The K + channel opener 1-EBIO potentiates residual function of mutant CFTR in rectal biopsies from cystic fibrosis patients

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Roth, Eva K ^a   Hirtz, Stephanie ^a   Duerr, Julia ^a   Wenning, Daniel ^a   Eichler, Irmgard ^b   Seydewitz, Hans H ^c   Amaral, Margarida D ^d,e   Mall, Marcus A ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF FREIBURG   (Germany)

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

^e UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

1 ETHYL 2 BENZIMIDAZOLONE; CAMP DEPENDENT POTASSIUM CHANNEL; CHLORIDE ION; CLOTRIMAZOLE; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCNN4; POTASSIUM CHANNEL STIMULATING AGENT; UNCLASSIFIED DRUG; 1 ETHYL 2 BENZIMIDAZOLINONE; 1-ETHYL-2-BENZIMIDAZOLINONE; BENZIMIDAZOLE DERIVATIVE; CALCIUM; CHLORIDE; CHOLINE; CYCLIC AMP; MUTANT PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ADOLESCENT; ADULT; ARTICLE; CELL SURFACE; CFTR GENE; CHANNEL GATING; CHILD; CHLORIDE CONDUCTANCE; CHLORIDE TRANSPORT; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE; GENE MUTATION; HUMAN; HUMAN TISSUE; INFANT; PRESCHOOL CHILD; RECTUM BIOPSY; RECTUM MUCOSA; SCHOOL CHILD; BIOPSY; DRUG EFFECT; EPITHELIUM; GENETICS; GENOTYPE; IN VITRO STUDY; METABOLISM; MIDDLE AGED; PATHOLOGY; RECTUM;

ADOLESCENT; ADULT; BENZIMIDAZOLES; BIOPSY; CALCIUM; CHILD; CHILD, PRESCHOOL; CHLORIDES; CHOLINE; CYCLIC AMP; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIUM; GENOTYPE; HUMANS; ION CHANNEL GATING; MIDDLE AGED; MUTANT PROTEINS; POTASSIUM CHANNELS; RECTUM; YOUNG ADULT;

EID: 80052328287     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024445     Document Type: Article

References (53)

1. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, et al. (1989) Identification of the cystic fibrosis gene: genetic analysis. Science 245: 1073-1080.
2. Welsh MJ, Ramsey BW, Accurso F, Cutting GR, (2001) Cystic fibrosis. In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The Metabolic & Molecular Bases of Inherited Disease. 8th ed New York McGraw-Hill pp. 5121-5188.
3. Riordan JR, (2008) CFTR function and prospects for therapy. Annu Rev Biochem 77: 701-726.
4. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, et al. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834.
5. Hamosh A, Trapnell BC, Zeitlin PL, Montrose-Rafizadeh C, Rosenstein BJ, et al. (1991) Severe deficiency of cystic fibrosis transmembrane conductance regulator messenger RNA carrying nonsense mutations R553X and W1316X in respiratory epithelial cells of patients with cystic fibrosis. J Clin Invest 88: 1880-1885.
6. Sheppard DN, Rich DP, Ostedgaard LS, Gregory RJ, Smith AE, et al. (1993) Mutations in CFTR associated with mild-disease-form Cl- channels with altered pore properties. Nature 362: 160-164.
7. Welsh MJ, Smith AE, (1993) Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73: 1251-1254.
8. Kunzelmann K, Mall M, (2002) Electrolyte transport in the mammalian colon: mechanisms and implications for disease. Physiol Rev 82: 245-289.
9. Boucher RC, (2007) Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu Rev Med 58: 157-170.
10. Sloane PA, Rowe SM, (2010) Cystic fibrosis transmembrane conductance regulator protein repair as a therapeutic strategy in cystic fibrosis. Curr Opin Pulm Med 16: 591-597.
11. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Cao D, et al. (2009) Rescue of CF airway epithelial cell function in vitro by a CFTR potentiator, VX-770. Proc Natl Acad Sci U S A 106: 18825-18830.
12. Accurso FJ, Rowe SM, Clancy JP, Boyle MP, Dunitz JM, et al. (2010) Effect of VX-770 in persons with cystic fibrosis and the G551D-CFTR mutation. N Engl J Med 363: 1991-2003.
13. Knowles MR, Paradiso AM, Boucher RC, (1995) In vivo nasal potential difference: techniques and protocols for assessing efficacy of gene transfer in cystic fibrosis. Hum Gene Ther 6: 445-455.
14. Du M, Liu X, Welch EM, Hirawat S, Peltz SW, et al. (2008) PTC124 is an orally bioavailable compound that promotes suppression of the human CFTR-G542X nonsense allele in a CF mouse model. Proc Natl Acad Sci U S A 105: 2064-2069.
15. Kerem E, Hirawat S, Armoni S, Yaakov Y, Shoseyov D, et al. (2008) Effectiveness of PTC124 treatment of cystic fibrosis caused by nonsense mutations: a prospective phase II trial. Lancet 372: 719-727.
16. Noone PG, Zhou Z, Silverman LM, Jowell PS, Knowles MR, et al. (2001) Cystic fibrosis gene mutations and pancreatitis risk: relation to epithelial ion transport and trypsin inhibitor gene mutations. Gastroenterology 121: 1310-1319.
17. Hirtz S, Gonska T, Seydewitz HH, Thomas J, Greiner P, et al. (2004) CFTR Cl- channel function in native human colon correlates with the genotype and phenotype in cystic fibrosis. Gastroenterology 127: 1085-1095.
18. MacVinish LJ, Hickman ME, Mufti DA, Durrington HJ, Cuthbert AW, (1998) Importance of basolateral K+ conductance in maintaining Cl- secretion in murine nasal and colonic epithelia. J Physiol 510: 237-247.
19. Mall M, Bleich M, Greger R, Schürlein M, Kühr J, et al. (1998) Cholinergic ion secretion in human colon requires co-activation by cAMP. Am J Physiol 275: G1274-G1281.
20. Devor DC, Singh AK, Gerlach AC, Frizzell RA, Bridges RJ, (1997) Inhibition of intestinal Cl- secretion by clotrimazole: direct effect on basolateral membrane K+ channels. Am J Physiol 273: C531-C540.
21. Joiner WJ, Wang LY, Tang MD, Kaczmarek LK, (1997) hSK4, a member of a novel subfamily of calcium-activated potassium channels. Proc Natl Acad Sci 94: 11013-11018.
22. Warth R, Hamm K, Bleich M, Kunzelmann K, von Hahn T, et al. (1999) Molecular and functional characterization of the small Ca(2+)-regulated K+ channel (rSK4) of colonic crypts. Pflügers Arch 438: 437-444.
23. Flores CA, Melvin JE, Figueroa CD, Sepulveda FV, (2007) Abolition of Ca2+-mediated intestinal anion secretion and increased stool dehydration in mice lacking the intermediate conductance Ca2+-dependent K+ channel Kcnn4. J Physiol 583: 705-717.
24. Matos JE, Sausbier M, Beranek G, Sausbier U, Ruth P, et al. (2007) Role of cholinergic-activated KCa1.1 (BK), KCa3.1 (SK4) and KV7.1 (KCNQ1) channels in mouse colonic Cl- secretion. Acta Physiol (Oxf) 189: 251-258.
25. Lohrmann E, Burhoff I, Nitschke RB, Lang H-J, Mania D, et al. (1995) A new class of inhibitors of cAMP-mediated Cl- secretion in rabbit colon, acting by the reduction of cAMP-activated K+ conductance. Pflugers Arch 429: 517-530.
26. Bleich M, Briel M, Busch AE, Lang H-J, Gerlach U, et al. (1997) KVLQT channels are inhibited by the K+ channel blocker 293B. Pflügers Arch 434: 499-501.
