Curcumin and genistein additively potentiate G551D-CFTR

Journal of Cystic Fibrosis

Volumn 10, Issue 4, 2011, Pages 243-252

  Yu, Ying Chun ^a   Miki, Haruna ^b,e   Nakamura, Yumi ^a   Hanyuda, Akiko ^a   Matsuzaki, Yohei ^a   Abe, Yoichiro ^a   Yasui, Masato ^a   Tanaka, Kazuhiko ^e   Hwang, Tzyh Chang ^b,c   Bompadre, Silvia G ^b,d   Sohma, Yoshiro ^a,b  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

^e OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

Additive effect; CFTR; Curcumin; Cystic fibrosis; G551D mutation; Genistein

Indexed keywords

ASPARTIC ACID; CURCUMIN; GENISTEIN; GLYCINE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CYSTIC FIBROSIS; DRUG POTENTIATION; MISSENSE MUTATION; NONHUMAN; PATCH CLAMP; PROTEIN BINDING;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CHO CELLS; CRICETINAE; CRICETULUS; CURCUMIN; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DRUG SYNERGISM; GENISTEIN; GREEN FLUORESCENT PROTEINS; HUMANS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MUTATION, MISSENSE; PATCH-CLAMP TECHNIQUES; PHYTOESTROGENS; TRANSFECTION;

EID: 79958276128     PISSN: 15691993     EISSN: 18735010     Source Type: Journal    
DOI: 10.1016/j.jcf.2011.03.001     Document Type: Article

References (48)

