KH. Biliary adenocarcinoma. Characterisation of three new human tumor cell lines. J Hepatol 1: 579-596, 1985.
37. Kurino M, Fukunaga K, Ushio Y, and Miyamoto E. Cyclic AMP inhibits activation of mitogen-activated protein kinase and cell proliferation in response to growth factors in cultured rat cortical astrocytes. J Neurochem 67: 2246-2255, 1996.
38. Kurz AK, Block C, Graf D, Dahl SV, Schliess F, and Haussinger D. Phosphoinositide 3-kinase-dependent Ras activation by tauroursodeoxycholate in rat liver. Biochem J 350: 207-213, 2000.
39. Leirdal M and Sioud M. Protein kinase Ca isoform regulates the activation of the MAP kinase ERK1/2 in human glioma cells: involvement in cell survival and gene expression. Mol Cell Biol Res Commun 4: 106-110, 2000.
40. LeSage G, Glaser S, Ueno Y, Alvaro D, Baiocchi L, Kanno N, Phinizy JL, Francis H, and Alpini G. Regression of cholangiocyte proliferation after cessation of ANIT feeding is coupled with increased apoptosis. Am J Physiol Gastrointest Liver Physiol 281: G182-G190, 2001.
41. LeSage GD, Marucci L, Alvaro D, Glaser SS, Benedetti A, Marzioni M, Patel T, Francis H, Phinizy JL, and Alpini G. Insulin inhibits secretin-induced ductal secretion by activation of PKC alpha and inhibition of PKA activity. Hepatology 36: 641-651, 2002.
42. Marchesa P, Lashner BA, Lavery IC, Milsom J, Hull TL, Strong SA, Church JM, Navarro G, and Fazio VW. The risk of cancer and dysplasia among ulcerative colitis patients with primary sclerosing cholangitis. Am J Gastroenterol 92: 1285-1288, 1997.
43. Matsumura M, Tanaka N, Kuroki T, Ichihashi M, and Ohba M. The eta isoform of protein kinase C inhibits UV-induced activation of caspase-3 in normal human keratinocytes. Biochem Biophys Res Commun 303: 350-356, 2003.
44. Matsuzaki Y, Bouscarel B, Le M, Ceryak S, Gettys TW, Shoda J, and Fromm H. Effect of cholestasis on regulation of cAMP synthesis by glucagon and bile acids in isolated hepatocytes. Am J Physiol Gastrointest Liver Physiol 273: G164-G174, 1997.
45. McConkey DJ, Orrenius S, and Jondal M. Agents that elevate cAMP stimulate DNA fragmentation in thymocytes. J Immunol 145: 1227-1230, 1990.
46. McGarrity TJ, Pfeiffer LP, Neely EB, Palavarapu RG, Koltun WA, Parker P, and Howett MK. Localization of protein kinase C alpha isoform expression in the human gastrointestinal tract. Cell Growth Differ 7: 953-959, 1996.
47. Mellor H and Parker PJ. The extended protein kinase C superfamily. Biochem J 332: 281-292, 1998.
48. Milkiewicz P, Roma MG, Cardenas R, Mills CO, Elias E, and Coleman R. Effect of tauroursodeoxycholate and S-adenosyl-1-methionine on 17β-estradiol glucuronide-induced cholestasis. J Hepatol 34: 184-191, 2001.
49. Milovic V, Teller IC, Faust D, Caspary WF, and Stein J. Effects of deoxycholate on human colon cancer cells: apoptosis or proliferation. Eur J Clin Invest 32: 29-34, 2002.
50. Pongracz J, Clark P, Neoptolemos JP, and Lord JM. Expression of protein kinase C isoenzymes in colorectal cancer tissue and their differential activation by different bile acids. Int J Cancer 61: 35-39, 1995.
51. Poo JL, Feldmann G, Erlinger S, Braillon A, Gaudin C, Dumont M, and Lebrec D. Ursodeoxycholic acid limits liver histologic alterations and portal hypertension induced by bile duct ligation in the rat. Gastroenterology 102: 1752-1759, 1992.
