Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors

Biochemical Pharmacology

Volumn 70, Issue 7, 2005, Pages 1035-1047

  Cheng, Kunrong ^a   Raufman, Jean Pierre ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine; Bile acids; Colon cancer; Epidermal growth factor receptor; Muscarinic receptors; Proliferation; Signal transduction

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ATROPINE; BILE ACID; BILE ACID CONJUGATE; CASPASE 3; DEOXYCHOLIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCINE; LITHOCHOLIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC M3 RECEPTOR; TAURINE; TYROSINE;

AGONIST; APOPTOSIS; ARTICLE; BILE ACID SYNTHESIS; CANCER CELL CULTURE; CELL PROLIFERATION; CELL STRAIN; CHOLINERGIC ACTIVITY; COLON CARCINOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG RECEPTOR BINDING; HUMAN; HUMAN CELL; LIVER CELL CULTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ACETYLCHOLINE; BILE ACIDS AND SALTS; CASPASE 3; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS);

EID: 24344479257     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.07.023     Document Type: Article

References (71)

1. D.W. Kinzler, and B. Vogelstein Lessons from hereditary colorectal cancer Cell 87 1996 159 170
2. J.R. Jass, V.L. Whitehall, J. Young, and B.A. Leggett Emerging concepts in colorectal neoplasia Gastroenterology 123 2002 862 876
3. M.J. Hill, B.S. Drasar, R.E. Williams, T.W. Meade, A.G. Cox, and J.E. Simpson Faecal bile-acids and clostridia in patients with cancer of the large bowel Lancet 1 1975 535 539
4. B.S. Reddy, and E.L. Wynder Metabolic epidemiology of colon cancer. Fecal bile acids and neutral sterols in colon cancer patients and patients with adenomatous polyps Cancer 39 1977 2533 2539
5. M.J. Hill Bile acids and colorectal cancer: hypothesis Eur J Cancer Prev 1 1991 69 74
6. B. Glinghammar, and J. Rafter Carcinogenesis in the colon: interaction between luminal factors and genetic factors Eur J Cancer Prev 8 1999 S87 S94
7. P. Lichtenstein, N.V. Holm, P.K. Verkasalo, A. Iliadou, J. Kaprio, and Koskenvuo Environmental and heritable factors in the causation of cancer N Engl J Med 343 2000 78 85
8. K.A. Gould, and W.F. Dove Action of Min and Mom1 on neoplasia in ectopic intestinal grafts Cell Growth Differ 7 1996 1361 1368
9. A.F. Hofmann, J. Sjovall, G. Kurz, A. Radominska, C.D. Schteingart, and G.S. Tint A proposed nomenclature for bile acids J Lipid Res 33 1992 599 604
10. T. Narisawa, N.E. Magadia, J.H. Weisburger, and E.L. Wynder Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of N-methyl-N′-nitro-N-nitrosoguanidine in rats J Natl Cancer Instit 53 1974 1093 1097
11. B.S. Reddy, T. Narasawa, J.H. Weisburger, and E.L. Wynder Promoting effect of sodium deoxycholate on colon adenocarcinomas in germfree rats J Natl Cancer Instit 56 1976 441 442
12. F.M. Nagengast, M.J.A.L. Grubben, and I.P. van Munster Role of bile acids in colorectal carcinogenesis Eur J Cancer 31A 1995 1067 1070
13. D.L. Earnest, H. Holubec, R.K. Wali, C.S. Jolley, M. Bissonette, and A.K. Bhattacharyya Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid Cancer Res 54 1994 5071 5074
14. T. Narisawa, Y. Fukaura, K. Terada, and H. Sekiguchi Prevention of N-methylnitrosourea-induced colon tumorigenesis by ursodeoxycholic acid in F344 rats Jpn J Cancer Res 89 1998 1009 1013
15. D.S. Pardi, E.V. Loftus Jr., W.K. Kremers, J. Keach, and K.D. Lindor Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis Gastroenterology 124 2003 889 893
