CFTR directly mediates nucleotide-regulated glutathione flux

EMBO Journal

Volumn 22, Issue 9, 2003, Pages 1981-1989

  Kogan, Ilana ^a,b   Ramjeesingh, Mohabir ^a   Li, Canhui ^a   Kidd, Jackie F ^a   Wang, Yanchun ^a   Leslie, Elaine M ^c   Cole, Susan P C ^c   Bear, Christine E ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

CFTR; Glutathione; Purified protein; R347D pore mutant; Walker A mutants

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE MAGNESIUM; GLUTATHIONE; MUTANT PROTEIN; NUCLEOTIDE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

AIRWAY; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROLYSIS; MEMBRANE VESICLE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; PROTEOLIPOSOME; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUTATHIONE; PROTEOLIPIDS; RECOMBINANT PROTEINS; SPODOPTERA;

ANIMALIA;

EID: 0038369932     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg194     Document Type: Article

References (63)

1. - salvage mechanisms in model systems and the mouse pancreatic duct. J. Biol. Chem., 276, 17236-17243.
2. Al-Nakkash, L., Hu, S., Li, M. and Hwang, T.C. (2001) A common mechanism for cystic fibrosis transmembrane conductance regulator protein activation by genistein and benzimidazolone analogs. J. Pharmacol. Exp. Ther., 296, 464-472.
3. Aleksandrov, A.A., Chang, X., Aleksandrov, L. and Riordan, J.R. (2000) The non-hydrolytic pathway of cystic fibrosis transmembrane conductance regulator ion channel gating. J. Physiol., 528, 259-265.
4. Aleksandrov, L., Aleksandrov, A.A., Chang, X.B. and Riordan, J.R. (2002) The first nucleotide binding domain of cystic fibrosis transmembrane conductance regulator is a site of stable nucleotide interaction, whereas the second is a site of rapid turnover. J. Biol. Chem., 277, 15419-15425.
5. Anderson, M., Gregory, R., Thompson, S., Souza, D., Paul, S., Mulligan, R., Smith, A. and Welsh, M. (1991a) Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science, 253, 202-205.
6. Anderson, M.P., Berger, H.A., Rich, D.P., Gregory, R.J., Smith, A.E. and Welsh, M.J. (1991b) Nucleoside triphosphates are required to open the CFTR chloride channel. Cell, 67, 775-784.
7. Bear, C.E., Li, C., Kartner, N., Bridges, R., Jensen, T., Ramjeesingh, M. and Riordan, J. (1992) Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR). Cell, 68, 809-818.
8. Behr, J., Degenkolb, B., Maier, K., Braun, B., Beinert, T., Krombach, F., Vogelmeier, C. and Fruhmann, G. (1995) Increased oxidation of extracellular glutathione by bronchoalveolar inflammatory cells in diffuse fibrosing alveolitis. Eur. Respir. J., 8, 1286-1292.
9. Boat, T.F., Welsh, M.J. and Beaudet, A.L. (1989) Cystic fibrosis. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic Basis of Inherited Disease. McGraw-Hill, New York, NY, pp. 2649-2680.
10. Boucher, R.C. (1999) Molecular insights into the physiology of the 'thin film' of airway surface liquid. J. Physiol., 516, 631-638.
11. Cantin, A.M., North, S.L., Hubbard, R.C. and Crystal, R.G. (1987) Normal alveolar epithelial lining fluid contains high levels of glutathione. J. Appl. Physiol., 63, 152-157.
12. Chang, G. and Roth, C.B. (2001) Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science, 293, 1793-1800.
13. Cherrington, N.J., Hartley, D.P., Li, N., Johnson, D.R. and Klaassen, C.D. (2002) Organ distribution of multidrug resistance proteins 1, 2 and 3 (Mrp1, 2 and 3) mRNA and hepatic induction of Mrp3 by constitutive androstane receptor activators in rats. J. Pharmacol. Exp. Ther., 300, 97-104.
14. Cole, S.P. et al. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 258, 1650-1654.
15. Cotten, J.F. and Welsh, M.J. (1999) Cystic fibrosis-associated mutations at arginine 347 alter the pore architecture of CFTR. Evidence for disruption of a salt bridge. J. Biol. Chem., 274, 5429-5435.
