Impact of the cystic fibrosis mutation F508del-CFTR on renal cyst formation and growth

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 8, 2012, Pages

  Li, Hongyu ^a   Yang, Wanding ^a   Mendes, Filipa ^b,c   Amaral, Margarida D ^b,c   Sheppard, David N ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF LISBON   (Portugal)

^c NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

Author keywords

Autosomal dominant polycystic kidney disease; Chloride ion channel; Epithelial ion transport; Madin darby canine kidney (MDCK) epithelial cells; Small molecule CFTR modulators

Indexed keywords

CHLORIDE; COLLAGEN GEL; FORSKOLIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYSTIC FIBROSIS; EPITHELIUM CELL; GENE MUTATION; KIDNEY CYST; KIDNEY EPITHELIUM; NONHUMAN; PRIORITY JOURNAL;

EID: 84867719641     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00130.2012     Document Type: Article

References (70)

1. Aleksandrov AA, Kota P, Cui L, Jensen T, Alekseev AE, Reyes S, He L, Gentzsch M, Aleksandrov LA, Dokholyan NV, Riordan JR. Allo-steric modulation balances thermodynamic stability and restores function of AF508 CFTR. J Mol Biol 419: 41-60, 2012.
2. Amaral MD. Processing of CFTR: traversing the cellular maze-how much CFTR needs to go through to avoid cystic fibrosis? Pediatr Pulmonol 39: 479-491, 2005.
3. Brill SR, Ross KE, Davidow CJ, Ye M, Grantham JJ, Caplan M.J. Immunolocalization of ion transport proteins in human autosomal dominant polycystic kidney epithelial cells. Proc Natl Acad Sci USA 93: 10206-10211, 1996.
4. Cai ZW, Liu J, Li HY, Sheppard DN. Targeting F508del-CFTR to develop rational new therapies for cystic fibrosis. Acta Pharmacol Sin 32: 693-701, 2011.
5. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, Smith AE. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834, 1990.
6. Crawford I, Maloney PC, Zeitlin PL, Guggino WB, Hyde SC, Turley H, Gatter KC, Harris A, Higgins CF. Immunocytochemical localization of the cystic fibrosis gene product CFTR. Proc Natl Acad Sci USA 88: 9262-9266, 1991.
7. Dalemans W, Barbry P, Champigny G, Jallat S, Dott K, Dreyer D, Crystal RG, Pavirani A, Lecocq JP, Lazdunski M. Altered chloride ion channel kinetics associated with the AF508 cystic fibrosis mutation. Nature 354: 526-528, 1991.
8. Davidow CJ, Maser RL, Rome LA, Calvet JP, Grantham JJ. The cystic fibrosis transmembrane conductance regulator mediates transepithe-lial fluid secretion by human autosomal dominant polycystic kidney disease epithelium in vitro. Kidney Int 50: 208-218, 1996.
9. Delmas P. Polycystins: polymodal receptor/ion-channel cellular sensors. Pflügers Arch 451: 264-276, 2005.
10. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764, 1992.
11. Denning GM, Ostedgaard LS, Welsh MJ. Abnormal localization of cystic fibrosis transmembrane conductance regulator in primary cultures of cystic fibrosis airway epithelia. J Cell Biol 118: 551-559, 1992.
12. Gadsby DC, Nairn AC. Control of cystic fibrosis transmembrane conductance regulator channel gating by phosphorylation and nucleotide hydrolysis. Physiol Rev 79, Suppl 1: S77-S107, 1999.
13. Gadsby DC, Vergani P, Csanády L. The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440: 477-483, 2006.
14. Grantham JJ, Uchic M, Cragoe EJ Jr, Kornhaus J, Grantham JA, Donoso V, Mangoo-Karim R, Evan A, McAteer J. Chemical modification of cell proliferation and fluid secretion in renal cysts. Kidney Int 35: 1379-1389, 1989.