16. J.D. Martinez, E.D. Stratagoules, J.M. LaRue, A.A. Powell, P.R. Gause, and M.T. Craven Different bile acids exhibit distinct biological effects: the tumor promoter deoxycholic acid induces apoptosis and the chemopreventive agent ursodeoxycholic acid inhibits cell proliferation Nutr Cancer 31 1998 111 118
17. D. Qiao, W. Chen, E.D. Stratagoules, and J.D. Martinez Bile acid-induced activation of activator protein-1 requires both extracellular signal-regulated kinase and protein kinase C signaling J Biol Chem 275 2000 15090 15098
18. D. Qiao, S.V. Gaitonde, W. Qi, and J.D. Martinez Deoxycholic acid suppresses p53 by stimulating proteasome-mediated p53 protein degradation Carcinogenesis 22 2001 957 964
19. D. Qiao, E.D. Stratagouleas, and J.D. Martinez Activation and role of mitogen-activated protein kinases in deoxycholic acid-induced apoptosis Carcinogenesis 22 2001 35 41
20. N.W. Werneburg, J.H. Yoon, H. Higuchi, and G.J. Gores Bile acids activate EGF receptor via a TGF-alpha-dependent mechanism in human cholangiocyte cell lines Am J Physiol Gastrointest Liver Physiol 285 2003 G31 G36
21. R.B. Roberts, L. Min, M.K. Washington, S.J. Olsen, S.H. Settle, and R.J. Coffey Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis Proc Natl Acad Sci USA 99 2002 1521 1526
22. O.M. Fischer, S. Hart, A. Gschwind, and A. Ullrich EGFR signal transactivation in cancer cells Biochem Soc Trans 31 2003 1203 1208
23. E. Im, and J.D. Martinez Ursodeoxycholic acid (UDCA) can inhibit deoxycholic acid (DCA)-induced apoptosis via modulation of EGFR/Raf-1/ERK signaling in human colon cancer cells J Nutr 134 2004 483 486
24. J.P. Raufman, P. Zimniak, and A. Bartoszko-Malik Lithocholyltaurine interacts with cholinergic receptors on dispersed chief cells from guinea pig stomach Am J Physiol 274 1998 G997 G1004
25. J.P. Raufman, K. Cheng, and P. Zimniak Activation of muscarinic receptor signaling by bile acids: physiological and medical implications Dig Dis Sci 48 2003 1431 1444
26. H. Frucht, A.F. Gazdar, J-A. Park, H. Oie, and R.T. Jensen Characterization of functional receptors for gastrointestinal hormones on human colon cancer cells Cancer Res 52 1992 1114 1122
27. H. Frucht, R.T. Jensen, D. Dexter, W-L. Yang, and Y. Xiao Human colon cancer cell proliferation mediated by the M3 muscarinic cholinergic receptor Clin Cancer Res 5 1999 2532 2539
28. W.L. Yang, and H. Frucht Cholinergic receptor up-regulates COX-2 expression and prostaglandin E(2) production in colon cancer cells Carcinogenesis 21 2000 1789 1793
29. K. Cheng, Y. Chen, P. Zimniak, J. Raufman, Y. Xiao, and H. Frucht Functional interaction of lithocholic acid conjugates with M3 muscarinic receptors on a human colon cancer cell line Biochim Biophys Acta 1588 2002 48 55
30. H. Daub, F.U. Weiss, C. Wallasch, and A. Ullrich Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors Nature 379 1996 557 560
31. L.M. Luttrell, G.J. Della Rocca, T. van Biesen, D.K. Luttrell, and R.J. Lefkowitz Gbetagamma subunits mediate Src-dependent phosphorylation of the epidermal growth factor receptor. A scaffold for G protein-coupled receptor-mediated Ras activation J Biol Chem 272 1997 4637 4644
32. 3 muscarinic acetylcholine receptor is coupled to mitogen-activated protein kinase via protein kinase C and epidermal growth factor receptor kinase Biochem J 348 Pt 2 2000 381 387
33. S.J. Keely, J.M. Uribe, and K.E. Barrett Carbachol stimulates transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T84 cells. Implications for carbachol-stimulated chloride secretion J Biol Chem 273 1998 27111 27117
