Deoxycholyltaurine rescues human colon cancer cells from apoptosis by activating EGFR-dependent PI3K/Akt signaling

Journal of Cellular Physiology

Volumn 215, Issue 2, 2008, Pages 538-549

  Raufman, Jean Pierre ^a   Shant, Jasleen ^a   Chang, Yue Guo ^a   Roy, Sanjit ^a   Cheng, Kunrong ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARAMYOSIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN KINASE B; SERINE; TAURODEOXYCHOLIC ACID; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER PREVENTION; CELL ACTIVATION; CELL PROLIFERATION; CELL PROTECTION; CELL STIMULATION; CELL STRAIN HT29; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME SUBSTRATE; GENETIC TRANSFECTION; HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL DETECTION; COLON TUMOR; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; ENZYME ACTIVATION; HUMANS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TAURODEOXYCHOLIC ACID; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 40949163839     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21332     Document Type: Article

References (62)

1. Alberts DS, Martinez ME, Hess LM, Einspahr JG, Green SB, Bhattacharyya AK, Guillen J, Krutzsch M, Batta AK, Salen G, Fales L, Koonce K, Parish D, Clouser M, Roe D, Lance P. 2005. Phase III trial of ursodeoxycholic acid to prevent colorectal adenoma recurrence. J Natl Cancer Inst 97:846-853.
2. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15:6541-6551.
3. Bellacosa A, Kumar CC, Di Cristofano A, Testa JR. 2005. Activation of AKT kinases in cancer: Implications for therapeutic targeting. Adv Cancer Res 94:29-86.
4. Castro RE, Amaral JD, Sola S, Kren BT, Steer C, Rodrigues CM. 2007. Differential regulation of cyclin D1 and cell death by bile acids in primary rat hepatocytes. Am J Physiol Gastrointest Liver Physiol 293:G327-G334.
5. Cheng K, Koland JG. 1998. Nucleotide-binding properties of kinase-deficient epidermal-growth-factor-receptor mutants. Biochem J 330:353-359.
6. Cheng K, Raufman JP. 2005. Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors. Biochem Pharmacol 70:1035-1047.
7. Cheng K, Chen Y, Zimniak P, Raufman J, Xiao Y, Frucht H. 2002. Functional interaction of lithocholic acid conjugates with M3 muscarinic receptors on a human colon cancer cell line. Biochim Biophys Acta 1588:48-55.
8. Cheng K, Zimniak P, Raufman JP. 2003. Transactivation of the epidermal growth factor receptor mediates cholinergic agonist-induced proliferation of H508 human colon cancer cells. Cancer Res 63:6744-6750.
9. Cheng K, Xie G, Raufman JP. 2007. Matrix metalloproteinase-7-catalyzed release of HB-EGF mediates deoxycholyltaurine-induced proliferation of a human colon cancer cell line. Biochem Pharmacol 73:1001-1012.
10. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
11. Datta SR, Brunet A, Greenberg ME. 1999. Cellular survival: A play in three Akts. Genes Dev 13:2905-2927.
12. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
13. Dent P, Fang Y, Gupta S, Studer E, Mitchell C, Spiegel S, Hylemon PB. 2005. Conjugated bile acids promote ERK1/2 and AKT activation via a pertussis toxin-sensitive mechanism in murine and human hepatocytes. Hepatology 42:1291-1299.
14. Diehl JA, Cheng M, Roussel MF, Sherr CJ. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12:3499-3511.
15. Earnest DL, Holubec H, Wali RK, Jolley CS, Bissonette M, Bhattacharyya AK, Roy H, Khare S, Brasitus TA. 1994. Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res 54:5071-5074.
16. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. 2007. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 282:11221-11229.
17. Fruman DA, Meyers RE, Cantley LC. 1998. Phosphoinositide kinases. Annu Rev Biochem 67:481-507.
18. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, Waterfield MD. 2007. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J 404:15-21.
19. Glinghammar B, Rafter J. 1999. Carcinogenesis in the colon: Interaction between luminal factors and genetic factors. Eur J Cancer Prev 8:587-594.
20. Glinghammar B, Inoue H, Rafter JJ. 2002. Deoxycholic acid causes DNA damage in colonic cells with subsequent induction of caspases, COX-2 promoter activity and the transcription factors NF-kB and AP-1. Carcinogenesis 23:839-845.
21. Gould KA, Dove WF. 1996. Action of Min and Mom1 on neoplasia in ectopic intestinal grafts. Cell Growth Differ 7:1361-1368.
22. Green DR, Evan GI. 2002. A matter of life and death. Cancer Cell 1:19-30.
23. Guo C, Raufman J-P. 2006. Bile acids activate epidermal growth factor receptor (EGFR) kinase-dependent phosphatidylinositol 3kinase (PI3K)/Akt proliferative signaling in colon cancer cells. Gastroenterology 130:A119.
24. Hamilton JP, Xie G, Raufman JP, Hogan S, Griffin TL, Packard CA, Chatfield DA, Hagey LR, Steinbach JH, Hofmann AF. 2007. Human cecal bile acids: Concentration and spectrum. Am J Physiol Gastrointest Liver Physiol 293:G256-G263.
25. Haridas V, Darnay BG, Natarajan K, Heller R, Aggarwal BB. 1998. Overexpression of the p80 TNF receptor leads to TNF-dependent apoptosis, nuclear factor-kappa B activation, and c-Jun kinase activation. J Immunol 160:3152-3162.
26. Hofmann AF, Sjovall J, Kurz G, Radominska A, Schteingart CD, Tint GS, Valacevic ZR, Setchell DR. 1992. A proposed nomenclature for bile acids. J Lipid Res 33:599-604.
27. Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, Kothari N, Natesan S, Brugge JS. 2005. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol 171:1023-1034.
28. Janes KA, Gaudet S, Albeck JG, Nielsen UB, Lauffenburger DA, Sorger PK. 2006. The response of human epithelial cells to TNF involves an inducible autocrine cascade. Cell 124:1225-1239.
29. Jean-Louis S, Akare S, Ali MA, Mash EA, Jr., Meuillet E, Martinez JD. 2006. Deoxycholic acid induces intracellular signaling through membrane perturbations. J Biol Chem 281:14948-14960.
30. Jobin C, Sartor RB. 2000. The I kappa B/NF-kappa B system: A key determinant of mucosalinflammation and protection. Am J Physiol Cell Physiol 278:C451-C462.
31. Karin M. 2006. Nuclear factor-kappaB in cancer development and progression. Nature 441:431-436.
32. Karin M, Lin A. 2002. NF-kappaB at the crossroads of life and death. Nat Immunol 3:221-227.
33. Kinzler DW, Vogelstein B. 1996. Lessons from hereditary colorectal cancer. Cell 87: 159-170.
34. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Li J, Mizukami Y, Zhang X, Jo WS, Chung DC. 2005. Oncogenic K-ras stimulates Wnt signaling in colon cancer through inhibition of GSK-3beta. Gastroenterology 128:1907-1918.
36. Manna SK, Aggarwal BB. 2000. All-trans-retinoic acid upregulates TNF receptors and potentiates TNF-induced activation of nuclear factors-kappaB, activated protein-1 and apoptosis in human lung cancer cells. Oncogene 19:2110-2119.
37. Marasa BS, Rao JN, Zou T, Liu L, Keledjian KM, Zhang AH, Xiao L, Chen J, Turner DJ, Wang JY. 2006. Induced TRPC1 expression sensitizes intestinal epithelial cells to apoptosis by inhibiting NF-kappaB activation through Ca2+ influx. Biochem J 397:77-87.
38. Martinez JD, Stratagoules ED, LaRue JM, Powell AA, Gause PR, Craven MT, Payne CM, Powell MB, Gerner EW, Earnest DL. 1998. 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 31:111-118.
39. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. 2006. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21:749-760.
40. Merchant NB, Rogers CM, Trivedi B, Morrow J, Coffey RJ. 2005. Ligand-dependent activation of the epidermal growth factor receptor by secondary bile acids in polarizing colon cancer cells. Surgery 138:415-421.
