Ca2+-Dependent K+ Efflux Regulates Deoxycholate-Induced Apoptosis of BHK-21 and Caco-2 Cells

Gastroenterology

Volumn 137, Issue 3, 2009, Pages

  Gerbino, Andrea ^a   Ranieri, Marianna ^a   Lupo, Stefania ^a   Caroppo, Rosa ^a   Debellis, Lucantonio ^a   Maiellaro, Isabella ^a   Caratozzolo, Mariano F ^b   Lopez, Francesco ^c   Colella, Matilde ^a  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF MOLISE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BILE SALT; CALCIUM ION; CALCIUM IONOPHORE; CASPASE 3; CASPASE 7; DEOXYCHOLIC ACID; POTASSIUM ION; PROPIDIUM IODIDE; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATE; APAMIN; BRADYKININ; CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CHARYBDOTOXIN; CHELATING AGENT; CYCLOPIAZONIC ACID; DRUG DERIVATIVE; EGTAZIC ACID; INDOLE DERIVATIVE; POTASSIUM; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL MEMBRANE; CELL STRAIN BHK; CELL STRAIN CACO 2; COLON CARCINOMA; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MICROELECTRODE; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; ANIMAL; CELL LINE; CELL MEMBRANE POTENTIAL; CYTOSOL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; EXTRACELLULAR SPACE; FIBROBLAST; HAMSTER; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; APAMIN; APOPTOSIS; BRADYKININ; CACO-2 CELLS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CASPASE 3; CASPASE 7; CELL LINE; CHARYBDOTOXIN; CHELATING AGENTS; CRICETINAE; CYTOSOL; DEOXYCHOLIC ACID; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; EXTRACELLULAR SPACE; FIBROBLASTS; HUMANS; INDOLES; MEMBRANE POTENTIALS; MICROELECTRODES; POTASSIUM; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 69249213875     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2009.03.038     Document Type: Article

References (52)