15. Hallows KR, Raghuram V, Kemp BE, Witters LA, Foskett JK. Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J Clin Invest 105: 1711-1721, 2000.
16. Hanaoka K, Devuyst O, Schwiebert EM, Wilson PD, Guggino WB. A role for CFTR in human autosomal dominant polycystic kidney disease. Am J Physiol Cell Physiol 270: C389-C399, 1996.
17. Hanaoka K, Guggino WB. cAMP regulates cell proliferation and cyst formation in autosomal polycystic kidney disease cells. J Am Soc Nephrol 11: 1179-1187, 2000.
18. Husted RF, Volk KA, Sigmund RD, Stokes JB. Anion secretion by the inner medullary collecting duct: evidence for involvement of the cystic fibrosis transmembrane conductance regulator. J Clin Invest 95: 644-650, 1995.
19. Hwang TC, Sheppard DN. Molecular pharmacology of the CFTR Cl~ channel. Trends Pharmacol Sci 20: 448-453, 1999.
20. Ikeda M, Fong P, Cheng J, Boletta A, Qian F, Zhang XM, Cai H, Germino GG, Guggino WB. A regulatory role of polycystin-1 on cystic fibrosis transmembrane conductance regulator plasma membrane expression. Cell Physiol Biochem 18: 9-20, 2006.
21. Jouret F, Bernard A, Hermans C, Dom G, Terryn S, Leal T, Lebecque P, Cassiman JJ, Scholte BJ, de Jonge HR, Courtoy PJ, Devuyst O. Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney. J Am Soc Nephrol 18: 707-718, 2007.
22. Kappes JC, Wu X, Wakefield JK. Production of trans-lentiviral vector with predictable safety. Methods Mol Med 76: 449-465, 2003.
23. Kim Chiaw P, Wellhauser L, Huan LJ, Ramjeesingh M, Bear CE. A chemical corrector modifies the channel function of F508del-CFTR. Mol Pharmacol 78: 411-418, 2010.
24. Kopeikin Z, Sohma Y, Li M, Hwang TC. On the mechanism of CFTR inhibition by a thiazolidinone derivative. J Gen Physiol 136: 659-671, 2010.
25. Krouse ME, Wine JJ. Evidence that CFTR channels can regulate the open duration of other channels: cooperativity. J Membr Biol 182: 223-232, 2001.
26. Kunzelmann K. CFTR: interacting with everything? News Physiol Sci 16: 167-170, 2001.
27. LeSimple P, Liao J, Robert R, Gruenert DC, Hanrahan JW. Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J Physiol 588: 1195-1209, 2010.
28. Li H, Findlay IA, Sheppard DN. The relationship between cell proliferation, Cl~ secretion, and renal cyst growth: a study using CFTR inhibitors. Kidney Int 66: 1926-1938, 2004.
29. Li H, Sheppard DN. Therapeutic potential of cystic fibrosis transmembrane conductance regulator (CFTR) inhibitors in polycystic kidney disease. BioDrugs 23: 203-216, 2009.
30. Loo TW, Bartlett MC, Clarke DM. Correctors enhance maturation of AF508 CFTR by promoting interactions between the two halves of the molecule. Biochemistry 48: 9882-9890, 2009.
31. Lukacs GL, Chang XB, Bear C, Kartner N, Mohamed A, Riordan JR, Grinstein S. The AF508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane: determination of functional half-lives on transfected cells. J Biol Chem 268: 21592-21598, 1993.
32. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJV, Verkman AS. Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110: 1651-1658, 2002.
33. McCarty NA, McDonough S, Cohen BN, Riordan JR, Davidson N, Lester HA. Voltage-dependent block of the cystic fibrosis transmembrane conductance regulator Cl~ channel by two closely related arylaminoben-zoates. J Gen Physiol 102: 1-23, 1993.
34. Mendes F, Wakefield J, Bachhuber T, Barroso M, Bebok Z, Penque D, Kunzelmann K, Amaral MD. Establishment and characterization of a novel polarized MDCK epithelial cellular model for CFTR studies. Cell Physiol Biochem 16: 281-290, 2005.
