HEK-293 cells expressing the cystic fibrosis transmembrane conductance regulator (CFTR): A model for studying regulation of Cl- transport

Physiological Reports

Volumn 2, Issue 9, 2014, Pages

  Domingue, Jada C ^a   Ao, Mei ^a   Sarathy, Jayashree ^a,b   George, Alvin ^a   Alrefai, Waddah A ^a,c   Nelson, Deborah J ^d   Rao, Mrinalini C ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b BENEDICTINE UNIVERSITY   (United States)

^c JESSE BROWN VA MEDICAL CENTER   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

CFTR; Cl transport; HEK 293; TGR5

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FORSKOLIN; IODIDE; LITHOCHOLIC ACID; MULTIDRUG RESISTANCE PROTEIN 4; TUBULIN;

ARTICLE; BIOTINYLATION; CALCIUM TRANSPORT; CELL CULTURE; CELL MIGRATION; CELL SURFACE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRAVIOLET SPECTROPHOTOMETRY;

EID: 85009354316     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12158     Document Type: Article

References (47)

1. Alemi, F., D. P. Poole, J. Chiu, K. Schoonjans, F. Cattaruzza, J. R. Grider, et al. 2013. The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology 144:145–154. doi:10.1053/j.gastro.2012.09.055.
2. Anantamongkol, U., M. Ao, J. Sarathy Nee Venkatasubramanian, Y. S. Devi, N. Krishnamra, and M. C. Rao. 2012. Prolactin and dexamethasone regulate second messenger-stimulated cl(-) secretion in mammary epithelia. J. Signal Transduct. 2012:192142. doi: 10.1155/2012/192142.
3. Anbazhagan, A. N., S. Priyamvada, A. Kumar, D. B. Maher, A. Borthakur, W. A. Alrefai, et al. 2014. Translational repression of SLC26A3 by miR-494 in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 306:G123–G131. doi:10.1152/ajpgi.00222.2013.
4. Annaba, F., Z. Sarwar, P. Kumar, S. Saksena, J. R. Turner, P. K. Dudeja, et al. 2008. 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. doi:10.1152/ajpgi.00237.2007.
5. Annaba, F., P. Kumar, A. K. Dudeja, S. Saksena, R. K. Gill, and W. A. Alrefai. 2010. Green tea catechin EGCG inhibits ileal apical sodium bile acid transporter ASBT. Am. J. Physiol. Gastrointest. Liver Physiol. 298:G467–G473. doi:10.1152/ajpgi.00360.2009.
6. Annaba, F., Z. Sarwar, R. K. Gill, A. Ghosh, S. Saksena, A. Borthakur, et al. 2012. Enteropathogenic Escherichia coli inhibits ileal sodium-dependent bile acid transporter ASBT. Am. J. Physiol. Gastrointest. Liver Physiol. 302:G1216–G1222. doi:10.1152/ajpgi.00017.2012.
7. Ao, M., J. Sarathy, J. Domingue, W. A. Alrefai, and M. C. Rao. 2013. Chenodeoxycholic acid stimulates Cl(-) secretion via cAMP signaling and increases cystic fibrosis transmembrane conductance regulator phosphorylation in T84 cells. Am. J. Physiol. Cell Physiol. 305:C447–C456. doi:10.1152/ajpcell.00416.2012.
8. Bali, M., J. Lipecka, A. Edelman, and J. Fritsch. 2001. Regulation of ClC-2 chloride channels in T84 cells by TGF-alpha. Am. J. Physiol. Cell Physiol. 280:C1588–C1598.
9. Boonkaewwan, C., M. Ao, C. Toskulkao, and M. C. Rao. 2008. Specific immunomodulatory and secretory activities of stevioside and steviol in intestinal cells. J. Agric. Food Chem. 56:3777–3784. doi:10.1021/jf072681o.
10. Carlos, M. A., C. Nwagwu, M. Ao, J. Venkatasubramanian, C. Boonkaewwan, R. Prasad, et al. 2007. Epidermal growth factor stimulates chloride transport in primary cultures of weanling and adult rabbit colonocytes. J. Pediatr. Gastroenterol. Nutr. 44:300–311. doi:10.1097/MPG.0b013e31802fca72.
11. Chan, C. W., Y. Song, M. Ailenberg, M. Wheeler, S. F. Pang, G. M. Brown, et al. 1997. Studies of melatonin effects on epithelia using the human embryonic kidney-293 (HEK-293) cell line. Endocrinology 138:4732–4739. doi:10.1210/endo.138.11.5524.
12. Chang, S. Y., A. Di, A. P. Naren, H. C. Palfrey, K. L. Kirk, and D. J. Nelson. 2002. Mechanisms of CFTR regulation by syntaxin 1A and PKA. J. Cell Sci. 115(Pt 4):783–791.