1. Hofmann A.F. The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159 (1999) 2647-2658
2. Zhou J., Liu M., Zhai Y., et al. The anti-apoptotic role of pregnane X receptor in human colon cancer cells. Mol Endocrinol 22 (2007) 868-880
3. Reddy B.S., and Watanabe K. Effect of cholesterol metabolites and promoting effect of lithocholic acid in colon carcinogenesis in germ-free and conventional F344 rats. Cancer Res 39 (1979) 1521-1524
4. Bernstein H., Bernstein C., Payne C.M., et al. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 589 (2005) 47-65
5. Bernstein C., Bernstein H., Garewal H., et al. A bile acid-induced apoptosis assay for colon cancer risk and associated quality control studies. Cancer Res 59 (1999) 2353-2357
6. Bernstein H., Holubec H., Warneke J.A., et al. Patchy field defects of apoptosis resistance and dedifferentiation in flat mucosa of colon resections from colon cancer patients. Ann Surg Oncol 9 (2002) 505-517
7. Crowley-Weber C.L., Payne C.M., Gleason-Guzman M., et al. Development and molecular characterization of HCT-116 cell lines resistant to the tumor promoter and multiple stress-inducer, deoxycholate. Carcinogenesis 23 (2002) 2063-2080
8. Qiao D., Stratagouleas E.D., and Martinez J.D. Activation and role of mitogen-activated protein kinases in deoxycholic acid-induced apoptosis. Carcinogenesis 22 (2001) 35-41
9. Milovic V., Teller I.C., Murphy G.M., et al. Deoxycholic acid stimulates migration in colon cancer cells. Eur J Gastroenterol Hepatol 13 (2001) 945-949
10. Cheng K., Xie G., and Raufman J.P. Matrix metalloproteinase-7-catalyzed release of HB-EGF mediates deoxycholyltaurine-induced proliferation of a human colon cancer cell line. Biochem Pharmacol 73 (2007) 1001-1012
11. Raufman, Jean-Pierre J.S., Chang Yue G., et al. Deoxycholyltaurine rescues human colon cancer cells from apoptosis by activating EGFR-dependent PI3K/Akt signaling. J Cell Physiol 215 (2008) 538-549
12. Lau B.W., Colella M., Ruder W.C., et al. Deoxycholic acid activates protein kinase C and phospholipase C via increased Ca2+ entry at plasma membrane. Gastroenterology 128 (2005) 695-707
13. Kawamata Y., Fujii R., Hosoya M., et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem 278 (2003) 9435-9440
14. Montrose M.H., Lester R., Zimniak P., et al. Bile acids increase cellular free calcium in cultured kidney cells (LLC-PK). Pflugers Arch 412 (1988) 164-171
15. Glinghammar B., Inoue H., and Rafter J.J. 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 (2002) 839-845
16. Payne C.M., Weber C., Crowley-Skillicorn C., et al. Deoxycholate induces mitochondrial oxidative stress and activates NF-{kappa}B through multiple mechanisms in HCT-116 colon epithelial cells. Carcinogenesis 28 (2007) 215-222
17. Jean-Louis S., Akare S., Ali M.A., et al. Deoxycholic acid induces intracellular signaling through membrane perturbations. J Biol Chem 281 (2006) 14948-14960
18. Goerg K.J., Nell G., and Rummel W. Effect of deoxycholate on the perfused rat colon. Concentration dependence of the effect on net fluid and electrolyte transfer and the correlation with paracellular permeability. Digestion 26 (1983) 105-113
19. Farack U.M., Nell G., Lueg O., et al. Independence of the activation of mucus and potassium secretion on the inhibition of sodium and water absorption by deoxycholate in rat colon. Naunyn Schmiedebergs Arch Pharmacol 321 (1982) 336-340
20. Voronina S., Longbottom R., Sutton R., et al. Bile acids induce calcium signals in mouse pancreatic acinar cells: implications for bile-induced pancreatic pathology. J Physiol 540 (2002) 49-55
21. Voronina S.G., Gryshchenko O.V., Gerasimenko O.V., et al. Bile acids induce a cationic current, depolarizing pancreatic acinar cells and increasing the intracellular Na+ concentration. J Biol Chem 280 (2005) 1764-1770
22. Kim J.Y., Kim K.H., Lee J.A., et al. Transporter-mediated bile acid uptake causes Ca2+-dependent cell death in rat pancreatic acinar cells. Gastroenterology 122 (2002) 1941-1953
23. Marx J. Cancer biology. All in the stroma: cancer's Cosa Nostra. Science 320 (2008) 38-41
24. Moschetta A., Portincasa P., van Erpecum K.J., et al. Sphingomyelin protects against apoptosis and hyperproliferation induced by deoxycholate: potential implications for colon cancer. Dig Dis Sci 48 (2003) 1094-1101
25. Curci S., and Schettino T. Effect of external sodium on intracellular chloride activity in the surface cells of frog gastric mucosa. Microelectrode studies. Pflugers Arch 401 (1984) 152-159
