Potentiators exert distinct effects on human, murine, and xenopus CFTR

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 311, Issue 2, 2016, Pages L192-L207

  Cui, Guiying ^a   Khazanov, Netaly ^b   Stauffer, Brandon B ^a   Infield, Daniel T ^a   Imhoff, Barry R ^a   Senderowitz, Hanoch ^b   McCarty, Nael A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAR ILAN UNIVERSITY   (Israel)

Author keywords

Blocker; Human CFTR; Murine CFTR; Pharmacophore model; Potentiator; Xenopus CFTR

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GENISTEIN; GLYH 101; IOWH 032; IVACAFTOR; NPPB; OSSK 2; OSSK 3; P1; P2; P3; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; 5-NITRO-2-(3-PHENYLPROPYLAMINO)BENZOIC ACID; AMINOPHENOL DERIVATIVE; CFTR PROTEIN, HUMAN; CHLORIDE CHANNEL STIMULATING AGENT; GLYCINE; HYDRAZINE DERIVATIVE; N-(2-NAPHTHALENYL)-((3,5-DIBROMO-2,4-DIHYDROXYPHENYL)METHYLENE)GLYCINE HYDRAZIDE; NITROBENZOIC ACID DERIVATIVE; QUINOLONE DERIVATIVE;

ALLOSTERISM; ANIMAL CELL; ARTICLE; BINDING SITE; CELL MEMBRANE; COMPUTER AIDED DESIGN; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG CONFORMATION; HUMAN; LUNG FIBROSIS; MURINE; NONHUMAN; OOCYTE; ORTHOLOGY; PHARMACOPHORE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; STEADY STATE; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENE DELETION; GENETICS; MEMBRANE POTENTIAL; MOUSE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PRECLINICAL STUDY;

AMINO ACID SEQUENCE; AMINOPHENOLS; ANIMALS; CELLS, CULTURED; CHLORIDE CHANNEL AGONISTS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DRUG EVALUATION, PRECLINICAL; GLYCINE; HYDRAZINES; MEMBRANE POTENTIALS; MICE; NITROBENZOATES; PATCH-CLAMP TECHNIQUES; QUINOLONES; SEQUENCE DELETION; XENOPUS LAEVIS;

EID: 84983798005     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00056.2016     Document Type: Article

References (47)