13. Chappe, V., D. A. Hinkson, T. Zhu, X. B. Chang, J. R. Riordan, and J. W. Hanrahan. 2003. Phosphorylation of protein kinase C sites in NBD1 and the R domain control CFTR channel activation by PKA. J. Physiol. 548(Pt 1):39–52. doi:10.1113/jphysiol.2002.035790.
14. Cheng, J., V. Cebotaru, L. Cebotaru, and W. B. Guggino. 2010. Syntaxin 6 and CAL mediate the degradation of the cystic fibrosis transmembrane conductance regulator. Mol. Biol. Cell 21:1178–1187. doi:10.1091/mbc.E09-03-0229.
15. Cuppoletti, J., D. H. Malinowska, K. P. Tewari, Q. J. Li, A. M. Sherry, M. L. Patchen, et al. 2004. SPI-0211 activates T84 cell chloride transport and recombinant human ClC-2 chloride currents. Am. J. Physiol. Cell Physiol. 287:C1173–C1183. doi:10.1152/ajpcell.00528.2003.
16. Fuller, C. M., R. J. Bridges, and D. J. Benos. 1994. Forskolinbut not ionomycin-evoked Cl secretion in colonic epithelia depends on intact microtubules. Am. J. Physiol. 266(Pt 1): C661–C668.
17. Gill, R. K., A. Borthakur, K. Hodges, J. R. Turner, D. R. Clayburgh, S. Saksena, et al. 2007. Mechanism underlying inhibition of intestinal apical Cl/OH exchange following infection with enteropathogenic E. coli. J. Clin. Invest. 117:428–437. doi:10.1172/JCI29625.
18. Gitter, A. H., K. Bendfeldt, J. D. Schulzke, and M. Fromm. 2000. Trans/paracellular, surface/crypt, and epithelial/ subepithelial resistances of mammalian colonic epithelia. Pflugers Arch. 439:477–482.
19. Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36:59–74.
20. Granio, O., C. Norez, K. J. Ashbourne Excoffon, P. H. Karp, M. Lusky, F. Becq, et al. 2007. Cellular localization and activity of Ad-delivered GFP-CFTR in airway epithelial and tracheal cells. Am. J. Respir. Cell Mol. Biol. 37:631–639. doi: 10.1165/rcmb.2007-0026TE.
21. Hoque, K. M., O. M. Woodward, D. B. van Rossum, N. C. Zachos, L. Chen, G. P. Leung, et al. 2010. Epac1 mediates protein kinase A-independent mechanism of forskolin-activated intestinal chloride secretion. J. Gen. Physiol. 135:43–58. doi:10.1085/jgp.200910339.
22. Iosco, C. 2012. Characterization of ne wmolecular targets involved in iodide flux in the thyroid gland: the anoctamins: University of Bologna.
23. Jensen, D. D., C. B. Godfrey, C. Niklas, M. Canals, M. Kocan, D. P. Poole, et al. 2013. 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. doi:10.1074/jbc.M113.455774.
24. Keitel, V., K. Cupisti, C. Ullmer, W. T. Knoefel, R. Kubitz, and D. Haussinger. 2009. The membrane-bound bile acid receptor TGR5 is localized in the epithelium of human gallbladders. Hepatology 50:861–870. doi:10.1002/hep.23032.
25. Kunzelmann, K., R. Schreiber, A. Kmit, W. Jantarajit, J. R. Martins, D. Faria, et al. 2012. Expression and function of epithelial anoctamins. Exp. Physiol. 97:184–192. doi:10.1113/expphysiol.2011.058206.
26. Li, C., P. C. Krishnamurthy, H. Penmatsa, K. L. Marrs, X. Q. Wang, M. Zaccolo, et al. 2007. Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131:940–951. doi:10.1016/j.cell.2007.09.037.
27. - secretion via CFTR in Calu-3 airway epithelial cells. Am. J. Physiol. 275 (Pt 1):C913–C920.
28. Long, K. J., and K. B. Walsh. 1997. Iodide efflux measurements with an iodide-selective electrode: a non-radioactive procedure for monitoring cellular chloride transport. Methods Cell Sci. 19:207–212.
29. Lotscher, M., B. Kaissling, J. Biber, H. Murer, and M. Levi. 1997. Role of microtubules in the rapid regulation of renal phosphate transport in response to acute alterations in dietary phosphate content. J. Clin. Invest. 99:1302–1312. doi:10.1172/JCI119289.
30. +- and cAMP-dependent anion conductances in the apical membrane of polarized T84 cells. Am. J. Physiol. 275(Pt 1): C484–C495.
