Activation of the unfolded protein response by ΔF508 CFTR

American Journal of Respiratory Cell and Molecular Biology

Volumn 39, Issue 4, 2008, Pages 448-457

  Bartoszewski, Rafal ^a   Rab, Andras ^a,b   Jurkuvenaite, Asta ^a,b   Mazur, Marina ^b   Wakefield, John ^c   Collawn, James F ^a,b   Bebok, Zsuzsa ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c Tranzyme Inc   (United States)

Author keywords

F508 CFTR; Calu 3; Endoplasmic reticulum stress; Quantitative PCR; Unfolded protein response

Indexed keywords

MESSENGER RNA; PHENYLALANINE; PROTEASOME INHIBITOR; RNA; TRANSMEMBRANE CONDUCTANCE REGULATOR; TUNICAMYCIN;

AMINO ACID SEQUENCE; ARTICLE; BIOGENESIS; CELL CLONING; CYSTIC FIBROSIS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; LUNG ALVEOLUS CELL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; UNFOLDED PROTEIN RESONSE; WILD TYPE;

CELL LINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; HUMANS; MUTATION; PROTEIN FOLDING; RESPIRATORY MUCOSA; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 53349091619     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2008-0065OC     Document Type: Article

References (42)

1. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005;74:739-789.
2. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004;14:20-28.
3. Schroder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res 2005;569:29-63.
4. Welch WJ. Role of quality control pathways in human diseases involving protein misfolding. Semin Cell Dev Biol 2004;15:31-38.
5. Nanua S, Sajjan U, Keshavjee S, Hershenson MB. Absence of typical unfolded protein response in primary cultured cystic fibrosis airway epithelial cells. Biochem Biophys Res Commun 2006;343:135-143.
6. Hybiske K, Fu Z, Schwarzer C, Tseng J, Do J, Huang N, Machen TE. Effects of cystic fibrosis transmembrane conductance regulator and DeltaF508CFTR on inflammatory response, ER stress, and Ca2+ of airway epithelia. Am J Physiol Lung Cell Mol Physiol 2007;293:L1250-L1260.
7. Kerbiriou M, Le Drevo MA, Ferec C, Trouve P. Coupling cystic fibrosis to endoplasmic reticulum stress: differential role of Grp78 and ATF6. Biochim Biophys Acta 2007;1772:1236-1249.
8. Rab A, Bartoszewski R, Jurkuvenaite A, Wakefield J, Collawn JF, Bebok Z. Endoplasmic reticulum stress and the unfolded protein response regulate genomic cystic fibrosis transmembrane conductance regulator expression. Am J Physiol Cell Physiol 2007;292:C756-C766.
9. Vij N, Fang S, Zeitlin PL. Selective inhibition of endoplasmic reticulum-associated degradation rescues DeltaF508-cystic fibrosis transmembrane regulator and suppresses interleukin-8 levels: therapeutic implications. J Biol Chem 2006;281:17369-17378.
10. Egan ME, Glockner-Pagel J, Ambrose C, Cahill PA, Pappoe L, Balamuth N, Cho E, Canny S, Wagner CA, Geibel J, et al. Calcium-pump inhibitors induce functional surface expression of Delta F508-CFTR protein in cystic fibrosis epithelial cells. Nat Med 2002;8:485-492.
11. Egan ME, Pearson M, Weiner SA, Rajendran V, Rubin D, Glockner-Pagel J, Canny S, Du K, Lukacs GL, Caplan MJ. Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science 2004;304:600-602.
12. Norez C, Antigny F, Becq F, Vandebrouck C. Maintaining low Ca2+ level in the endoplasmic reticulum restores abnormal endogenous F508del-CFTR trafficking in airway epithelial cells. Traffic 2006;7:562-573.
13. Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, Boise LH. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 2006;107:4907-4916.
14. Chaabane C, Corvazier E, Bredoux R, Dally S, Raies A, Villemain A, Dupuy E, Enouf J, Bobe R. Sarco/endoplasmic reticulum Ca2+ ATPase type 3 isoforms (SERCA3b and SERCA3f): distinct roles in cell adhesion and ER stress. Biochem Biophys Res Commun 2006;345:1377-1385.
15. Hong M, Li M, Mao C, Lee AS. Endoplasmic reticulum stress triggers an acute proteasome-dependent degradation of ATF6. J Cell Biochem 2004;92:723-732.
16. Haws C, Finkbeiner WE, Widdicombe JH, Wine JJ. CFTR in Calu-3 human airway cells: channel properties and role in cAMP-activated Cl- conductance. Am J Physiol 1994;266:L502-L512.
17. Cliff WH, Schoumacher RA, Frizzell RA. cAMP-activated Cl channels in CFTR-transfected cystic fibrosis pancreatic epithelial cells. Am J Physiol 1992;262:C1154-C1160.
18. Varga K, Jurkuvenaite A, Wakefield J, Hong JS, Guimbellot JS, Venglarik CJ, Niraj A, Mazur M, Sorscher EJ, Collawn JF, et al. Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 2004;279:22578-22584.
19. Bebok Z, Collawn JF, Wakefield J, Parker W, Li Y, Varga K, Sorscher EJ, Clancy JP. Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o- airway epithelial monolayers. J Physiol 2005;569:601-615.
