CFTR induces extracellular acid sensing in Xenopus oocytes which activates endogenous Ca 2+-activated Cl - conductance

Pflugers Archiv European Journal of Physiology

Volumn 462, Issue 3, 2011, Pages 479-487

  Kongsuphol, Patthara ^a   Schreiber, Rainer ^a   Kraidith, Kamonshanok ^a   Kunzelmann, Karl ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

F508 CFTR; Acid; Ca 2+ activated chloride secretion; CaCC; CFTR; Cystic fibrosis transmembrane conductance regulator; Protons; TMEM16A

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ION; CHLORIDE CHANNEL; CHLORIDE ION; LYSOPHOSPHATIDIC ACID; PDZ PROTEIN; PROTON; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

ACIDIFICATION; ACIDITY; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN HEK293; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CHANNEL GATING; CHLORIDE CONDUCTANCE; CONTROLLED STUDY; EXTRACELLULAR ACID SENSING; HUMAN; HUMAN CELL; NONHUMAN; OOCYTE; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

1-METHYL-3-ISOBUTYLXANTHINE; 4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; ANIMALS; CALCIUM; CHLORIDE CHANNELS; CYCLOOXYGENASE INHIBITORS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FEMALE; FORSKOLIN; GENISTEIN; HEK293 CELLS; HUMANS; ION CHANNEL GATING; NIFLUMIC ACID; OOCYTES; PATCH-CLAMP TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; PROTEIN KINASE INHIBITORS; PROTONS; XENOPUS LAEVIS;

EID: 80054717104     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-011-0983-9     Document Type: Article

References (48)

