Chenodeoxycholic acid requires activation of EGFR, EPAC, and Ca2+ to stimulate CFTR-dependent Cl- secretion in human colonic T84 cells

American Journal of Physiology - Cell Physiology

Volumn 311, Issue 5, 2016, Pages C777-C792

  Domingue, Jada C ^a   Ao, Mei ^a   Sarathy, Jayashree ^a,b   Rao, Mrinalini C ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b BENEDICTINE UNIVERSITY   (United States)

Author keywords

Calcium ion; Chenodeoxycholic acid; Cystic fibrosis transmembrane conductance regulator; Epidermal growth factor receptor; Exchange protein directly activated by adenosine 3 ,5 cyclic monophosphate

Indexed keywords

CALCIUM ION; CHENODEOXYCHOLIC ACID; CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CYCLIC 3 5 ADENOSINE MONOPHOSPHATE; FARNESOID X RECEPTOR; G PROTEIN COUPLED BILE ACID RECEPTOR GPBAR1; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CALCIUM; CFTR PROTEIN, HUMAN; CHLORIDE; CHLORIDE CHANNEL; EGFR PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAPGEF3 PROTEIN, HUMAN;

ARTICLE; AUTOPHOSPHORYLATION; COLON CELL; COLON MUCOSA; DEVELOPMENT; ENZYME ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SHORT CIRCUIT CURRENT; SIGNAL TRANSDUCTION; CELL MEMBRANE; COLON; EPITHELIUM CELL; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CALCIUM; CELL LINE, TUMOR; CELL MEMBRANE; CHENODEOXYCHOLIC ACID; CHLORIDE CHANNELS; CHLORIDES; COLON; CYCLIC AMP; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; ERBB RECEPTORS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION;

EID: 84994578302     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00168.2016     Document Type: Article

References (74)