26. Debellis L., Curci S., and Fromter E. Effect of histamine on the basolateral K+ conductance of frog stomach oxyntic cells and surface epithelial cells. Am J Physiol 258 (1990) G631-G636
27. Demaurex N., Lew D.P., and Krause K.H. Cyclopiazonic acid depletes intracellular Ca2+ stores and activates an influx pathway for divalent cations in HL-60 cells. J Biol Chem 267 (1992) 2318-2324
28. Hofer A.M., Landolfi B., Debellis L., et al. Free [Ca2+] dynamics measured in agonist-sensitive stores of single living intact cells: a new look at the refilling process. EMBO J 17 (1998) 1986-1995
29. Abramson J.J., and Shamoo A.E. Anionic detergents as divalent cation ionophores across black lipid membranes. J Membr Biol 50 (1979) 241-255
30. Liu C., and Hermann T.E. Characterization of ionomycin as a calcium ionophore. J Biol Chem 253 (1978) 5892-5894
31. Arellano R.O., Woodward R.M., and Miledi R. A monovalent cationic conductance that is blocked by extracellular divalent cations in Xenopus oocytes. J Physiol 484 (1995) 593-604
32. Mauricio A.C., Slawik M., Heitzmann D., et al. Deoxycholic acid (DOC) affects the transport properties of distal colon. Pflugers Arch 439 (2000) 532-540
33. Sugg E.E., Garcia M.L., Reuben J.P., et al. Synthesis and structural characterization of charybdotoxin, a potent peptidyl inhibitor of the high conductance Ca2(+)-activated K+ channel. J Biol Chem 265 (1990) 18745-18748
34. van der Staay F.J., Fanelli R.J., Blokland A., et al. Behavioral effects of apamin, a selective inhibitor of the SK(Ca)-channel, in mice and rats. Neurosci Biobehav Rev 23 (1999) 1087-1110
35. Powell A.A., LaRue J.M., Batta A.K., et al. Bile acid hydrophobicity is correlated with induction of apoptosis and/or growth arrest in HCT116 cells. Biochem J 356 (2001) 481-486
36. Schlottman K., Wachs F.P., Krieg R.C., et al. Characterization of bile salt-induced apoptosis in colon cancer cell lines. Cancer Res 60 (2000) 4270-4276
37. Nakajima T., Okuda Y., Chisaki K., et al. Bile acids increase intracellular Ca(2+) concentration and nitric oxide production in vascular endothelial cells. Br J Pharmacol 130 (2000) 1457-1467
38. Rizzuto R., Pinton P., Ferrari D., et al. Calcium and apoptosis: facts and hypotheses. Oncogene 22 (2003) 8619-8627
39. Maenz D.D., and Forsyth G.W. Ricinoleate and deoxycholate are calcium ionophores in jejunal brush border vesicles. J Membr Biol 70 (1982) 125-133
40. Kurebe M. Effect of deoxycholate on Ca2+-ATPase of intestinal brush border membrane. Biochem Pharmacol 27 (1978) 1961-1965
41. Gerasimenko J.V., Flowerdew S.E., Voronina S.G., et al. Bile acids induce Ca2+ release from both the endoplasmic reticulum and acidic intracellular calcium stores through activation of inositol trisphosphate receptors and ryanodine receptors. J Biol Chem 281 (2006) 40154-40163
42. Dallaporta B., Hirsch T., Susin S.A., et al. Potassium leakage during the apoptotic degradation phase. J Immunol 160 (1998) 5605-5615
43. Wang Z. Roles of K+ channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch 448 (2004) 274-286
44. Bortner C.D., and Cidlowski J.A. Caspase independent/dependent regulation of K(+), cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J Biol Chem 274 (1999) 21953-21962
45. Sensi S.L., Canzoniero L.M., Yu S.P., et al. Measurement of intracellular free zinc in living cortical neurons: routes of entry. J Neurosci 17 (1997) 9554-9564
46. Burg E.D., Remillard C.V., and Yuan J.X. K+ channels in apoptosis. J Membr Biol 209 (2006) 3-20
47. Kunzelmann K. Ion channels and cancer. J Membr Biol 205 (2005) 159-173
48. Bonnet S., Archer S.L., Allalunis-Turner J., et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11 (2007) 37-51
49. Craven P.A., Pfanstiel J., Saito R., et al. Relationship between loss of rat colonic surface epithelium induced by deoxycholate and initiation of the subsequent proliferative response. Cancer Res 46 (1986) 5754-5759
50. Milovic V., Teller I.C., Faust D., et al. Effects of deoxycholate on human colon cancer cells: apoptosis or proliferation. Eur J Clin Invest 32 (2002) 29-34
51. Peiffer L.P., Peters D.J., and McGarrity T.J. Differential effects of deoxycholic acid on proliferation of neoplastic and differentiated colonocytes in vitro. Dig Dis Sci 42 (1997) 2234-2240
52. Shekels L.L., Beste J.E., and Ho S.B. Tauroursodeoxycholic acid protects in vitro models of human colonic cancer cells from cytotoxic effects of hydrophobic bile acids. J Lab Clin Med 127 (1996) 57-66