35. Mohamed A, Ferguson D, Seibert FS, Cai HM, Kartner N, Grinstein S, Riordan JR, Lukacs GL. Functional expression and apical localization of the cystic fibrosis transmembrane conductance regulator in MDCK I cells. Biochem J 322: 259-265, 1997.
36. Morales MM, Carroll TP, Morita T, Schwiebert EM, Devuyst O, Wilson PD, Lopes AG, Stanton BA, Dietz HC, Cutting GR, Guggino WB. Both the wild type and a functional isoform of CFTR are expressed in kidney. Am J Physiol Renal Fluid Electrolyte Physiol 270: F1038-F1048, 1996.
37. Nofziger C, Brown KK, Smith CD, Harrington W, Murray D, Bisi J, Ashton TT, Maurio FP, Kalsi K, West TA, Baines D, Blazer-Yost BL. PPAR-y agonists inhibit vasopressin-mediated anion transport in the MDCK-C7 cell line. Am J Physiol Renal Physiol 297: F55-F62, 2009.
38. O'Sullivan DA, Torres VE, Gabow PA, Thibodeau SN, King BF, Bergstralh EJ. Cystic fibrosis and the phenotypic expression of autosomal dominant polycystic kidney disease. Am J Kidney Dis 32: 976-983, 1998.
39. Okiyoneda T, Barrière H, Bagdány M, Rabeh WM, Du K, Höhfeld J, Young JC, Lukacs GL. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 329: 805-810, 2010.
40. Pedemonte N, Tomati V, Sondo E, Galietta LJV. Influence of cell background on pharmacological rescue of mutant CFTR. Am J Physiol Cell Physiol 298: C866-C874, 2010.
41. Persu A, Devuyst O, Lannoy N, Materne R, Brosnahan G, Gabow PA, Pirson Y, Verellen-Dumoulin C. CF gene and cystic fibrosis transmembrane conductance regulator expression in autosomal dominant polycystic kidney disease. J Am Soc Nephrol 11: 2285-2296, 2000.
42. Raghuram V, Mak DOD, Foskett JK. Regulation of cystic fibrosis transmembrane conductance regulator single-channel gating by bivalent PDZ-domain-mediated interaction. Proc Natl Acad Sci USA 98: 1300-1305, 2001.
43. Riordan JR, Rommens JM, Kerem BS, Alon N, Rozmahel R, Grzel-czak Z, Zielenski J, Lok S, Plavsic N, Chou JL, Drumm ML, Iannuzzi MC, Collins FS, Tsui LC. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073, 1989.
44. Schmidt A, Hughes LK, Cai Z, Mendes F, Li H, Sheppard DN, Amaral MD. Prolonged treatment of cells with genistein modulates the expression and function of the cystic fibrosis transmembrane conductance regulator. Br J Pharmacol 153: 1311-1323, 2008.
45. Schultz BD, Frizzell RA, Bridges RJ. Rescue of dysfunctional AF508-CFTR chloride channel activity by IBMX. J Membr Biol 170: 51-66, 1999.
46. Schultz BD, Singh AK, Devor DC, Bridges RJ. Pharmacology of CFTR chloride channel activity. Physiol Rev 79, Suppl 1: S109-S144, 1999.
47. Schwiebert EM, Benos DJ, Egan ME, Stutts MJ, Guggino WB. CFTR is a conductance regulator as well as a chloride channel. Physiol Rev 79, Suppl 1: S145-S166, 1999.
48. Shan J, Liao J, Huang J, Robert R, Palmer ML, Fahrenkrug SC, O'Grady SM, Hanrahan JW. Bicarbonate-dependent chloride transport drives fluid secretion by the human airway epithelial cell line Calu-3. J Physiol [Epub ahead of print].
49. Shen MR, Droogmans G, Eggermont J, Voets T, Ellory JC, Nilius B. Differential expression of volume-regulated anion channels during cell cycle progression of human cervical cancer cells. J Physiol 529: 385-394, 2000.
50. Sheppard DN, Ostedgaard LS, Rich DP, Welsh MJ. The amino-terminal portion of CFTR forms a regulated Cl~ channel. Cell 76: 1091-1098, 1994.