1. Alrefai WA, Saksena S, Tyagi S, Gill RK, Ramaswamy K, Dudeja PK. Taurodeoxycholate modulates apical Cl-/OH- exchange activity in Caco2 cells. Dig Dis Sci 52: 1270-1278, 2007.
2. Anderson MP, Welsh MJ. Calcium and cAMP activate different chloride channels in the apical membrane of normal and cystic fibrosis epithelia. Proc Natl Acad Sci USA 88: 6003-6007, 1991.
3. Andreev J, Galisteo ML, Kranenburg O, Logan SK, Chiu ES, Okigaki M, Cary LA, Moolenaar WH, Schlessinger J. Src and Pyk2 mediate G-protein-coupled receptor activation of epidermal growth factor receptor (EGFR) but are not required for coupling to the mitogen-activated protein (MAP) kinase signaling cascade. J Biol Chem 276: 20130-20135, 2001.
4. Annaba F, Sarwar Z, Kumar P, Saksena S, Turner JR, Dudeja PK, Gill RK, Alrefai WA. Modulation of ileal bile acid transporter (ASBT) activity by depletion of plasma membrane cholesterol: Association with lipid rafts. Am J Physiol Gastrointest Liver Physiol 294: G489-G497, 2008.
5. - secretion in human colonic epithelial T84 cells. Am J Physiol Cell Physiol 310: C1010-C1023, 2016.
6. - secretion via cAMP signaling and increases cystic fibrosis transmembrane conductance regulator phosphorylation in T84 cells. Am J Physiol Cell Physiol 305: C447-C456, 2013.
7. Ao M, Venkatasubramanian J, Boonkaewwan C, Ganesan N, Syed A, Benya RV, Rao MC. Lubiprostone activates Cl- secretion via cAMP signaling and increases membrane CFTR in the human colon carcinoma cell line, T84. Dig Dis Sci 56: 339-351, 2011.
8. Bertelsen LS, Barrett KE, Keely SJ. Gs protein-coupled receptor agonists induce transactivation of the epidermal growth factor receptor in T84 cells: implications for epithelial secretory responses. J Biol Chem 279: 6271-6279, 2004.
9. Binder HJ, Rawlins CL. Effect of conjugated dihydroxy bile salts on electrolyte transport in rat colon. J Clin Invest 52: 1460-1466, 1973.
10. Boonkaewwan C, Ao M, Toskulkao C, Rao MC. Specific immunomodulatory and secretory activities of stevioside and steviol in intestinal cells. J Ag Food Chem 56: 3777-3784, 2008.
11. Bos JL. Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci 31: 680-686, 2006.
12. Brunner H, Northfield TC, Hofmann AF, Go VL, Summerskill WH. Gastric emptying and secretion of bile acids, cholesterol, and pancreatic enzymes during digestion. Duodenal perfusion studies in healthy subjects. Mayo Clin Proc 49: 851-860, 1974.
13. 2+], electrical activity and force in phasic smooth muscle. Pflugers Arch 436: 801-803, 1998.
14. Carlos MA, Nwagwu C, Ao M, Venkatasubramanian J, Boonkaewwan C, Prasad R, Chowdhury SA, Vidyasagar D, Rao MC. Epidermal growth factor stimulates chloride transport in primary cultures of weanling and adult rabbit colonocytes. J Pediatr Gastroenterol Nutr 44: 300-311, 2007.
15. Cartwright CA, McRoberts JA, Mandel KG, Dharmsathaphorn K. Synergistic action of cyclic adenosine monophosphate- and calciummediated chloride secretion in a colonic epithelial cell line. J Clin Invest 76: 1837-1842, 1985.
16. Cheng K, Raufman JP. 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, 2005.
17. Cheng K, Xie G, Raufman JP. Matrix metalloproteinase-7-catalyzed release of HB-EGF mediates deoxycholyltaurine-induced proliferation of a human colon cancer cell line. Biochem Pharmacol 73: 1001-1012, 2007.
18. Chiang JY. Bile acid metabolism and signaling. Comp Physiol 3: 1191-1212, 2013.
19. Cipriani S, Mencarelli A, Chini MG, Distrutti E, Renga B, Bifulco G, Baldelli F, Donini A, Fiorucci S. The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PloS one 6: e25637, 2011.