1. Accurso F.J., Rowe S.M., Clancy J.P., Boyle M.P., Dunitz J.M., Durie P.R., et al. Effect of VX-770 in persons with cystic fibrosis and the G551D-CFTR mutation. N Engl J Med 2010, 363:1991-2003.
2. Aggarwal B.B., Kumar A., Bharti A.C. Anticancer potential of curcumin: preclinical and clinical studies. Anticancer Res 2003, 23:363-398.
3. Ai T., Bompadre S.G., Wang X., Hu S., Li M., Hwang T.-C. Capsaicin potentiates wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride-channel currents. Mol Pharmacol 2004, 65:1415-1426.
4. Al-Nakkash L., Hu S.M.L., Hwang T.-C. A common mechanism for cystic fibrosis transmembrane conductance regulator protein activation by genistein and benzimidazolone analogs. J Pharmacol Exp Ther 2001, 296:464-472.
5. Amaral M.D., Kunzelmann K. Molecular targeting of CFTR as a therapeutic approach to cystic fibrosis. Trends Pharmacol Sci 2007, 28:334-341.
6. Andersson C., Servetnyk Z., Roomans G. Activation of CFTR by genistein in human airway epithelial cell lines. Biochem Biophys Res Commun 2003, 308:518-522.
7. Berger A.L., Randak C., Ostedgaard L.S., Karp P., Vermeer D., Welsh M.J. Curcumin stimulates cystic fibrosis transmembrane conductance regulator Cl- channel activity. J Biol Chem 2005, 280:5221-5226.
8. Bernard K., Wang W., Narlawar R., Schmidt B., Kirk K.L. Curcumin cross-links cystic fibrosis transmembrane conductance regulator (CFTR) polypeptides and potentiates CFTR channel activity by distinct mechanisms. J Biol Chem 2009, 284:30754-30765.
9. Bompadre S.G., Sohma Y., Li M., Hwang T.-C. G551D and G1349D, two CF-associated mutations in the signature sequence of CFTR, exhibit distinct gating defects. J Gen Physiol 2007, 129:285-298.
10. Caci E., Folli C., Zegarra-Moran O., Ma T., Springsteel M.F., Sammelson R.E., et al. CFTR activation in human bronchial epithelial cells by novel benzoflavone and benzimidazolone compounds. Am J Physiol Lung Cell Mol Physiol 2003, 285:L180-L188.
11. Cai Z., Taddei A., Sheppard D.N. Differential sensitivity of the cystic fibrosis (CF)-associated mutants G551D and G1349D to potentiators of the cystic fibrosis transmembrane conductance regulator (CFTR) Cl- channel. J Biol Chem 2006, 281:1970-1977.
12. Chang X.-B., Tabcharani J.A., Hou Y.-X., Jensen T.J., Kartner N., Alon N., et al. Protein kinase A (PKA) still activates CFTR chloride channel after mutagenesis of all 10 PKA concensus phosphorylation sites. J Biol Chem 1993, 268:11304-11311.
13. Colquhoun D. Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br J Pharmacol 1998, 125:924-947.
14. Cutting G.R., Kasch L.M., Rosenstein B.J., Zielenski J., Tsui L.C., Antonarakis S.E., et al. A cluster of cystic fibrosis mutations in the first nucleotide-binding fold of the cystic fibrosis conductance regulator protein. Nature 1990, 346:366-369.
15. Dérand R., Bulteau-Pignoux L., Mettey Y., Zegarra-Moran O., Howell L.D., Randak C., et al. Activation of G551D CFTR channel with MPB-91: regulation by ATPase activity and phosphorylation. Am J Physiol Cell Physiol 2001, 281:C1657-C1666.
16. Dixon R., Ferreira D. Genistein. Phytochemistry 2002, 60:205-211.
17. Egan M.E., Pearson M., Weiner S.A., Rajendran V., Rubin D., Glockner-Pagel J., et al. Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science 2004, 304:600-602.
18. Gadsby D.C., Vergani P., Csanády L. The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 2006, 440:477-483.
19. Gopinath D., Ahmed M.R., Gomathi K., Chitra K., Sehgal P.K., Jayakumar R. Dermal wound healing processes with curcumin incorporated collagen films. Biomaterials 2004, 25:1911-1917.
20. Gray M.A., Greenwell J.R., Argent B.E. Secretin-regulated chloride channel on the apical plasma membrane of pancreatic duct cells. J Membr Biol 1988, 105:131-142.
21. Hwang T.-C., Wang F., Yang I.C., Reenstra W.W. Genistein potentiates wild-type and delta F508-CFTR channel activity. Am J Physiol 1997, 273:C988-C998.
22. Hwang T.C., Koeppe R.E., Andersen O.S. Genistein can modulate channel function by a phosphorylation-independent mechanism: importance of hydrophobic mismatch and bilayer mechanics. Biochemistry 2003, 42:13646-13658.
23. Illek B., Fischer H., Santos G.F., Widdicombe J.H., Machen T.E., Reenstra W.W. cAMP-independent activation of CFTR Cl channels by the tyrosine kinase inhibitor genistein. Am J Physiol 1995, 268:C886-C893.
24. Illek B., Fischer N. Flavonoids stimulate Cl conductance on human airway epithelium in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 1998, 275:L902-L910.
