TGF-beta downregulation of distinct chloride channels in cystic fibrosis-affected epithelia

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Sun, Hongtao ^a   Harris, William T ^b   Kortyka, Stephanie ^d   Kotha, Kavitha ^e   Ostmann, Alicia J ^a   Rezayat, Amir ^a   Sridharan, Anusha ^a   Sanders, Yan ^c   Naren, Anjaparavanda P ^a,f   Clancy, John P ^a,f  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Louisville School of Medicine   (United States)

^e NATIONWIDE CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; LUMACAFTOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN TMEM16A; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; ANO1 PROTEIN, HUMAN; CFTR PROTEIN, HUMAN; CHLORIDE; CHLORIDE CHANNEL; CLCA1 PROTEIN, HUMAN; CYCLIC AMP; MESSENGER RNA; TUMOR PROTEIN;

AIRWAY SURFACE LIQUID VOLUME; ARTICLE; CHLORIDE CURRENT; CONTROLLED STUDY; CYSTIC FIBROSIS; DOWN REGULATION; EPITHELIUM CELL; GENE DELETION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT PARAMETERS; SIGNAL TRANSDUCTION; T84 CELL LINE; WILD TYPE; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA;

CELL LINE; CHLORIDE CHANNELS; CHLORIDES; CYCLIC AMP; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; NEOPLASM PROTEINS; RESPIRATORY MUCOSA; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 84907494781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106842     Document Type: Article

References (62)