20. Czerucka D, Dahan S, Mograbi B, Rossi B, Rampal P. Implication of mitogen-activated protein kinases in T84 cell responses to enteropathogenic Escherichia coli infection. Infect Immun 69: 1298-1305, 2001.
21. Dahan S, Busuttil V, Imbert V, Peyron JF, Rampal P, Czerucka D. Enterohemorrhagic Escherichia coli infection induces interleukin-8 production via activation of mitogen-activated protein kinases and the transcription factors NF-kappaB and AP-1 in T84 cells. Infect Immun 70: 2304-2310, 2002.
22. Dethlefsen SM, Raab G, Moses MA, Adam RM, Klagsbrun M, Freeman MR. Extracellular calcium influx stimulates metalloproteinase cleavage and secretion of heparin-binding EGF-like growth factor independently of protein kinase C. J Cell Biochem 69: 143-153, 1998.
23. Devor DC, Sekar MC, Frizzell RA, Duffey ME. Taurodeoxycholate activates potassium and chloride conductances via an IP3-mediated release of calcium from intracellular stores in a colonic cell line (T84). J Clin Invest 92: 2173-2181, 1993.
24. Dharmsathaphorn K, Cohn J, Beuerlein G. Multiple calcium-mediated effector mechanisms regulate chloride secretory responses in T84 cells. Am J Physiol Cell Physiol 256: C1224-C1230, 1989.
25. Dharmsathaphorn K, Huott PA, Vongkovit P, Beuerlein G, Pandol SJ, Ammon HV. Cl- secretion induced by bile salts. A study of the mechanism of action based on a cultured colonic epithelial cell line. J Clin Invest 84: 945-953, 1989.
26. DiBaise IRa. Bile acids: an underrecognized and underappreciated cause of chronic diarrhea. Pract Gastroenterol 110: 32-44, 2012.
27. Ding L, Yang L, Wang Z, Huang W. Bile acid nuclear receptor FXR and digestive system diseases. Acta Pharm Sin B 5: 135-144, 2015.
28. Domingue JC, Ao M, Sarathy J, George A, Alrefai WA, Nelson DJ, Rao MC. HEK-293 cells expressing the cystic fibrosis transmembrane conductance regulator (CFTR): a model for studying regulation of Cltransport. Physiol Rep 2: 2014.
29. Duboc H, Tache Y, Hofmann AF. The bile acid TGR5 membrane receptor: from basic research to clinical application. Dig Liver Dis 46: 302-312, 2014.
30. Estrada Y, Dong J, Ossowski L. Positive crosstalk between ERK and p38 in melanoma stimulates migration and in vivo proliferation. Pig Cell Melanoma Res 22: 66-76, 2009.
31. 2+-dependent Cl- transport in human embryonic kidney-293 cells (HEK_293) is CFTR-independent. FASEB J 29: LB764, 2015.
32. Hofmann AF. Bile acids: trying to understand their chemistry and biology with the hope of helping patients. Hepatology 49: 1403-1418, 2009.
33. Hoque KM, Woodward OM, van Rossum DB, Zachos NC, Chen L, Leung GP, Guggino WB, Guggino SE, Tse CM. Epac1 mediates protein kinase A-independent mechanism of forskolin-activated intestinal chloride secretion. J Gen Physiol 135: 43-58, 2010.
34. Jean-Louis S, Akare S, Ali MA, Mash EA Jr, Meuillet E, Martinez JD. Deoxycholic acid induces intracellular signaling through membrane perturbations. J Biol Chem 281: 14948-14960, 2006.
35. Jensen DD, Godfrey CB, Niklas C, Canals M, Kocan M, Poole DP, Murphy JE, Alemi F, Cottrell GS, Korbmacher C, Lambert NA, Bunnett NW, Corvera CU. The bile acid receptor TGR5 does not interact with beta-arrestins or traffic to endosomes but transmits sustained signals from plasma membrane rafts. J Biol Chem 288: 22942-22960, 2013.
36. Kanchanapoo J, Ao M, Prasad R, Moore C, Kay C, Piyachaturawat P, Rao MC. Role of protein kinase C-σ in the age-dependent secretagogue action of bile acids in mammalian colon. Am J Physiol Cell Physiol 293: C1851-C1861, 2007.
37. Keating N, Mroz MS, Scharl MM, Marsh C, Ferguson G, Hofmann AF, Keely SJ. Physiological concentrations of bile acids down-regulate agonist induced secretion in colonic epithelial cells. J Cell Mol Med 13: 2293-2303, 2009.