52. Poupon RE, Poupon R, and Balkau B. Ursodiol for the long-term treatment of primary biliary cirrhosis. N Engl J Med 330: 1342-1347, 1994.
53. Rao YP, Studer EJ, Stravitz RT, Gupta S, Qiao L, Dent P, and Hylemon PB. Activation of the Raf-1/MEK/ERK cascade by bile acids occurs via the epidermal growth factor receptor in primary rat hepatocytes. Hepatology 35: 307-314, 2002.
54. Reyland ME, Barzen KA, Anderson SM, Quissell DO, and Matassa AA. Activation of PKC is sufficient to induce an apoptotic program in salivary acinar cells. Cell Death Differ 7: 1200-1209, 2002.
55. Rudolph G, Endele R, Senn M, and Stiehl A. Effect of ursodeoxycholic acid on the kinetics of cholic acid and chenodeoxycholic acid in patients with primary sclerosing cholangitis. Hepatology 17: 1028-1032, 1993.
56. Rumalla A, Baron TH, Wang KK, Gores GJ, Stadheim LM, and de Groen PC. Endoscopic application of photodynamic therapy for cholangiocarcinoma. Gastrointest Endosc 53: 500-504, 2001.
57. Sampson LK, Vickers SM, Ying W, and Phillips JO. Tamoxifen-mediated growth inhibition of human cholangiocarcinoma. Cancer Res 57: 1743-1749, 1997.
58. Shekels LL, Beste JE, and Ho SB. Tauroursodeoxycholic acid protects in vitro models of human colonic cancer cells from cytotoxic effects of hydrophobic bile acids. J Lab Clin Med 127: 57-66, 1996.
59. Sirica AE, Lai GH, Endo K, Zhang Z, and Yoon BI. Cyclooxygenase-2 and ERBB-2 in cholangiocarcinoma: potential therapeutic targets. Semin Liver Dis 22: 303-313, 2002.
60. Smeal T, Binetruy B, Mercola D, Grover BA, Heldecker G, Rapp UR, and Karin M. Oncoprotein-mediated signaling cascade stimulates c-Jun activity by phosphorylation of serines 63 and 73. Mol Cell Biol 12: 3507-3513, 1992.
61. Tan CK, Podila PV, Taylor JE, Nagorney DM, Wiseman GA, Gores GJ, and LaRusso NF. Human cholangiocarcinomas express somatostatin receptors and respond to somatostatin with growth inhibition. Gastroenterology 108: 1908-1916, 1995.
62. Thuluvath PJ, Rai R, Venbrux AC, and Yeo CJ. Cholangiocarcinoma: a review. Gastroenterologist 5: 306-315, 1997.
63. Tsukahara K, Kanai S, Ohta M, and Kitani K. Taurine conjugate of ursodeoxycholate plays a major role in the hepatoprotective effect against cholestasis induced by taurochenodeoxycholate in rats. Liver 13: 262-269, 1993.
64. Vossler MR, Yao H, York RD, Pan MG, Rim CS, and Stork PJ. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rapl-dependent pathway. Cell 89: 73-82, 1997.
65. Yamaguchi T, Nagao S, Wallace DP, Belibi FA, Cowley BD, Pelling JC, and Grantham JJ. Cyclic AMP activates B-Raf and ERK in cyst epithelial cells from autosomal-dominant polycystic kidneys. Kidney Int 63: 1983-1994, 2003.
66. Yoon YM, Kim SJ, Oh CD, Ju JW, Song WK, Yoo YJ, Huh TL, and Chun JS. Maintenance of differentiated phenotype of articular chondrocytes by protein kinase C and extracellular signal-regulated protein kinase. J Biol Chem 277: 8412-8420, 2002.
67. Zhang F, Subbaramaiah K, Altorki N, and Dannenberg AJ. Dihydroxy bile acids activate the transcription of cyclooxygenase-2. J Biol Chem 23: 2424-2428, 1998.
68. Zheng C, Xiang J, Hunter T, and Lin A. The JNKK2-JNK1 fusion protein acts as a constitutively active c-Jun kinase that stimulates c-Jun transcription activity. J Biol Chem 274: 28966-28971, 1990.