1. Amaral MD, Kunzelmann K (2007) Molecular targeting of CFTR as a therapeutic approach to cystic fibrosis. Trends Pharmacol Sci 28:334-341 (Pubitemid 47016687)
2. Anderson MP, Welsh MJ (1991) 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 (Pubitemid 21914874)
3. Arnett T (2003) Regulation of bone cell function by acid-base balance. Proc Nutr Soc 62:511-520 (Pubitemid 36841626)
4. Barro Soria R, AlDehni F, Almaca J, Witzgall R, Schreiber R, Kunzelmann K (2009) ER localized bestrophin1 acts as a counterion channel to activate Ca2+ dependent ion channels TMEM16A and SK. Pflugers Arch 459:485-497
5. Bompadre SG, Sohma Y, Li M, Hwang TC (2007) G551D and G1349D, two CF-associated mutations in the signature sequences of CFTR, exhibit distinct gating defects. J Gen Physiol 129:285-298 (Pubitemid 46506980)
6. Bronckers A, Kalogeraki L, Jorna HJ, Wilke M, Bervoets TJ, Lyaruu DM, Zandieh-Doulabi B, Denbesten P, De Jonge H (2010) The cystic fibrosis transmembrane conductance regulator (CFTR) is expressed in maturation stage ameloblasts, odontoblasts and bone cells. Bone 46:1188-1196
7. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ (2008) TMEM16A, a membrane protein associated with calciumdependent chloride channel activity. Science 322:590-594
8. Chen JH, Cai Z, Sheppard DN (2009) Direct sensing of intracellular pH by the cystic fibrosis transmembrane conductance regulator (CFTR) Cl-channel. J Biol Chem 284:35495-35506
9. Dalemans W, Barbry P, Champigny G, Jallat S, Dott K, Dreyer D, Crystal RG, Pavirani A, Lecocq J-P, Lazdunski M (1992) Altered chloride ion channel kinetics associated with the deltaF508 cystic fibrosis mutation. Nature 354:526-528 (Pubitemid 21896832)
10. Dawson DC, Smith SS, Mansoura MK (1999) CFTR: mechanism of anion conduction. Physiol Rev 79:S47-S75 (Pubitemid 29058909)
11. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358:761-764
12. Dif F, Marty C, Baudoin C, de Vernejoul MC, Levi G (2004) Severe osteopenia in CFTR-null mice. Bone 35:595-603 (Pubitemid 39144418)
13. Doring G, Conway SP (2008) Osteoporosis in cystic fibrosis. J Pediatr 84:1-3 (Pubitemid 351287714)
14. Drumm ML, Wilkinson DJ, Smit LS, Worrell RT, Strong TV, Frizzell RA, Dawson DC, Collins FS (1991) Chloride conductance expressed by deltaF508 and other mutant CFTRs in Xenopus oocytes. Science 254:1797-1799 (Pubitemid 21917530)
15. Duffield MD, Rychkov GY, Bretag AH, Roberts ML (2005) Zinc inhibits human ClC-1 muscle chloride channel by interacting with its common gating mechanism. J Physiol 568:5-12 (Pubitemid 41448616)
16. Ferrera L, Caputo A, Ubby I, Bussani E, Zegarra-Moran O, Ravazzolo R, Pagani F, Galietta LJ (2009) Regulation of TMEM16A chloride channel properties by alternative splicing. J Biol Chem 284:33360-33368
17. Grubb BR, Vick RN, Boucher RC (1994) Hyperabsorption of Na+ and raised Ca + mediated Cl-secretion in nasal epithelia of CF mice. Am J Physiol 266:C1478-C1483 (Pubitemid 24170677)
18. Guggino WB, Stanton BA (2006) New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol 7:426-436 (Pubitemid 44050096)
19. Haston CK, Li W, Li A, Lafleur M, Henderson JE (2008) Persistent osteopenia in adult cystic fibrosis transmembrane conductance regulator-deficient mice. Am J Respir Crit Care Med 177:309-315 (Pubitemid 351198374)
20. Henriksen K, Bollerslev J, Everts V, Karsdal MA (2011) Osteoclast activity and subtypes as a function of physiology and pathology - implications for future treatments of osteoporosis. Endocr Rev 32:31-63
21. Javier RM, Jacquot J (2011) Bone disease in cystic fibrosis: what's new? Joint Bone Spine
22. Knowles MR, Clarke LL, Boucher RC (1991) Activation by extracellular nucleotides of chloride secretion in the airway epithelia of patients with cystic fibrosis. N Engl J Med 325:533-538
23. Kunzelmann K (2001) CFTR: interacting with everything? News Physiol Sci 17:167-170 (Pubitemid 33713264)
24. Kunzelmann K (2011) Assessment of CFTR function. In: Cystic fibrosis: methods and protocols. In: Amaral M, Kunzelmann K (eds) Methods in molecular biology (in press) 2
25. Kunzelmann K, Kongsuphol P, AlDehni F, Tian Y, Ousingsawat J, Warth R, Schreiber R (2009) Bestrophin and TMEM16 - Ca + activated Cl-channels with different functions. Cell Calcium 46:233-241
26. Kunzelmann K, Mall M, Briel M, Hipper A, Nitschke R, Ricken S, Greger R (1997) The cystic fibrosis transmembrane conductance regulator attenuates the endogenous Ca2+ activated Clconductance in Xenopus ooyctes. Pflugers Arch 434:178-181 (Pubitemid 28068754)
27. Kunzelmann K, Schreiber R, Cook DI (2002) Mechanisms for inhibition of amiloride-sensitive Na+ absorption by extracellular nuceotides in mouse trachea. Pflugers Arch 444:220-226 (Pubitemid 34499264)