1. Ai T, Bompadre SG, Wang X, Hu S, Li M, Hwang TC. Capsaicin potentiates wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride-channel currents. Mol Pharmacol 65: 1415-1426, 2004.
2. Alexander C, Ivetac A, Liu X, Norimatsu Y, Serrano JR, Landstrom A, Sansom M, Dawson DC. Cystic fibrosis transmembrane conductance regulator: using differential reactivity toward channel-permeant and chan-nel-impermeant thiol-reactive probes to test a molecular model for the pore. Biochemistry 48: 10078-10088, 2009.
3. Ataullakhanov FI, Vitvitsky VM. What determines the intracellular ATP concentration. Biosci Rep 22: 501-511, 2002.
4. Beis I, Newsholme EA. The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem J 152: 23-32, 1975.
5. – channel activity. J Biol Chem 280: 5221-5226, 2005.
6. – channel. Biochem Soc Trans 43: 975-982, 2015.
7. Caldwell RA, Grove DE, Houck SA, Cyr DM. Increased folding and channel activity of a rare cystic fibrosis mutant with CFTR modulators. Am J Physiol Lung Cell Mol Physiol 301: L346-L352, 2011.
8. Caputo A, Hinzpeter A, Caci E, Pedemonte N, Arous N, Di Duca M, Zegarra-Moran O, Fanen P, Galietta LJ. Mutation-specific potency and efficacy of cystic fibrosis transmembrane conductance regulator chloride channel potentiators. J Pharmacol Exp Ther 330: 783-791, 2009.
9. Csanady L, Torocsik B. Structure-activity analysis of a CFTR channel potentiator: distinct molecular parts underlie dual gating effects. J Gen Physiol 144: 321-336, 2014.
10. Cui G, Freeman CS, Knotts T, Prince CZ, Kuang C, McCarty NA. Two salt bridges differentially contribute to the maintenance of cystic fibrosis transmembrane conductance regulator (CFTR) channel function. J Biol Chem 288: 20758-20767, 2013.
11. Cui G, McCarty NA. Murine and human CFTR exhibit different sensitivities to CFTR potentiators. Am J Physiol Lung Cell Mol Physiol 309: L687-L699, 2015.
12. Cui G, Rahman KS, Infield DT, Kuang C, Prince CZ, McCarty NA. Three charged amino acids in extracellular loop 1 are involved in maintaining the outer pore architecture of CFTR. J Gen Physiol 144: 159-179, 2014.
13. Cui G, Song B, Turki HW, McCarty NA. Differential contribution of TM6 and TM12 to the pore of CFTR identified by three sulfonylureabased blockers. Pflügers Arch 463: 405-418, 2012.
14. Dong Q, Ostedgaard LS, Rogers C, Vermeer DW, Zhang Y, Welsh MJ. Human-mouse cystic fibrosis transmembrane conductance regulator (CFTR) chimeras identify regions that partially rescue CFTR-DeltaF508 processing and alter its gating defect. Proc Natl Acad Sci USA 109: 917-922, 2012.
15. Drumm ML, Wilkinson DJ, Smit LS, Worrell RT, Strong TV, Frizzell RA, Dawson DC, Collins FS. Chloride conductance expressed by delta F508 and other mutant CFTRs in Xenopus oocytes. Science 254: 1797-1799, 1991.
16. Duret G, Van Renterghem C, Weng Y, Prevost M, Moraga-Cid G, Huon C, Sonner JM, Corringer PJ. Functional prokaryotic-eukaryotic chimera from the pentameric ligand-gated ion channel family. Proc Natl Acad Sci USA 108: 12143-12148, 2011.
17. Irwin JJ, Shoichet BK. ZINC—a free database of commercially available compounds for virtual screening. J Chem Inf Model 45: 177-182, 2005.
18. Irwin JJ, Sterling T, Mysinger MM, Bolstad ES, Coleman RG. ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52: 1757-1768, 2012.
19. Jones AM, Barry PJ. Lumacaftor/ivacaftor for patients homozygous for Phe508del-CFTR: should we curb our enthusiasm? Thorax 70: 615-616, 2015.
20. Liu X, Dawson DC. Cystic fibrosis transmembrane conductance regulator (CFTR) potentiators protect G551D but not DeltaF508 CFTR from thermal instability. Biochemistry 53: 5613-5618, 2014.
21. Mandal S, Moudgil M, Mandal SK. Rational drug design. Eur J Pharmacol 625: 90-100, 2009.
22. McCarty NA, Zhang ZR. Identification of a region of strong discrimination in the pore of CFTR. Am J Physiol Lung Cell Mol Physiol 281: L852-L867, 2001.
23. Melani R, Tomati V, Galietta LJ, Zegarra-Moran O. Modulation of cystic fibrosis transmembrane conductance regulator (CFTR) activity and genistein binding by cytosolic pH. J Biol Chem 285: 41591-41596, 2010.
24. Mense M, Vergani P, White DM, Altberg G, Nairn AC, Gadsby DC. In vivo phosphorylation of CFTR promotes formation of a nucleotidebinding domain heterodimer. EMBO J 25: 4728-4739, 2006.
25. Moran O, Zegarra-Moran O. A quantitative description of the activation and inhibition of CFTR by potentiators: genistein. FEBS Lett 579: 3979-3983, 2005.
26. Muanprasat C, Sonawane ND, Salinas D, Taddei A, Galietta LJ, Verkman AS. Discovery of glycine hydrazide pore-occluding CFTR inhibitors: mechanism, structure-activity analysis, and in vivo efficacy. J Gen Physiol 124: 125-137, 2004.