20. Hung JH, Su IJ, Lei HY, Wang HC, Lin WC, Chang WT, Huang W, Chang WC, Chang YS, Chen CC, et al. Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-kappaB and pp38 mitogen-activated protein kinase. J Biol Chem 2004;279:46384-46392.
21. Bebok Z, Varga K, Hicks JK, Venglarik CJ, Kovacs T, Chen L, Hardiman KM, Collawn JF, Sorscher EJ, Matalon S. Reactive oxygen nitrogen species decrease cystic fibrosis transmembrane conductance regulator expression and cAMP-mediated Cl- secretion in airway epithelia. J Biol Chem 2002;277:43041-43049.
22. Olsen JC, Sechelski J. Use of sodium butyrate to enhance production of retroviral vectors expressing CFTR cDNA. Hum Gene Ther 1995;6:1195-1202.
23. Roy J, Denovan-Wright EM, Linsdell P, Cowley EA. Exposure to sodium butyrate leads to functional downregulation of calcium-activated potassium channels in human airway epithelial cells. Pflugers Arch 2006;453:167-176.
24. Oliver J, Jungnickel B, Gorlich D, Rapoport T, High S. The Sec61 complex is essential for the insertion of proteins into the membrane of the endoplasmic reticulum. FEBS Lett 1995;362:126-130.
25. Heda GD, Marino CR. Surface expression of the cystic fibrosis transmembrane conductance regulator mutant DeltaF508 is markedly upregulated by combination treatment with sodium butyrate and low temperature. Biochem Biophys Res Commun 2000;271:659-664.
26. Moyer BD, Loffing-Cueni D, Loffing J, Reynolds D, Stanton BA. Butyrate increases apical membrane CFTR but reduces chloride secretion in MDCK cells. Am J Physiol 1999;277:F271-F276.
27. Loffing J, Moyer BD, Reynolds D, Stanton BA. PBA increases CFTR expression but at high doses inhibits Cl(-) secretion in Calu-3 airway epithelial cells. Am J Physiol 1999;277:L700-L708.
28. Farinha CM, Amaral MD. Most F508del-CFTR is targeted to degradation at an early folding checkpoint and independently of calnexin. Mol Cell Biol 2005;25:5242-5252.
29. Zhang F, Kartner N, Lukacs GL. Limited proteolysis as a probe for arrested conformational maturation of delta F508 CFTR. Nat Struct Biol 1998;5:180-183.
30. Cantin AM, Bilodeau G, Ouellet C, Liao J, Hanrahan JW. Oxidant stress suppresses CFTR expression. Am J Physiol Cell Physiol 2006;290:C262-C270.
31. Kreindler JL, Jackson AD, Kemp PA, Bridges RJ, Danahay H. Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am J Physiol Lung Cell Mol Physiol 2005;288:L894-L902.
32. Baudouin-Legros M, Hinzpeter A, Jaulmes A, Brouillard F, Costes B, Fanen P, Edelman A. Cell-specific posttranscriptional regulation of CFTR gene expression via influence of MAPK cascades on 3′UTR part of transcripts. Am J Physiol Cell Physiol 2005;289:C1240-C1250.
33. Braun ME, Jones L, O'Neel W, Ribeiro CM. An unfolded protein response is present in native CF tissues and is triggered by Infection/Inflammation in an in vitro model of CF airway epithelia. Pediatr Pulmonol Supplement 2006;236.
34. Akiba Y, Jung M, Ouk S, Kaunitz JD. A novel small molecule CFTR inhibitor attenuates HCO3- secretion and duodenal ulcer formation in rats. Am J Physiol Gastrointest Liver Physiol 2005;289:G753-G759.
35. Howard M, Fischer H, Roux J, Santos BC, Gullans SR, Yancey PH, Welch WJ. Mammalian osmolytes and S-nitrosoglutathione promote Delta F508 cystic fibrosis transmembrane conductance regulator (CFTR) protein maturation and function. J Biol Chem 2003;278:35159-35167.
36. Pedemonte N, Lukacs GL, Du K, Caci E, Zegarra-Moran O, Galietta LJ, Verkman AS. Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening. J Clin Invest 2005;115:2564-2571.
37. Rowe SM, Clancy JP. Advances in cystic fibrosis therapies. Curr Opin Pediatr 2006;18:604-613.
38. Verkman AS. Drug discovery and epithelial physiology. Curr Opin Nephrol Hypertens 2004;13:563-568.
39. Yang H, Shelat AA, Guy RK, Gopinath VS, Ma T, Du K, Lukacs GL, Taddei A, Folli C, Pedemonte N, et al. Nanomolar affinity small molecule correctors of defective Delta F508-CFTR chloride channel gating. J Biol Chem 2003;278:35079-35085.
40. Paul T, Li S, Khurana S, Leleiko NS, Walsh MJ. The epigenetic signature of CFTR expression is co-ordinated via chromatin acetylation through a complex intronic element. Biochem J 2007;408:317-326.
41. Amaral MD, Clarke LA, Ramalho AS, Beck S, Broackes-Carter F, Rowntree R, Mouchel N, Williams SH, Harris A, Tzetis M, et al. Quantitative methods for the analysis of CFTR transcripts/splicing variants. J Cyst Fibros 2004;3:17-23.
42. Trezise AE, Farinha CM, Heda GD, Harris A, Amaral MD, Mouchel N. Non-PCR methods for the analysis of CFTR transcripts. J Cyst Fibros 2004;3:25-28.