27. Schroeder BC, Waldegger S, Fehr S, Bleich M, Warth R, et al. (2000) A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature 403: 196-199.
28. Vallon V, Grahammer F, Volkl H, Sandu CD, Richter K, et al. (2005) KCNQ1-dependent transport in renal and gastrointestinal epithelia. Proc Natl Acad Sci U S A 102: 17864-17869.
29. Preston P, Wartosch L, Gunzel D, Fromm M, Kongsuphol P, et al. (2010) Disruption of the K+ channel beta-subunit KCNE3 reveals an important role in intestinal and tracheal Cl- transport. J Biol Chem 285: 7165-7175.
30. Heitzmann D, Warth R, (2008) Physiology and pathophysiology of potassium channels in gastrointestinal epithelia. Physiol Rev 88: 1119-1182.
31. Devor DC, Singh AK, Frizzell RA, Bridges RJ, (1996) Modulation of Cl- secretion by benzimidazolones. I. Direct activation of a Ca2+- dependent K+ channel. Am J Physiol 271: L775-L784.
32. Devor DC, Singh AK, Bridges RJ, Frizzell RA, (1996) Modulation of Cl- secretion by benzimidazolones. II. Coordinate regulation of apical GCl and basolateral GK. Am J Physiol 271: L785-L795.
33. Cuthbert AW, Hickman ME, Thorn P, MacVinish LJ, (1999) Activation of Ca(2+)- and cAMP-sensitive K(+) channels in murine colonic epithelia by 1-ethyl-2-benzimidazolone. Am J Physiol 277: C111-C120.
34. MacVinish LJ, Keogh J, Cuthbert AW, (2001) EBIO, an agent causing maintained epithelial chloride secretion by co-ordinate actions at both apical and basolateral membranes. Pflugers Arch 443 (Suppl 1): S127-S131.
35. Cuthbert AW, (2001) Assessment of CFTR chloride channel openers in intact normal and cystic fibrosis murine epithelia. Br J Pharmacol 132: 659-668.
36. Mall M, Kreda SM, Mengos A, Jensen TJ, Hirtz S, et al. (2004) The DeltaF508 mutation results in loss of CFTR function and mature protein in native human colon. Gastroenterology 126: 32-41.
37. Rosenstein BJ, Cutting GR, (1998) The diagnosis of cystic fibrosis: a consensus statement. J Pediatr 132: 589-595.
38. De Boeck K, Wilschanski M, Castellani C, Taylor C, Cuppens H, et al. (2006) Cystic fibrosis: terminology and diagnostic algorithms. Thorax 61: 627-635.
39. Wallis C, Leung T, Cubitt D, Reynolds A, (1997) Stool elastase as a diagnostic test for pancreatic function in children with cystic fibrosis. Lancet 350: 1001.
40. Mall M, Wissner A, Seydewitz HH, Kuehr J, Brandis M, et al. (2000) Defective cholinergic Cl- secretion and detection of K+ secretion in rectal biopsies from cystic fibrosis patients. Am J Physiol Gastrointest Liver Physiol 278: G617-G624.
41. Mall M, Wissner A, Seydewitz HH, Hübner M, Kuehr J, et al. (2000) Effect of genistein on native epithelial tissue from normal individuals and CF patients and on ion channels expressed in Xenopus oocytes. Br J Pharmacol 130: 1884-1892.
42. Mall M, Gonska T, Thomas J, Schreiber R, Seydewitz HH, et al. (2003) Modulation of Ca2+-activated Cl- secretion by basolateral K+ channels in human normal and cystic fibrosis airway epithelia. Pediatr Res 53: 608-618.
43. Mall M, Wissner A, Schreiber R, Kuehr J, Seydewitz HH, et al. (2000) Role of KVLQT1 in cAMP-mediated Cl- secretion in human airway epithelia. Am J Respir Cell Molec Biol 23: 283-289.
44. von Hahn T, Thiele I, Zingaro L, Hamm K, Garcia-Alzamora M, et al. (2001) Characterisation of the rat SK4/IK1 K(+) channel. Cell Physiol Biochem 11: 219-230.
45. Devor DC, Bridges RJ, Pilewski JM, (2000) Pharmacological modulation of ion transport across wild-type and ΔF508 CFTR-expressing human bronchial epithelia. Am J Physiol Cell Physiol 279: C461-C479.
46. Becq F, (2006) On the discovery and development of CFTR chloride channel activators. Curr Pharm Des 12: 471-484.
47. Verkman AS, Lukacs GL, Galietta LJ, (2006) CFTR chloride channel drug discovery--inhibitors as antidiarrheals and activators for therapy of cystic fibrosis. Curr Pharm Des 12: 2235-2247.
48. Singh S, Syme CA, Singh AK, Devor DC, Bridges RJ, (2001) Benzimidazolone activators of chloride secretion: potential therapeutics for cystic fibrosis and chronic obstructive pulmonary disease. J Pharmacol Exp Ther 296: 600-611.
49. Namkung W, Padmawar P, Mills AD, Verkman AS, (2008) Cell-based fluorescence screen for K+ channels and transporters using an extracellular triazacryptand-based K+ sensor. J Am Chem Soc 130: 7794-7795.
50. Veeze HJ, Sinaasappel M, Bijman J, Bouquet J, De Jonge HR, (1991) Ion transport abnormalities in rectal suction biopsies from childern with cystic fibrosis. Gastroenterology 101: 398-403.
51. Derichs N, Sanz J, Von Kanel T, Stolpe C, Zapf A, et al. (2010) Intestinal current measurement for diagnostic classification of patients with questionable cystic fibrosis: validation and reference data. Thorax 65: 594-599.
52. Amaral MD, (2011) Targeting CFTR: How to Treat Cystic Fibrosis by CFTR-Repairing Therapies. Curr Drug Targets 12: 683-693.
53. Gonska T, Ip W, Turner D, Han WS, Rose J, et al. (2009) Sweat gland bioelectrics differ in cystic fibrosis: a new concept for potential diagnosis and assessment of CFTR function in cystic fibrosis. Thorax 64: 932-938.