34. S.J. Keely, S.O. Calandrella, and K.E. Barrett Carbachol-stimulated transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T(84) cells is mediated by intracellular ca(2+), PYK-2, and p60(src) J Biol Chem 275 2000 12619 12625
35. K. Cheng, P. Zimniak, and J.P. Raufman Transactivation of the epidermal growth factor receptor mediates cholinergic agonist-induced proliferation of H508 human colon cancer cells Cancer Res 63 2003 6744 6750
36. J.I. Ukegawa, Y. Takeuchi, S. Kusayanagi, and K. Mitamura Growth-promoting effect of muscarinic acetylcholine receptors in colon cancer cells J Cancer Res Clin Oncol 129 2003 272 278
37. K. Cheng, S. Khurana, Y. Chen, R.H. Kennedy, P. Zimniak, and J.P. Raufman Lithocholylcholine, a bile acid/acetylcholine hybrid, is a muscarinic receptor antagonist J Pharmacol Exp Ther 303 2002 29 35
38. 3 muscarinic acetylcholine receptors. Evidence for involvement of tyrosine phosphorylation Eur J Biochem 225 1994 667 675
39. D.C. Heimbrook, S.M. Stirdivant, J.D. Ahern, N.L. Balishin, D.R. Patrick, and G.M. Edwards Transforming growth factor alpha-Pseudomonas exotoxin fusion protein prolongs survival of nude mice bearing tumor xenografts Proc Natl Acad Sci USA 87 1990 4697 4701
40. P. Skehan, R. Storeng, D. Scudiero, A. Monks, J. McMahon, and D. Vistica New colorimetric cytotoxicity assay for anticancer-drug screening J Natl Cancer Instit 82 1990 1107 1112
41. M. Frodin, and S. Gammeltoft Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction Mol Cell Endocrinol 151 1999 65 77
42. C. Klos, G. Paumgartner, and J. Reichen Cation-anion gap and choleretic properties of rat bile Am J Physiol 236 1979 E434 E440
43. J.M. Pries, C.A. Sherman, G.C. Williams, and R.F. Hanson Hepatic extraction of bile salts in conscious dog Am J Physiol 236 1979 E191 E197
44. G. Alpini, S.S. Glaser, Y. Ueno, R. Rodgers, J.L. Phinizy, and H. Francis Bile acid feeding induces cholangiocyte proliferation and secretion: evidence for bile acid-regulated ductal secretion Gastroenterology 116 1999 179 186
45. J.P. Raufman, Y. Chen, K. Cheng, C. Compadre, L. Compadre, and P. Zimniak Selective interaction of bile acids with muscarinic receptors: a case of molecular mimicry Eur J Pharmacol 457 2002 77 84
46. J.P. Raufman, Y. Chen, P. Zimniak, and K. Cheng Deoxycholic acid conjugates are muscarinic cholinergic receptor antagonists Pharmacology 65 2002 215 221
47. R. Reinehr, D. Graf, and D. Haussinger Bile salt-induced hepatocyte apoptosis involves epidermal growth factor receptor-dependent CD95 tyrosine phosphorylation Gastroenterology 125 2003 839 853
48. A. Levitzki, and A. Gazit Tyrosine kinase inhibition: an approach to drug development Science 267 1995 1782 1788
49. D.W. Fry, A.J. Bridges, W.A. Denny, A. Doherty, K.D. Greis, and J.L. Hicks Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor Proc Natl Acad Sci USA 95 1998 12022 12027
50. G.W. Rewcastle, D.K. Murray, W.L. Elliott, D.W. Fry, C.T. Howard, and J.M. Nelson Tyrosine kinase inhibitors. 14. Structure-activity relationships for methylamino-substituted derivatives of 4-[(3-bromophenyl)amino]-6-(methylamino) -pyrido[3,4-d]pyrimidine (PD 158780), a potent and specific inhibitor of the tyrosine kinase activity of receptors for the EGF family of growth factors J Med Chem 41 1998 742 751
51. D. Rotin, B. Margolis, M. Mohammadi, R.J. Daly, G. Daum, and N. Li SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma Embo J 11 1992 559 567