31. Mondini, A., F. Sassone, D. A. Civello, M. L. Garavaglia, C. Bazzini, S. Rodighiero, et al. 2012. Hypertension-linked mutation of alpha-adducin increases CFTR surface expression and activity in HEK and cultured rat distal convoluted tubule cells. PLoS ONE 7:e52014. doi:10.1371/journal.pone.0052014.
32. Mroz, M. S., and S. J. Keely. 2012. Epidermal growth factor chronically upregulates Ca(2+)-dependent Cl(-) conductance and TMEM16A expression in intestinal epithelial cells. J. Physiol. 590(Pt 8):1907–1920. doi:10.1113/jphysiol.2011.226126.
33. Penmatsa, H., W. Zhang, S. Yarlagadda, C. Li, V. G. Conoley, J. Yue, et al. 2010. Compartmentalized cyclic adenosine 30,50-monophosphate at the plasma membrane clusters PDE3A and cystic fibrosis transmembrane conductance regulator into microdomains. Mol. Biol. Cell 21:1097–1110. doi:10.1091/mbc.E09-08-0655.
34. Schroeder, B. C., T. Cheng, Y. N. Jan, and L. Y. Jan. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019–1029. doi:10.1016/j.cell.2008.09.003.
35. Shaw, G., S. Morse, M. Ararat, and F. L. Graham. 2002. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16:869–871. doi:10.1096/fj.01-0995fje.
36. Sheppard, D. N. 2012. CFTR channel pharmacology: insight from a flock of clones. Focus on “Divergent CFTR orthologs respond differently to the channel inhibitors CFTRinh-172, glibenclamide, and GlyH-101”. Am. J. Physiol. Cell Physiol. 302:C24–C26. doi:10.1152/ajpcell.00376.2011.
37. Taylor, A., M. Mamelak, E. Reaven, and R. Maffly. 1973. Vasopressin: possible role of microtubules and microfilaments in its action. Science 181:347–350.
38. Thomas, C., A. Gioiello, L. Noriega, A. Strehle, J. Oury, G. Rizzo, et al. 2009. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10:167–177. doi:10.1016/j.cmet.2009.08.001.
39. Tousson, A., C. M. Fuller, and D. J. Benos. 1996. Apical recruitment of CFTR in T-84 cells is dependent on cAMP and microtubules but not Ca2+ or microfilaments. J. Cell Sci. 109(Pt 6):1325–1334.
40. Venglarik, C. J., R. J. Bridges, and R. A. Frizzell. 1990. A simple assay for agonist-regulated Cl and K conductances in salt-secreting epithelial cells. Am. J. Physiol. 259(Pt 1): C358–C364.
41. Venkatasubramanian, J., N. Selvaraj, M. Carlos, S. Skaluba, M. M. Rasenick, and M. C. Rao. 2001. Differences in Ca (2+) signaling underlie age-specific effects of secretagogues on colonic Cl(-) transport. Am. J. Physiol. Cell Physiol. 280: C646–C658.
42. Ward, J. B., M. S. Mroz, and S. J. Keely. 2013. The bile acid receptor, TGR5, regulates basal and cholinergic-induced secretory responses in rat colon. Neurogastroenterol. Motil. 25:708–711. doi:10.1111/nmo.12148.
43. Xie, M., T. C. Rich, C. Scheitrum, M. Conti, and W. Richter. 2011. Inactivation of multidrug resistance proteins disrupts both cellular extrusion and intracellular degradation of cAMP. Mol. Pharmacol. 80:281–293. doi:10.1124/mol.111.071134.
44. Yang, Y. D., H. Cho, J. Y. Koo, M. H. Tak, Y. Cho, W. S. Shim, et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210–1215. doi:10.1038/nature07313.
45. Yoneno, K., T. Hisamatsu, K. Shimamura, N. Kamada, R. Ichikawa, M. T. Kitazume, et al. 2013. TGR5 signalling inhibits the production of pro-inflammatory cytokines by in vitro differentiated inflammatory and intestinal macrophages in Crohn’s disease. Immunology 139:19–29. doi:10.1111/imm.12045.
46. Yu, J. Z., R. H. Dave, J. A. Allen, T. Sarma, and M. M. Rasenick. 2009. Cytosolic G{alpha}s acts as an intracellular messenger to increase microtubule dynamics and promote neurite outgrowth. J. Biol. Chem. 284:10462–10472. doi:10.1074/jbc.M809166200.
47. Zimmerman, N. P., S. N. Kumar, J. R. Turner, and M. B. Dwinell. 2012. Cyclic AMP dysregulates intestinal epithelial cell restitution through PKA and RhoA. Inflamm. Bowel Dis. 18:1081–1091. doi:10.1002/ibd.21898.