28. Li C, Dandridge KS, Di A, Marrs KL, Harris EL, Roy K, Jackson JS, Makarova NV, Fujiwara Y, Farrar PL, Nelson DJ, Tigyi GJ, Naren AP (2005) Lysophosphatidic acid inhibits cholera toxininduced secretory diarrhea through CFTR-dependent protein interactions. J Exp Med 202:975-986 (Pubitemid 41396897)
29. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, Jalink K, Li M, Nelson DJ, Schuetz JD, Naren AP (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131:940-951 (Pubitemid 350138082)
30. Mall M, Gonska T, Thomas J, Schreiber R, Seydewitz HH, Kuehr J, Brandis M, Kunzelmann K (2003) Modulation of Ca2+ activated Springer Cl-secretion by basolateral K+ channels in human normal and cystic fibrosis airway epithelia. Pediatr Res 53:608-618 (Pubitemid 36406731)
31. Martins JR, Kongsuphol P, Sammels E, AlDehni F, Clarke L, Schreiber R, De Smedt H, Amaral MD, Kunzelmann K (2011) F508del-CFTR increases intracellular Ca2+ signaling that causes enhanced calcium-dependent Cl-conductance in cystic fibrosis. Acta Physiol Scand (Abtract) 201S 682:P271
32. Namkung W, Thiagarajah JR, Phuan PW, Verkman AS (2010) Inhibition of Ca2+-activated Cl-channels by gallotannins as a possible molecular basis for health benefits of red wine and green tea. FASEB J 24:4178-4186
33. Naren AP, Cobb B, Li C, Roy K, Nelson D, Heda GD, Liao J, Kirk KL, Sorscher EJ, Hanrahan JW, Clancy JP (2003) A macromolecular complex of beta 2 adrenergic receptor, CFTR, and ezrin/radixin/moesin-binding phosphoprotein 50 is regulated by PKA. Proc Natl Acad Sci USA 100:342-346 (Pubitemid 36078076)
34. Noh SJ, Kim MJ, Shim S, Han JK (1998) Different signaling pathway between sphingosine-1-phosphate and lysophosphatidic acid in Xenopus oocytes: functional coupling of the sphingosine-1-phosphate receptor to PLC-xbeta in Xenopus oocytes. J Cell Physiol 176:412-423 (Pubitemid 28319725)
35. Oceandy D, McMorran BJ, Smith SN, Schreiber R, Kunzelmann K, Alton EWF, Hume DA, Wainwright BJ (2002) Gene complementation of airway epithelium in the cystic fibrosis mouse in necessary and sufficient to correct the pathogen clearance and inflammatory abnormalities. Hum Mol Genet 11:1059-1067 (Pubitemid 34521087)
36. Ousingsawat J, Martins JR, Schreiber R, Rock JR, Harfe BD, Kunzelmann K (2009) Loss of TMEM16A causes a defect in epithelial Ca2+ dependent chloride transport. J Biol Chem 284:28698-28703
37. Paradiso AM, Ribeiro CM, Boucher RC (2001) Polarized signaling via purinoceptors in normal and cystic fibrosis airway epithelia. J Gen Physiol 117:53-68
38. Pashuck TD, Franz SE, Altman MK, Wasserfall CH, Atkinson MA, Wronski TJ, Flotte TR, Stalvey MS (2009) Murine model for cystic fibrosis bone disease demonstrates osteopenia and sex-related differences in bone formation. Pediatr Res 65:311-316
39. Penmatsa H, Zhang W, Yarlagadda S, Li C, Conoley VG, Yue J, Bahouth SW, Buddington RK, Zhang G, Nelson DJ, Sonecha MD, Manganiello V, Wine JJ, Naren AP (2010) Compartmentalized cAMP at the plasma membrane clusters PDE3A and CFTR into microdomains. Mol Biol Cell 21:1097-1100
40. Qu Z, Hartzell HC (2000) Anion permeation in Ca2+-activated Cl-channels. J Gen Physiol 116:825-844
41. Qu Z, Hartzell HC (2001) Functional geometry of the permeation pathway of Ca2+-activated Cl-channels inferred from analysis of voltage-dependent block. J Biol Chem 276:18423-18429
42. Rock JR, O'Neal WK, Gabriel SE, Randell SH, Harfe BD, Boucher RC, Grubb BR (2009) Transmembrane protein 16A (TMEM16A) is a Ca2+ regulated Cl-secretory channel in mouse airways. J Biol Chem 284:14875-14880
43. Schreiber R, Uliyakina I, Kongsuphol P, Warth R, Mirza M, Martins JR, Kunzelmann K (2010) Expression and function of epithelial anoctamins. J Biol Chem 285:7838-7845
44. Schroeder BC, Cheng T, Jan YN, Jan LY (2008) Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019-1029
45. Treharne KJ, Xu Z, Chen J-H, Best OG, Cassidy D, Gruenert DC, Hegyi P, Gray L, Sheppard DN, Kunzelmann K, Mehta A (2009) Inhibition of protein kinase CK2 closes the CFTR Cl-channel, but has no effect on the cystic fibrosis mutant F508-CFTR. Cell Physiol Biochem 24:347-360
46. Van der Wijk T, De Jonge HR, Tilly BC (1999) Osmotic cell swelling-induced ATP release mediates the activation of extracellular signal-regulated protein kinase (Erk)-1/2 but not the activation of osmo-sensitive anion channels. Biochem J 343(Pt 3):579-586 (Pubitemid 29537369)
47. Wei L, Vankeerberghen A, Cuppens H, Eggermont J, Cassiman JJ, Droogmans G, Nilius B (1999) Interaction between calcium-activated chloride channels and the cystic 487 fibrosis transmembrane conductance regulator. Pflugers Arch 438:635-641 (Pubitemid 29454978)
48. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210-1215