16. Droge, W., Eck, H.P., Gmunder, H. and Mihm, S. (1991) Modulation of lymphocyte functions and immune responses by cysteine and cysteine derivatives. Am. J. Med., 91, 140S-144S.
17. - channels by protein kinase A corrected by insertion of CFTR. Nature, 358, 581-584.
18. Frizzell, R.A. (1999) Ten years with CFTR. Physiol. Rev., 79, S1-S2.
19. - channels: a newly emerging anion transport family. Pflugers Arch., 443, S107-110.
20. Gao, L., Kim, K.J., Yankaskas, J.R. and Forman, H.J. (1999) Abnormal glutathione transport in cystic fibrosis airway epithelia. Am. J. Physiol., 277, L113-L118.
21. Gunderson, K.L. and Kopito, R.R. (1995) Conformational states of CFTR associated with channel gating: the role of ATP binding and hydrolysis. Cell, 82, 231-239.
22. Gyomorey, K., Rozmahel, R. and Bear, C.E. (2000) Amelioration of intestinal disease severity in cystic fibrosis mice is associated with improved chloride secretory capacity. Pediatr. Res., 48, 731-734.
23. Higgins, C. (1995) The ABC of channel regulation. Cell, 82, 693-696.
24. Hudson, V.M. (2001) Rethinking cystic fibrosis pathology: the critical role of abnormal reduced glutathione (GSH) transport caused by CFTR mutation. Free Radic. Biol. Med., 30, 1440-1461.
25. - channel. Trends Pharmacol. Sci., 20, 448-453.
26. - channel gating by ATP binding and hydrolysis. Proc. Natl Acad. Sci. USA, 97, 8675-8680.
27. Jovov, B., Ismailov, I.I., Berdiev, B.K., Fuller, C.M., Sorscher, E.J., Dedman, J.R., Kaetzel, M.A. and Benos, D.J. (1995) Interaction between cystic fibrosis transmembrane conductance regulator and outwardly rectified chloride channels. J. Biol. Chem., 270, 29194-29200.
28. Jungas, T., Motta, I., Duffieux, F., Fanen, P., Stoven, V. and Ojcius, D.M. (2002) Glutathione levels and BAX activation during apoptosis due to oxidative stress in cells expressing wild-type and mutant CFTR. J. Biol. Chem., 277, 27912-27918.
29. Kelly, F.J. (1999) Gluthathione: in defence of the lung. Food Chem. Toxicol., 37, 963-966.
30. Khan, T.Z., Wagener, J.S., Bost, T., Martinez, J., Accurso, F.J. and Riches, D.W. (1995) Early pulmonary inflammation in infants with cystic fibrosis. Am. J. Respir. Crit. Care Med., 151, 1075-1082.
31. Kogan, I., Ramjeesingh, M., Huan, L.J., Wang, Y. and Bear, C.E. (2001) Perturbation of the pore of the cystic fibrosis transmembrane conductance regulator (CFTR) inhibits its ATPase activity. J. Biol. Chem., 276, 11575-11581.
32. Kogan, I., Ramjeesingh, M., Li, C. and Bear, C.E. (2002) Studies of the molecular basis for cystic fibrosis using purified reconstituted CFTR protein. Methods Mol. Med., 70, 143-157.
33. - exchange by cystic fibrosis transmembrane conductance regulator expressed in NIH 3T3 and HEK 293 cells. J. Biol. Chem., 274, 3414-3421.
34. Li, C., Ramjeesingh, M. and Bear, C.B. (1996) Purified cystic fibrosis transmembrane conductance regulator (CFTR) does not function as an ATP channel. J. Biol. Chem., 271, 11623-11626.
35. Linsdell, P. and Hanrahan, J. (1998a) Adenosine triphosphate-dependent asymmetry of anion permeation in the cystic fibrosis transmembrane conductance regulator chloride channel. J. Gen. Physiol., 111, 601-614.
36. Linsdell, P. and Hanrahan, J. (1998b) Glutathione permeability of CFTR. Am. J. Physiol., 275, C323-C326.
37. Locher, K.P., Lee, A.T. and Rees, D.C. (2002) The E.coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science, 296, 1091-1098.
38. Loe, D.W., Almquist, K.C., Deeley, R.G. and Cole, S.P. (1996) Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J. Biol. Chem., 271, 9675-9682.
39. Loe, D.W., Oleschuk, C.J., Deeley, R.G. and Cole, S.P. (2000) Structure-activity studies of verapamil analogs that modulate transport of leukotriene C(4) and reduced glutathione by multidrug resistance protein MRP1. Biochem. Biophys. Res. Commun., 275, 795-803.