41. Milovic V, Teller IC, Faust D, Caspary WF, Stein J. 2002. Effects of deoxycholate on human colon cancer cells: Apoptosis or proliferation. Eur J Clin Invest 32:29-34.
42. Nagengast FM, Grubben MJAL, van Munster IP. 1995. Role of bile acids in colorectal carcinogenesis. Eur J Cancer 31A:1067-1070.
43. Narisawa T, Magadia NE, Weisburger JH, Wynder EL. 1974. Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of N-methyl-N′-nitro-N-nitrosoguanidine in rats. J Natl Cancer Inst 53:1093-1097.
44. Narisawa T, Fukaura Y, Terada K, Sekiguchi H. 1998. Prevention of N-methylnitrosourea-induced colon tumorigenesis by ursodeoxycholic acid in F344 rats. Jpn J Cancer Res 89:1009-1013.
45. Pai R, Tarnawski AS, Tran T. 2004. Deoxycholic acid activates beta-catenin signaling pathway and increases colon cell cancer growth and invasiveness. Mol Biol Cell 15:2156-2163.
46. Pardi DS, Loftus EV, Jr., Kremers WK, Keach J, Lindor KD. 2003. Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis. Gastroenterology 124:889-893.
47. Parsons DW, Wang TL, Samuels Y, Bardelli A, Cummins JM, DeLong L, Silliman N, Ptak J, Szabo S, Willson JK, Markowitz S, Kinzler KW, Vogelstein B, Lengauer C, Velculescu VE. 2005. Colorectal cancer: Mutations in a signalling pathway. Nature 436:792.
48. Radeff-Huang J, Seasholtz TM, Chang JW, Smith JM, Walsh CT, Brown JH. 2007. Tumor necrosis factor-alpha-stimulated cell proliferation is mediated through sphingosine kinase-dependent Akt activation and cyclin D expression. J Biol Chem 282:863-870.
49. Reddy BS, Narasawa T, Weisburger JH, Wynder EL. 1976. Promoting effect of sodium deoxycholate on colon adenocarcinomas in germfree rats. J Natl Cancer Inst 56:441-442.
50. Roberts RB, Min L, Washington MK, Olsen SJ, Settle SH, Coffey RJ, Threadgill DW. 2002. Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proc Natl Acad Sci USA 99:1521-1526.
51. Rust C, Karnitz LM, Paya CV, Moscat J, Simari RD, Gores GJ. 2000. The bile acid taurochenodeoxycholate activates a phosphatidylinositol 3-kinase-dependent survival signaling cascade. J Biol Chem 275:20210-20216.
52. Sastry KS, Karpova Y, Prokopovich S, Smith AJ, Essau B, Gersappe A, Carson JP, Weber MJ, Register TC, Chen YQ, Penn RB, Kulik G. 2007. Epinephrine Protects Cancer Cells from Apoptosis via Activation of cAMP-dependent Protein Kinase and BAD Phosphorylation. J Biol Chem 282:14094-14100.
53. Schlottman K, Wachs FP, Krieg RC, Kullmann F, Scholmerich J, Rogler G. 2000. Characterization of bile salt-induced apoptosis in colon cancer cell lines. Cancer Res 60:4270-4276.
54. Shaw RJ, Cantley LC. 2006. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441:424-430.
55. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR. 1990. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82:1107-1112.
56. Song G, Ouyang G, Bao S. 2005. The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9:59-71.
57. Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, Kogan S, Cordon-Cardo C, Pelletier J, Lowe SW. 2004. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428:332-337.
58. Wennstrom S, Downward J. 1999. Role of phosphoinositide 3-kinase in activation of ras and mitogen-activated protein kinase by epidermal growth factor. Mol Cell Biol 19:4279-4288.
59. Woodgett JR. 2005. Recent advances in the protein kinase B signaling pathway. Curr Opin Cell Biol 17:150-157.
60. Yao R, Cooper GM. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003-2006.
61. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87:619-628.
62. Zhang HM, Rao JN, Guo X, Liu L, Zou T, Turner DJ, Wang JY. 2004. Akt kinase activation blocks apoptosis in intestinal epithelial cells by inhibiting caspase-3 after polyamine depletion. J Biol Chem 279:22539-22547.