25. Illek B., Zhang L., Lewis N.C., Moss R.B., Dong J.Y., Fischer H. Defective function of the cystic fibrosis-causing missense mutation G551D is recovered by genistein. Am J Physiol 1999, 277:C833-C839.
26. Joe B., Vijaykumar M., Lokesh B.R. Biological properties of curcumin-cellular and molecular mechanisms of action. Crit Rev Food Sci Nutr 2004, 44:97-111.
27. Knowles M.R., Stutts M.J., Spock A., Fischer N., Gatzy J.T., Boucher R.C. Abnormal ion permeation through cystic fibrosis respiratory epithelium. Science 1983, 221:1067-1070.
28. Lansdell K., Cai Z., Kidd J.F., Sheppard D.N. Two mechanisms of genistein inhibition of cystic fibrosis transmembrane conductance regulator Cl- channels expressed in murine cell line. J Physiol 2000, 524:317-330.
29. Lewis H.A., Buchanan S.G., Burley S.K., Conners K., Dickey M., Dorwart M., et al. Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 2004, 23:282-293.
30. Li C., Ramjeesingh M., Wang W., Garami E., Hewryk M., Lee D., et al. ATPase activity of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 1996, 271:28463-28468.
31. Melin P., Thoreau V., Norez C., Bilan F., Kitzis A., Becq F. The cystic fibrosis mutation G1349D within the signature motif LSHGH of NBD2 abolishes the activation of CFTR chloride channels by genistein. Biochem Pharmacol 2004, 67:2187-2196.
32. Miquel J., Bernd A., Sempere J.M., Diaz-Alperi J., Ramirez A. The curcuma antioxidants: pharmacological effects and prospects for future clinical use. A review. Arch. Geronto. Geriatr 2002, 34:37-46.
33. Moran O., Galietta L.J., Zegarra-Moran O. Binding site of activators of the cystic fibrosis transmembrane conductance regulator in the nucleotide binding domains. Cell Mol Life Sci 2005, 62:446-460.
34. Noel S., Faveau C., Norez C., Rogier C., Mettey Y., Becq F. Discovery of pyrrolo[2,3-b]pyrazines derivatives as submicromolar affinity activators of wild type, G551D, and F508del cystic fibrosis transmembrane conductance regulator chloride channels. J Pharmacol Exp Ther 2006, 319:349-359.
35. Ono K., Hasegawa K., Naiki H., Yamada M. Curcumin has potent anti-amyloidogenic effects for Alzheimer's beta-amyloid fibrils in vitro. J Neurosci Res 2004, 75:742-750.
36. Pedemonte N., Sonawane N.D., Taddei A., Hu J., Zegarra-Moran O., Suen Y.F., et al. Phenylglycine and sulfonamide correctors of defective δF508 and G551D cystic fibrosis transmembrane conductance regulator chloride-channel gating. Mol Pharmacol 2005, 67:1797-1807.
37. Quinton P.M. Missing Cl conductance in cystic fibrosis. Am J Physiol 1986, 251:C649-C652.
38. Riordan J.R., Rommens J.M., Kerem B., Alon N., Rozmahel R., Grzelczak Z., et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
39. Schmidt A., Hughes L.K., Cai Z., Mendes F., Li H., Sheppard D.N., et al. Prolonged treatment of cells with genistein modulates the expression and function of the cystic fibrosis transmembrane conductance regulator. Br J Pharmacol 2008, 153:1311-1323.
40. Song Y., Sonawane N.D., Salinas D., Qian L., Pedemonte N., Galietta L.J., et al. Evidence against the rescue of defective DeltaF508-CFTR cellular processing by curcumin in cell culture and mouse models. J Biol Chem 2004, 279:40629-40633.
41. Van Goor F., Hadida S., Grootenhuis P.D., Burton B., Cao D., Neuberger T., et al. Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci USA 2009, 106:18825-18830.
42. Verkman A.S., Galietta L.J. Chloride channels as drug targets. Nat Rev Drug Discov 2009, 8:153-171.
43. Wang F., Zeltwanger S., Yang I.C.-H., Nairn A.C., Hwang T.-C. Actions of genistein on cystic fibrosis transmembrane conductance regulator channel gating. J Gen Physiol 1998, 111:477-490.
44. Wang W., Bernard K., Li G., Kirk K.L. Curcumin opens cystic fibrosis transmembrane conductance regulator channels by a novel mechanism that requires neither ATP binding nor dimerization of the nucleotide-binding domains. J Biol Chem 2007, 282:4533-4544.
45. Weinreich F., Wood P.G., Riordan J.R., Nagel G. Direct action of genistein on CFTR. Pflugers Arch 1997, 434:484-491.
46. Welsh M.J., Liedtke C.M. Chloride and potassium channels in cystic fibrosis airway epithelia. Nature 1986, 332:467-470.
47. Welsh M.J., Smith A.E. Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 1993, 73(7):1251-1254.
48. Zegarra-Moran O., Romio L., Folli C., Caci E., Becq F., Vierfond J.M., et al. Correction of G551D-CFTR transport defect in epithelial monolayers by genistein but not by CPX or MPB-07. Br J Pharmacol 2002, 137:504-512.