51. Sheppard DN, Ostedgaard LS, Winter MC, Welsh MJ. Mechanism of dysfunction of two nucleotide binding domain mutations in cystic fibrosis transmembrane conductance regulator that are associated with pancreatic sufficiency. EMBO J 14: 876-883, 1995.
52. Sheppard DN, Robinson KA. Mechanism of glibenclamide inhibition of cystic fibrosis transmembrane conductance regulator Cl~ channels expressed in a murine cell line. J Physiol 503: 333-346, 1997.
53. Sheppard DN, Welsh MJ. Structure and function of the cystic fibrosis transmembrane conductance regulator chloride channel. Physiol Rev 79, Suppl 1: S23-S45, 1999.
54. Stanton BA. Cystic fibrosis transmembrane conductance regulator (CFTR) and renal function. Wien Klin Wochenschr 109: 457-464, 1997.
55. Sullivan LP, Wallace DP, Grantham JJ. Chloride and fluid secretion in polycystic kidney disease. J Am Soc Nephrol 9: 903-916, 1998.
56. Torres VE, Harris PC, Pirson Y. Autosomal dominat polycystic kidney disease. Lancet 369: 1287-1301, 2007.
57. Uchida S, Sasaki S. Function of chloride channels in the kidney. Annu Rev Physiol 67: 759-778, 2005.
58. Van Goor F, Hadida S, Grootenhuis PDJ, Burton B, Stack JH, Straley KS, Decker CJ, Miller M, McCartney J, Olson ER, Wine JJ, Frizzell RA, Ashlock M, Negulescu PA. Correction of the F508del-CFTR protein processing defect in vitro by the investigational drug VX-809. Proc Natl Acad Sci USA 108: 18843-18848, 2011.
59. Van Goor F, Straley KS, Cao D, González 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 PDJ, Negulescu P. Rescue of AF508-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.
60. Vennekens R, Trouet D, Vankeerberghen A, Voets T, Cuppens H, Eggermont J, Cassiman JJ, Droogmans G, Nilius B. Inhibition of volume-regulated anion channels by expression of the cystic fibrosis transmembrane conductance regulator. J Physiol 515: 75-85, 1999.
61. Verkman AS, Galietta LJV. Chloride channels as drug targets. Nat Rev Drug Discov 8: 153-171, 2009.
62. Wang S, Yue H, Derin RB, Guggino WB, Li M. Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103: 169-179, 2000.
63. Wang Y, Bartlett MC, Loo TW, Clarke DM. Specific rescue of cystic fibrosis transmembrane conductance regulator processing mutants using pharmacological chaperones. Mol Pharmacol 70: 297-302, 2006.
64. Welsh MJ, Ramsey BW, Accurso F, Cutting GR. Cystic fibrosis. In: The Metabolic and Molecular Basis of Inherited Disease, edited by Scriver CR, Beaudet AL, Sly WS, Valle D. New York: McGraw-Hill, 2001.
65. Welsh MJ, Smith AE. Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73: 1251-1254, 1993.
66. Wilson PD, Goilav B. Cystic disease of the kidney. Annu Rev Pathol Mech Dis 2: 341-368, 2007.
67. Xu N, Glockner JF, Rossetti S, Babovic-Vuksanovic D, Harris PC, Torres VE. Autosomal dominant polycystic kidney disease coexisting with cystic fibrosis. J Nephrol 19: 529-534, 2006.
68. Yamaguchi T, Pelling JC, Ramaswamy NT, Eppler JW, Wallace DP, Nagao S, Rome LA, Sullivan LP, Grantham JJ. cAMP stimulates the in vitro proliferation of renal cyst epithelial cells by activating the extracellular signal-regulated kinase pathway. Kidney Int 57: 1460-1471, 2000.
69. Yang B, Sonawane ND, Zhao D, Somlo S, Verkman AS. Small-molecule CFTR inhibitors slow cyst growth in polycystic kidney disease. J Am Soc Nephrol 19: 1300-1310, 2008.
70. Ye M, Grantham JJ. The secretion of fluid by renal cysts from patients with autosomal dominant polycystic kidney disease. N Engl J Med 329: 310-313, 1993.