38. Keely SJ, Scharl MM, Bertelsen LS, Hagey LR, Barrett KE, Hofmann AF. Bile acid-induced secretion in polarized monolayers of T84 colonic epithelial cells: Structure-activity relationships. Am J Physiol Gastrointest Liver Physiol 292: G290-G297, 2007.
39. Keitel V, Cupisti K, Ullmer C, Knoefel WT, Kubitz R, Haussinger D. The membrane-bound bile acid receptor TGR5 is localized in the epithelium of human gallbladders. Hepatology 50: 861-870, 2009.
40. Keitel V, Gorg B, Bidmon HJ, Zemtsova I, Spomer L, Zilles K, Haussinger D. The bile acid receptor TGR5 (Gpbar-1) acts as a neurosteroid receptor in brain. Glia 58: 1794-1805, 2010.
41. Kim Y, Chang KO. Inhibitory effects of bile acids and synthetic farnesoid X receptor agonists on rotavirus replication. J Virol 85: 12570-12577, 2011.
42. Ko EA, Jin BJ, Namkung W, Ma T, Thiagarajah JR, Verkman AS. Chloride channel inhibition by a red wine extract and a synthetic small molecule prevents rotaviral secretory diarrhoea in neonatal mice. Gut 63: 1120-1129, 2014.
43. Kwong E, Li Y, Hylemon PB, Zhou H. Bile acids and sphingosine-1- phosphate receptor 2 in hepatic lipid metabolism. Acta Pharm Sin B 5: 151-157, 2015.
44. Lieu T, Jayaweera G, Bunnett NW. GPBA: a GPCR for bile acids and an emerging therapeutic target for disorders of digestion and sensation. Br J Pharmacol 171: 1156-1166, 2014.
45. Maloney PR, Parks DJ, Haffner CD, Fivush AM, Chandra G, Plunket KD, Creech KL, Moore LB, Wilson JG, Lewis MC, Jones SA, Willson TM. Identification of a chemical tool for the orphan nuclear receptor FXR. J Med Chem 43: 2971-2974, 2000.
46. Margolis B, Rhee SG, Felder S, Mervic M, Lyall R, Levitzki A, Ullrich A, Zilberstein A, Schlessinger J. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling. Cell 57: 1101-1107, 1989.
47. McCole DF, Keely SJ, Coffey RJ, Barrett KE. Transactivation of the epidermal growth factor receptor in colonic epithelial cells by carbachol requires extracellular release of transforming growth factor-alpha. J Biol Chem 277: 42603-42612, 2002.
48. Meisenhelder J, Suh PG, Rhee SG, Hunter T. Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro. Cell 57: 1109-1122, 1989.
49. Mekjian HS, Phillips SF, Hofmann AF. Colonic secretion of water and electrolytes induced by bile acids: perfusion studies in man. J Clin Invest 50: 1569-1577, 1971.
50. Mroz MS, Keating N, Ward JB, Sarker R, Amu S, Aviello G, Donowitz M, Fallon PG, Keely SJ. Farnesoid X receptor agonists attenuate colonic epithelial secretory function and prevent experimental diarrhoea in vivo. Gut 63: 808-817, 2014.
51. Nakahori Y, Takenaka O, Nakagome Y. A human X-Y homologous region encodes “amelogenin.” Genomics 9: 264-269, 1991.
52. Nakanishi S, Kakita S, Takahashi I, Kawahara K, Tsukuda E, Sano T, Yamada K, Yoshida M, Kase H, Matsuda Y. Wortmannin, a microbial product inhibitor of myosin light chain kinase. J Biol Chem 267: 2157-2163, 1992.
53. Oda K, Matsuoka Y, Funahashi A, Kitano H. A comprehensive pathway map of epidermal growth factor receptor signaling. Mol Sys Biol 1: 2005 0010, 2005.
54. Pallagi-Kunstar E, Farkas K, Maleth J, Rakonczay Z Jr, Nagy F, Molnar T, Szepes Z, Venglovecz V, Lonovics J, Razga Z, Wittmann T, Hegyi P. Bile acids inhibit Na(+)/H(+) exchanger and Cl(-)/HCO(3)(-) exchanger activities via cellular energy breakdown and Ca(2)(+) overload in human colonic crypts. Pflugers Arch 467: 1277-1290, 2015.
55. Pols TW, Nomura M, Harach T, Lo Sasso G, Oosterveer MH, Thomas C, Rizzo G, Gioiello A, Adorini L, Pellicciari R, Auwerx J, Schoonjans K. TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab 14: 747-757, 2011.