52. M.A. Olayioye, R.M. Neve, H.A. Lane, and N.E. Hynes The ErbB signaling network: receptor heterodimerization in development and cancer Embo J 19 2000 3159 3167
53. L.M. Sturla, G. Amorino, M.S. Alexander, R.B. Mikkelsen, K. Valerie, and R.K. Schmidt-Ullrichr Requirement of Tyr-992 and Tyr-1173 in Phosphorylation of the epidermal growth factor receptor by ionizing radiation and modulation by SHP2 J Biol Chem 280 2005 14597 14604
54. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
55. Y. Yarden, and M.X. Sliwkowski Untangling the ErbB signalling network Nat Rev Mol Cell Biol 2 2001 127 137
56. V.E. Sutliff, S. Rattan, J.D. Gardner, and R.T. Jensen Characterization of cholinergic receptors mediating pepsinogen secretion from chief cells Am J Physiol 257 1989 G226 G234
57. Q.A. Justman, and G.M. Clinton Herstatin, an autoinhibitor of the human epidermal growth factor receptor 2 tyrosine kinase, modulates epidermal growth factor signaling pathways resulting in growth arrest J Biol Chem 277 2002 20618 20624
58. R. Radinsky, Risin, Fan, Dong, Bielenberg, C.D. Bucana, and J. Fidler Level and function of epidermal growth factor receptor predict the metastatic potential of human colon carcinoma cells Clin Cancer Res 1 1995 19 31
59. C. Parker, B.J. Roseman, C.D. Bucana, R. Tsan, and R. Radinsky Preferential activation of the epidermal growth factor receptor in human colon carcinoma liver metastases in nude mice J Histochem Cytochem 46 1998 595 602
60. S.B. Noonberg, and C.C. Benz Tyrosine kinase inhibitors targeted to the epidermal growth factor receptor subfamily: role as anticancer agents Drugs 59 2000 753 767
61. R.L. Patterson, D.B. van Rossum, D.L. Ford, K.J. Hurt, S.S. Bae, and P.G. Suh Phospholipase C-gamma is required for agonist-induced Ca2+ entry Cell 111 2002 529 541
62. R.C. Harris, E. Chung, and R.J. Coffey EGF receptor ligands Exp Cell Res 284 2003 2 13
63. R.N. Jorissen, F. Walker, N. Pouliot, T.P. Garrett, C.W. Ward, and A.W. Burgess Epidermal growth factor receptor: mechanisms of activation and signalling Exp Cell Res 284 2003 31 53
64. J.R. Poley, and A.F. Hofmann Role of fat maldigestion in pathogenesis of steatorrhea in ileal resection Gastroenterology 71 1976 38 44
65. M. Makishima, A.Y. Okamoto, J.J. Repa, H. Tu, R.M. Learned, and A. Luk Identification of a nuclear receptor for bile acids Science 284 1999 1362 1365
66. D.J. Parks, S.G. Blanchard, R.K. Bledsoe, G. Chandra, T.G. Consler, and S.A. Kliewer Bile acids: natural ligands for an orphan nuclear receptor Science 284 1999 1365 1368
67. M. Makishima, T. Lu, W. Xie, G. Whitfield, H. Domoto, and R. Evans Vitamin D receptor as an intestinal bile acid sensor Science 296 2002 1313 1316
68. S. Winawer, R. Fletcher, D. Rex, J. Bond, R. Burt, and J. Ferrucci Colorectal cancer screening and surveillance: clinical guidelines and rationale-update based on new evidence Gastroenterology 124 2003 544 560
69. A.P. Soler, R.D. Miller, K.V. Laughlin, N.Z. Carp, D.M. Klurfeld, and J.M. Mullin Increased tight junctional permeability is associated with the development of colon cancer Carcinogenesis 20 1999 1425 1431
70. C.L. Wilson, K.J. Heppner, P.A. Labosky, B.L. Hogan, and L.M. Matrisian Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin Proc Natl Acad Sci USA 94 1997 1402 1407
71. P.K. Baijal, D.W. Fitzpatrick, and R.P. Bird Comparative effects of secondary bile acids, deoxycholic and lithocholic acids, on aberrant crypt foci growth in the postinitiation phases of colon carcinogenesis Nutr Cancer 31 1998 81 89