1. Rowe SM, Miller S, Sorscher EJ (2005) Cystic fibrosis. The New England journal of medicine 352: 1992-2001.
2. Com G, Clancy JP (2009) Adenosine receptors, cystic fibrosis, and airway hydration. Handbook of experimental pharmacology: 363-381.
3. Anderson MP, Welsh MJ (1992) Regulation by ATP and ADP of CFTR chloride channels that contain mutant nucleotide-binding domains. Science (New York, NY 257: 1701-1704.
4. Smith JJ, Welsh MJ (1992) cAMP stimulates bicarbonate secretion across normal, but not cystic fibrosis airway epithelia. The Journal of clinical investigation 89: 1148-1153.
5. Kunzelmann K, Mehta A (2013) CFTR: a hub for kinases and crosstalk of cAMP and Ca2+. The FEBS journal 280: 4417-4429.
6. Paradiso AM, Ribeiro CM, Boucher RC (2001) Polarized signaling via purinoceptors in normal and cystic fibrosis airway epithelia. The Journal of general physiology 117: 53-67.
7. Namkung W, Phuan PW, Verkman AS (2011) TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. The Journal of biological chemistry 286: 2365-2374.
8. Ferrera L, Caputo A, Galietta LJ (2010) TMEM16A protein: a new identity for Ca(2+)-dependent Cl(-) channels. Physiology (Bethesda) 25: 357-363.
9. Rock JR, O'Neal WK, Gabriel SE, Randell SH, Harfe BD, et al. (2009) Transmembrane protein 16A (TMEM16A) is a Ca2+-regulated Cl- secretory channel in mouse airways. The Journal of biological chemistry 284: 14875-14880.
10. Tarran R, Button B, Boucher RC (2006) Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress. Annual review of physiology 68: 543-561.
11. Grubb BR, Vick RN, Boucher RC (1994) Hyperabsorption of Na+ and raised Ca(2+)-mediated Cl- secretion in nasal epithelia of CF mice. The American journal of physiology 266: C1478-1483.
12. Coakley RD, Sun H, Clunes LA, Rasmussen JE, Stackhouse JR, et al. (2008) 17beta-Estradiol inhibits Ca2+-dependent homeostasis of airway surface liquid volume in human cystic fibrosis airway epithelia. The Journal of clinical investigation 118: 4025-4035.
13. Zhang L, Bukreyev A, Thompson CI, Watson B, Peeples ME, et al. (2005) Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. Journal of virology 79: 1113-1124.
14. Tarran R, Button B, Picher M, Paradiso AM, Ribeiro CM, et al. (2005) Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. The Journal of biological chemistry 280: 35751-35759.
15. Drumm ML, Konstan MW, Schluchter MD, Handler A, Pace R, et al. (2005) Genetic modifiers of lung disease in cystic fibrosis. The New England journal of medicine 353: 1443-1453.
16. Collaco JM, Cutting GR (2008) Update on gene modifiers in cystic fibrosis. Current opinion in pulmonary medicine 14: 559-566.
17. Dorfman R, Sandford A, Taylor C, Huang B, Frangolias D, et al. (2008) Complex two-gene modulation of lung disease severity in children with cystic fibrosis. The Journal of clinical investigation 118: 1040-1049.
18. Bremer LA, Blackman SM, Vanscoy LL, McDougal KE, Bowers A, et al. (2008) Interaction between a novel TGFB1 haplotype and CFTR genotype is associated with improved lung function in cystic fibrosis. Human molecular genetics 17: 2228-2237.
19. Willis BC, Borok Z (2007) TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. American journal of physiology 293: L525-534.
20. Massague J (2012) TGF-beta signaling in development and disease. FEBS letters 586: 1833.
21. Heldin CH, Vanlandewijck M and Moustakas A (2012) Regulation of EMT by TGFbeta in cancer. FEBS letters 586: 1959-1970.
22. Coward WR, Saini G, Jenkins G (2010) The pathogenesis of idiopathic pulmonary fibrosis. Therapeutic advances in respiratory disease 4: 367-388.
23. Wynn TA (2011) Integrating mechanisms of pulmonary fibrosis. The Journal of experimental medicine 208: 1339-1350.
24. Selman M, Pardo A (2002) Idiopathic pulmonary fibrosis: an epithelial/ fibroblastic cross-talk disorder. Respiratory research 3: 3.
25. Howe KL, Wang A, Hunter MM, Stanton BA, McKay DM (2004) TGFbeta down-regulation of the CFTR: a means to limit epithelial chloride secretion. Experimental cell research 298: 473-484.
26. Snodgrass SM, Cihil KM, Cornuet PK, Myerburg MM, Swiatecka-Urban A (2013) Tgf-beta1 inhibits Cftr biogenesis and prevents functional rescue of DeltaF508-Cftr in primary differentiated human bronchial epithelial cells. PloS one 8: e63167.
27. Van Goor F, Hadida S, Grootenhuis PD, Burton B, Stack JH, et al. (2011) Correction of the F508del-CFTR protein processing defect in vitro by the investigational drug VX-809. Proc Natl Acad Sci U S A 108: 18843-18848.
28. Clancy JP, Rowe SM, Accurso FJ, Aitken ML, Amin RS, et al. (2012) Results of a phase IIa study of VX-809, an investigational CFTR corrector compound, in subjects with cystic fibrosis homozygous for the F508del-CFTR mutation. Thorax 67: 12-18.
29. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH (2005) Welldifferentiated human airway epithelial cell cultures. Methods in molecular medicine 107: 183-206.
30. Rowe SM, Pyle LC, Jurkevante A, Varga K, Collawn J, et al. (2010) DeltaF508 CFTR processing correction and activity in polarized airway and non-airway cell monolayers. Pulmonary pharmacology & therapeutics 23: 268-278.
31. Hirtz S, Gonska T, Seydewitz HH, Thomas J, Greiner P, et al. (2004) CFTR Clchannel function in native human colon correlates with the genotype and phenotype in cystic fibrosis. Gastroenterology 127: 1085-1095.
32. Clancy JP, Szczesniak RD, Ashlock MA, Ernst SE, Fan L, et al. (2013) Multicenter intestinal current measurements in rectal biopsies from CF and non- CF subjects to monitor CFTR function. PloS one 8: e73905.
33. 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.
34. Thiagarajah JR, Song Y, Haggie PM, Verkman AS (2004) A small molecule CFTR inhibitor produces cystic fibrosis-like submucosal gland fluid secretions in normal airways. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 18: 875-877.