40. - channel. J. Clin. Invest., 102, 1986-1993.
41. Ogura, T., Furukawa, T., Toyozaki, T., Yamada, K., Zheng, Y.J., Katayama, Y., Nakaya, H. and Inagaki, N. (2002) ClC-3B, a novel ClC-3 splicing variant that interacts with EBP50 and facilitates expression of CFTR-regulated ORCC. FASEB J., 16, 863-865.
42. Paradiso, A.M., Ribeiro, C.M. and Boucher, R.C. (2001) Polarized signaling via purinoceptors in normal and cystic fibrosis airway epithelia. J. Gen. Physiol., 117, 53-67.
43. Rahman, I. and MacNee, W. (2000) Oxidative stress and regulation of glutathione in lung inflammation. Eur. Respir. J., 16, 534-554.
44. Ramjeesingh, M., Garami, E., Galley, K., Li, C., Wang, Y. and Bear, C.E. (1999a) Purification and reconstitution of epithelial chloride channel cystic fibrosis transmembrane conductance regulator. Methods Enzymol., 294, 227-246.
45. Ramjeesingh, M., Li, C., Garami, E., Huan, L.J., Galley, K., Wang, Y. and Bear, C.E. (1999b) Walker mutations reveal loose relationship between catalytic and channel-gating activities of purified CFTR (cystic fibrosis transmembrane conductance regulator). Biochemistry, 38, 1463-1468.
46. - conductances. JOP, 2, 212-218.
47. Riordan, J.R., Deuchars, K., Kartner, N., Alon, N., Trent, J. and Ling, V. (1985) Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature, 316, 817-819.
48. Riordan, J. et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science, 245, 1066-1073.
49. Rosenberg, M.F. et al. (2001) Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J., 20, 5615-5625.
50. Roum, J.H., Buhl, R., McElvaney, N.G., Borok, Z. and Crystal, R.G. (1993) Systemic deficiency of glutathione in cystic fibrosis. J. Appl. Physiol., 75, 2419-2424.
51. Schultz, B.D., Bridges, R.J. and Frizzell, R.A. (1996) Lack of conventional ATPase properties in CFTR chloride channel gating. J. Membr. Biol., 151, 63-75.
52. Schwiebert, E.M., Flotte, T., Cutting, G.R. and Guggino, W.B. (1994) Both CFTR and outwardly rectifying chloride channels contribute to cAMP-stimulated whole cell chloride currents. Am. J. Physiol., 266, C1464-C1477.
53. Schwiebert, E.M., Benos, D.J., Egan, M.E., Stutts, M.J. and Guggino, W.B. (1999) CFTR is a conductance regulator as well as a chloride channel. Physiol. Rev., 79, S145-S166.
54. Smith, T.K., Ikeda, Y., Fujii, J., Taniguchi, N. and Meister, A. (1995) Different sites of acivicin binding and inactivation of γ-glutamyl transpeptidases. Proc. Natl Acad. Sci. USA, 92, 2360-2364.
55. Stutts, M.J., Caneesa, C., Olsen, J., Hamrick, M., Cohn, J., Rossier, B., Rossier, R. and Boucher, B. (1995) CFTR as a cAMP-dependent regulator of sodium channels. Science, 269, 847-850.
56. - channel in CHO cells stably expressing the cystic fibrosis gene. Nature, 352, 628-631.
57. Tabcharani, J., Rommens, J., Hou, Y., Chang, X., Tsui, L., Riordan, J. and Hanrahan, J. (1993) Multi-ion pore behaviour in the CFTR chloride channel. Nature, 366, 79-82.
58. - currents in guinea-pig paneth cells without relevant evidence for CFTR expression. J. Physiol., 512, 765-777.
59. Velsor, L.W., van Heeckeren, A. and Day, B.J. (2001) Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am. J. Physiol. Lung Cell Mol. Physiol., 281, L31-L38.
60. Venglarik, C.J., Singh, A.K. and Bridges, R.J. (1994) Comparison of -nitro versus -amino 4,4′-substituents of disulfonic stilbenes as chloride channel blockers. Mol. Cell. Biochem., 140, 137-146.
61. - channels. J. Gen. Physiol., 121, 17-36.
62. Wright, S.R., Boag, A.H., Valdimarsson, G., Hipfner, D.R., Campling, B.G., Cole, S.P. and Deeley, R.G. (1998) Immunohistochemical detection of multidrug resistance protein in human lung cancer and normal lung. Clin. Cancer Res., 4, 2279-2289.
63. - channels in mammalian cardiac myocytes. Circ. Res., 81, 101-109.