56. Potter GD, Sellin JH, Burlingame SM. Bile acid stimulation of cyclic AMP and ion transport in developing rabbit colon. J Pediatr Gastroenterol Nutr 13: 335-341, 1991.
57. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402: 884-888, 1999.
58. Proulx P. Structure-function relationships in intestinal brush border membranes. Biochim Biophys Acta 1071: 255-271, 1991.
59. Qiao L, Studer E, Leach K, McKinstry R, Gupta S, Decker R, Kukreja R, Valerie K, Nagarkatti P, El Deiry W, Molkentin J, Schmidt-Ullrich R, Fisher PB, Grant S, Hylemon PB, Dent P. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and FAS receptor in primary hepatocytes: inhibition of EGFR/mitogen-activated protein kinase-signaling module enhances DCA-induced apoptosis. Mol Biol Cell 12: 2629-2645, 2001.
60. Raimondi F, Santoro P, Barone MV, Pappacoda S, Barretta ML, Nanayakkara M, Apicella C, Capasso L, Paludetto R. Bile acids modulate tight junction structure and barrier function of Caco-2 monolayers via EGFR activation. Am J Physiol Gastrointest Liver Physiol 294: G906-G913, 2008.
61. Schmidt M, Evellin S, Weernink PA, von Dorp F, Rehmann H, Lomasney JW, Jakobs KH. A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 3: 1020-1024, 2001.
62. Sheikh IA, Koley H, Chakrabarti MK, Hoque KM. The Epac1 signaling pathway regulates Cl- secretion via modulation of apical KCNN4c channels in diarrhea. J Biol Chem 288: 20404-20415, 2013.
63. Singh N, Yadav M, Singh AK, Kumar H, Dwivedi SK, Mishra JS, Gurjar A, Manhas A, Chandra S, Yadav PN, Jagavelu K, Siddiqi MI, Trivedi AK, Chattopadhyay N, Sanyal S. Synthetic FXR agonist GW4064 is a modulator of multiple G protein-coupled receptors. Mol Endocrinol 28: 659-673, 2014.
64. 2+ levels, myosin light chain phosphorylation and force in vascular smooth muscle. Naunyn Schmiedebergs Arch Pharmacol 354: 120-127, 1996.
65. - transport in T84 human colonic epithelial cells. Am J Physiol Cell Physiol 271: C914-C922, 1996.
66. Vajanaphanich M, Schultz C, Rudolf MT, Wasserman M, Enyedi P, Craxton A, Shears SB, Tsien RY, Barrett KE, Traynor-Kaplan A. Long-term uncoupling of chloride secretion from intracellular calcium levels by Ins(3,4,5,6)P4. Nature 371: 711-714, 1994.
67. Vajanaphanich M, Schultz C, Tsien RY, Traynor-Kaplan AE, Pandol SJ, Barrett KE. Cross-talk between calcium and cAMP-dependent intra- cellular signaling pathways. Implications for synergistic secretion in T84 colonic epithelial cells and rat pancreatic acinar cells. J Clin Invest 96: 386-393, 1995.
68. - transport. Am J Physiol Cell Physiol 280: C646-C658, 2001.
69. Ward JB, Mroz MS, Keely SJ. The bile acid receptor, TGR5, regulates basal and cholinergic-induced secretory responses in rat colon. Neurogastroenterol Motil 25: 708-711, 2013.
70. Werneburg NW, Yoon JH, Higuchi H, Gores GJ. Bile acids activate EGF receptor via a TGF-α-dependent mechanism in human cholangiocyte cell lines. Am J Physiol Gastrointest Liver Physiol 285: G31-G36, 2003.
71. Wu W, Graves LM, Gill GN, Parsons SJ, Samet JM. Src-dependent phosphorylation of the epidermal growth factor receptor on tyrosine 845 is required for zinc-induced Ras activation. J Biol Chem 277: 24252-24257, 2002.
72. Xiao YQ, Malcolm K, Worthen GS, Gardai S, Schiemann WP, Fadok VA, Bratton DL, Henson PM. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-beta. J Biol Chem 277: 14884-14893, 2002.
73. Zhou H, Hylemon PB. Bile acids are nutrient signaling hormones. Steroids 86: 62-68, 2014.
74. Zwick E, Daub H, Aoki N, Yamaguchi-Aoki Y, Tinhofer I, Maly K, Ullrich A. Critical role of calcium- dependent epidermal growth factor receptor transactivation in PC12 cell membrane depolarization and bradykinin signaling. J Biol Chem 272: 24767-24770, 1997.