35. Ito Y, Sato S, Ohashi T, Nakayama S, Shimokata K, et al. (2004) Reduction of airway anion secretion via CFTR in sphingomyelin pathway. Biochemical and biophysical research communications 324: 901-908.
36. Harvey PR, Tarran R, Garoff S, Myerburg MM (2011) Measurement of the airway surface liquid volume with simple light refraction microscopy. American journal of respiratory cell and molecular biology 45: 592-599.
37. Pruliere-Escabasse V, Fanen P, Dazy AC, Lechapt-Zalcman E, Rideau D, et al. (2005) TGF-beta 1 downregulates CFTR expression and function in nasal polyps of non-CF patients. American journal of physiology 288: L77-83.
38. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, et al. (1998) Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
39. Pierucci-Alves F, Yi S, Schultz BD (2012) Transforming growth factor beta 1 induces tight junction disruptions and loss of transepithelial resistance across porcine vas deferens epithelial cells. Biology of reproduction 86: 36.
40. Harris WT, Muhlebach MS, Oster RA, Knowles MR, Noah TL (2009) Transforming growth factor-beta(1) in bronchoalveolar lavage fluid from children with cystic fibrosis. Pediatric pulmonology 44: 1057-1064.
41. Harris WT, Muhlebach MS, Oster RA, Knowles MR, Clancy JP, et al. (2011) Plasma TGF-beta(1) in pediatric cystic fibrosis: potential biomarker of lung disease and response to therapy. Pediatric pulmonology 46: 688-695.
42. Restrick LJ, Sampson AP, Piper PJ, Costello JF (1995) Inulin as a marker of dilution of bronchoalveolar lavage in asthmatic and normal subjects. American journal of respiratory and critical care medicine 151: 1211-1217.
43. Rennard SI, Basset G, Lecossier D, O'Donnell KM, Pinkston P, et al. (1986) Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J Appl Physiol (1985) 60: 532-538.
44. Arkwright PD, Laurie S, Super M, Pravica V, Schwarz MJ, et al. (2000) TGFbeta( 1) genotype and accelerated decline in lung function of patients with cystic fibrosis. Thorax 55: 459-462.
45. Corvol H, Boelle PY, Brouard J, Knauer N, Chadelat K, et al. (2008) Genetic variations in inflammatory mediators influence lung disease progression in cystic fibrosis. Pediatric pulmonology 43: 1224-1232.
46. Fernandez IE, Eickelberg O (2012) The impact of TGF-beta on lung fibrosis: from targeting to biomarkers. Proceedings of the American Thoracic Society 9: 111-116.
47. Meulmeester E, Ten Dijke P (2011) The dynamic roles of TGF-beta in cancer. The Journal of pathology 223: 205-218.
48. McLean S, Bhattacharya M, Di Guglielmo GM (2013) betaarrestin2 interacts with TbetaRII to regulate Smad-dependent and Smad-independent signal transduction. Cellular signalling 25: 319-331.
49. Yoshida M, Okubo N, Chosa N, Hasegawa T, Ibi M, et al. (2012) TGF-betaoperated growth inhibition and translineage commitment into smooth muscle cells of periodontal ligament-derived endothelial progenitor cells through Smadand p38 MAPK-dependent signals. International journal of biological sciences 8: 1062-1074.
50. Gomes LR, Terra LF, Wailemann RA, Labriola L, Sogayar MC (2012) TGFbeta1 modulates the homeostasis between MMPs and MMP inhibitors through p38 MAPK and ERK1/2 in highly invasive breast cancer cells. BMC cancer 12: 26.
51. Biernacka A, Dobaczewski M, Frangogiannis NG (2011) TGF-beta signaling in fibrosis. Growth Factors 29: 196-202.
52. Janknecht R, Wells NJ, Hunter T (1998) TGF-beta-stimulated cooperation of smad proteins with the coactivators CBP/p300. Genes & development 12: 2114-2119.
53. Peters DM, Vadasz I, Wujak L, Wygrecka M, Olschewski A, et al. (2014) TGFbeta directs trafficking of the epithelial sodium channel ENaC which has implications for ion and fluid transport in acute lung injury. Proc Natl Acad Sci U S A 111: E374-383.
54. Matsumura Y, David LL, Skach WR (2011) Role of Hsc70 binding cycle in CFTR folding and endoplasmic reticulum-associated degradation. Molecular biology of the cell 22: 2797-2809.
55. Schmidt BZ, Watts RJ, Aridor M, Frizzell RA (2009) Cysteine string protein promotes proteasomal degradation of the cystic fibrosis transmembrane conductance regulator (CFTR) by increasing its interaction with the C terminus of Hsp70-interacting protein and promoting CFTR ubiquitylation. The Journal of biological chemistry 284: 4168-4178.
56. Ren A, Zhang W, Sunitha Y, Arora K, Sinha C, et al. (2013) MAST205 Competes with CAL for Binding to CFTR to Regulate CFTR-mediated Fluid Transport. The Journal of biological chemistry.
57. Cheng J, Wang H, Guggino WB (2005) Regulation of cystic fibrosis transmembrane regulator trafficking and protein expression by a Rho family small GTPase TC10. The Journal of biological chemistry 280: 3731-3739.
58. Gentzsch M, Chang XB, Cui L, Wu Y, Ozols VV, et al. (2004) Endocytic trafficking routes of wild type and DeltaF508 cystic fibrosis transmembrane conductance regulator. Molecular biology of the cell 15: 2684-2696.
59. Silvis MR, Bertrand CA, Ameen N, Golin-Bisello F, Butterworth MB, et al. (2009) Rab11b regulates the apical recycling of the cystic fibrosis transmembrane conductance regulator in polarized intestinal epithelial cells. Molecular biology of the cell 20: 2337-2350.
60. Webster P, Vanacore L, Nairn AC, Marino CR (1994) Subcellular localization of CFTR to endosomes in a ductal epithelium. The American journal of physiology 267: C340-348.
61. Riordan JR (2008) CFTR function and prospects for therapy. Annual review of biochemistry 77: 701-726.
62. Cobb BR, Ruiz F, King CM, Fortenberry J, Greer H, et al. (2002) A(2) adenosine receptors regulate CFTR through PKA and PLA(2). American journal of physiology 282: L12-25.