27. Namkung W, Park J, Seo Y, Verkman AS. Novel amino-carbonitrilepyrazole identified in a small molecule screen activates wild-type and DeltaF508 cystic fibrosis transmembrane conductance regulator in the absence of a cAMP agonist. Mol Pharmacol 84: 384-392, 2013.
28. Pedemonte N, Sonawane ND, Taddei A, Hu J, Zegarra-Moran O, Suen YF, Robins LI, Dicus CW, Willenbring D, Nantz MH, Kurth MJ, Galietta LJ, Verkman AS. Phenylglycine and sulfonamide correctors of defective delta F508 and G551D cystic fibrosis transmembrane conductance regulator chloride-channel gating. Mol Pharmacol 67: 1797-1807, 2005.
29. Phuan PW, Yang B, Knapp JM, Wood AB, Lukacs GL, Kurth MJ, Verkman AS. Cyanoquinolines with independent corrector and potentiator activities restore DeltaPhe508-cystic fibrosis transmembrane conductance regulator chloride channel function in cystic fibrosis. Mol Pharmacol 80: 683-693, 2011.
30. Price MP, Ishihara H, Sheppard DN, Welsh MJ. Function of Xenopus cystic fibrosis transmembrane conductance regulator (CFTR) Cl channels and use of human-Xenopus chimeras to investigate the pore properties of CFTR. J Biol Chem 271: 25184-25191, 1996.
31. Rahman KS, Cui G, Harvey SC, McCarty NA. Modeling the conformational changes underlying channel opening in CFTR. PLoS One 8: e74574, 2013.
32. Ramsey BW, Davies J, McElvaney NG, Tullis E, Bell SC, Drevinek P, Griese M, McKone EF, Wainwright CE, Konstan MW, Moss R, Ratjen F, Sermet-Gaudelus I, Rowe SM, Dong Q, Rodriguez S, Yen K, Ordonez C, Elborn JS. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Eng J Med 365: 1663-1672, 2011.
33. - channel with the gating behavior of murine CFTR. Proc Natl Acad Sci USA 104: 16365-16370, 2007.
34. Thiagarajah JR, Verkman AS. CFTR inhibitors for treating diarrheal disease. Clin Pharmacol Ther 92: 287-290, 2012.
35. Tucker SJ, Tannahill D, Higgins CF. Identification and developmental expression of the Xenopus laevis cystic fibrosis transmembrane conductance regulator gene. Hum Mol Genet 1: 77-82, 1992.
36. Uhler MD, Abou-Chebl A. Cellular concentrations of protein kinase A modulate prostaglandin and cAMP induction of alkaline phosphatase. J Biol Chem 267: 8658-8665, 1992.
37. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Cao D, Neuberger T, Turnbull A, Singh A, Joubran J, Hazlewood A, Zhou J, McCartney J, Arumugam V, Decker C, Yang J, Young C, Olson ER, Wine JJ, Frizzell RA, Ashlock M, Negulescu P. Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci USA 106: 18825-18830, 2009.
38. Van Goor F, Straley KS, Cao D, Gonzalez J, Hadida S, Hazlewood A, Joubran J, Knapp T, Makings LR, Miller M, Neuberger T, Olson E, Panchenko V, Rader J, Singh A, Stack JH, Tung R, Grootenhuis PD, Negulescu P. Rescue of -∆F508-CFTR trafficking and gating in human cystic fibrosis airway primary cultures by small molecules. Am J Physiol Lung Cell Mol Physiol 290: L1117-L1130, 2006.
39. Van Goor F, Yu H, Burton B, Hoffman BJ. Effect of ivacaftor on CFTR forms with missense mutations associated with defects in protein processing or function. J Cyst Fibros 13: 29-36, 2014.
40. Veit G, Avramescu RG, Perdomo D, Phuan PW, Bagdany M, Apaja PM, Borot F, Szollosi D, Wu YS, Finkbeiner WE, Hegedus T, Verkman AS, Lukacs GL. Some gating potentiators, including VX-770, diminish DeltaF508-CFTR functional expression. Sci Trans Med 6: 246ra297, 2014.
41. Wainwright CE, Elborn JS, Ramsey BW, Marigowda G, Huang X, Cipolli M, Colombo C, Davies JC, De Boeck K, Flume PA, Konstan MW, McColley SA, McCoy K, McKone EF, Munck A, Ratjen F, Rowe SM, Waltz D, Boyle MP. Lumacaftor-Ivacaftor in patients with cystic fibrosis homozygous for Phe508del CFTR. N Eng J Med 373: 220-231, 2015.
42. Walters R, Welsh M. Mechanism by which calcium phosphate coprecipitation enhances adenovirus-mediated gene transfer. Gene Ther 6: 1845-1850, 1999.
43. Wang W, Hong JS, Rab A, Sorscher EJ, Kirk KL. Robust stimulation of W1282X-CFTR channel activity by a combination of allosteric modulators. PLoS One 11: e0152232, 2016.
44. Wang W, Li G, Clancy JP, Kirk KL. Activating cystic fibrosis transmembrane conductance regulator channels with pore blocker analogs. J Biol Chem 280: 23622-23630, 2005.
45. Wolber G, Langer T. LigandScout: 3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. J Chem Inf Model 45: 160-169, 2005.
46. Yu K, Whitlock JM, Lee K, Ortlund EA, Cui YY, Hartzell HC. Identification of a lipid scrambling domain in ANO6/TMEM16F. eLife 4: e06901, 2015.
47. Zhang ZR, Zeltwanger S, McCarty NA. Direct comparison of NPPB and DPC as probes of CFTR expressed in Xenopus oocytes. J Membr Biol 175: 35-52, 2000.