Enhanced Ca2+ entry due to Orai1 plasma membrane insertion increases IL-8 secretion by cystic fibrosis airways

FASEB Journal

Volumn 25, Issue 12, 2011, Pages 4274-4291

  Balghi, Haouaria ^a   Robert, Renaud ^a   Rappaz, Benjamin ^a   Zhang, Xuexin ^c   Wohlhuter Haddad, Adeline ^a   Evagelidis, Alexandra ^a   Luo, Yishan ^a   Goepp, Julie ^a   Ferraro, Pasquale ^d   Roméo, Philippe ^e   Trebak, Mohamed ^c   Wiseman, Paul W ^a   Thomas, David Y ^a   Hanrahan, John W ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c ALBANY MEDICAL COLLEGE   (United States)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^e MONTREAL HEART INSTITUTE   (Canada)

Author keywords

Calcium channels; Calcium influx; CFTR; Cystic fibrosis transmembrane conductance regulator; Cytokine

Indexed keywords

CALCIUM; INTERLEUKIN 8; STROMAL INTERACTION MOLECULE 1; TRANSMEMBRANE CONDUCTANCE REGULATOR; CALCIUM CHANNEL; CFTR PROTEIN, HUMAN; IL8 PROTEIN, HUMAN; MEMBRANE PROTEIN; MUTANT PROTEIN; ORAI1 PROTEIN, HUMAN; PRIMER DNA; SMALL INTERFERING RNA; STIM1 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; BIOTINYLATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; CELL SURFACE; CYSTIC FIBROSIS; DOWN REGULATION; ELECTROPHYSIOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOCYTOSIS; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; LUNG FIBROSIS; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESPIRATORY EPITHELIUM; SPECTROSCOPY; STORE OPERATED CALCIUM ENTRY; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; CELL MEMBRANE POTENTIAL; DRUG ANTAGONISM; GENE SILENCING; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; SIGNAL TRANSDUCTION;

BASE SEQUENCE; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MEMBRANE; CELLS, CULTURED; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA PRIMERS; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTERLEUKIN-8; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MUTANT PROTEINS; NEOPLASM PROTEINS; RESPIRATORY MUCOSA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 82655171620     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-187682     Document Type: Article

References (67)

1. Gadsby, D. C., Vergani, P., and Csanady, L. (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440, 477-483
2. Rommens, J. M., Zengerling, S., Burns, J., Melmer, G., Kerem, B. S., Plavsic, N., Zsiga, M., Kennedy, D., Markiewicz, D., Rozmahel, R., Riordan, J. R., Buchwald, M., and Tsui, L.-C. (1988) Identification and regional localization of DNA markers on chromosome 7 for the cloning of the cystic fibrosis gene. Am. J. Hum. Genet. 43, 645-663 (Pubitemid 18269245)
3. Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J. L., Drumm, M. L., Iannuzzi, M. C., Collins, F. S., and Tsui, L. C. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066-1073 (Pubitemid 19231814)
4. Hanrahan, J. W., and Wioland, M. A. (2004) Revisiting cystic fibrosis transmembrane conductance regulator structure and function. Proc. Am. Thorac. Soc. 1, 17-21
5. Naren, A. P., Cobb, B., Li, C., Roy, K., Nelson, D., Heda, G. D., Liao, J., Kirk, K. L., Sorscher, E. J., Hanrahan, J., and Clancy, J. P. (2003) A macromolecular complex of beta 2 adrenergic receptor, CFTR, and ezrin/radixin/moesin-binding phosphoprotein 50 is regulated by PKA. Proc. Natl. Acad. Sci. U. S. A. 100, 342-346 (Pubitemid 36078076)
6. Guggino, W. B., and Stanton, B. A. (2006) New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat. Rev. Mol. Cell Biol. 7, 426-436 (Pubitemid 44050096)
7. Weber, A. J., Soong, G., Bryan, R., Saba, S., and Prince, A. (2001) Activation of NF-kappaB in airway epithelial cells is dependent on CFTR trafficking and Cl- channel function. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L71-L78
8. Ribeiro, C. M., Paradiso, A. M., Carew, M. A., Shears, S. B., and Boucher, R. C. (2005) Cystic fibrosis airway epithelial Ca2+ i signaling: the mechanism for the larger agonist-mediated Ca2+ i signals in human cystic fibrosis airway epithelia. J. Biol. Chem. 280, 10202-10209 (Pubitemid 40395875)
9. Antigny, F., Norez, C., Becq, F., and Vandebrouck, C. (2008) Calcium homeostasis is abnormal in cystic fibrosis airway epithelial cells but is normalized after rescue of F508del-CFTR. Cell Calcium 43, 175-183
10. Antigny, F., Norez, C., Cantereau, A., Becq, F., and Vandebrouck, C. (2008) Abnormal spatial diffusion of Ca2+ in F508del-CFTR airway epithelial cells. Respir. Res. 9, 70
11. Ratner, A. J., Bryan, R., Weber, A., Nguyen, S., Barnes, D., Pitt, A., Gelber, S., Cheung, A., and Prince, A. (2001) Cystic fibrosis pathogens activate Ca2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells. J. Biol. Chem. 276, 19267-19275
12. Fu, Z., Bettega, K., Carroll, S., Buchholz, K. R., and Machen, T. E. (2007) Role of Ca2+ in responses of airway epithelia to Pseudomonas aeruginosa, flagellin, ATP, and thapsigargin. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L353-L364 (Pubitemid 46103460)
13. Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D., Velicelebi, G., and Stauderman, K. A. (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435-445 (Pubitemid 40686694)
14. Liou, J., Kim, M. L., Heo, W. D., Jones, J. T., Myers, J. W., Ferrell, J. E., Jr., and Meyer, T. (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15, 1235-1241 (Pubitemid 40950523)
15. Luik, R. M., Wu, M. M., Buchanan, J., and Lewis, R. S. (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol. 174, 815-825 (Pubitemid 44373731)
16. Hoth, M., and Penner, R. (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355, 353-356
17. Vig, M., Peinelt, C., Beck, A., Koomoa, D. L., Rabah, D., Koblan-Huberson, M., Kraft, S., Turner, H., Fleig, A., Penner, R., and Kinet, J. P. (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312, 1220-1223 (Pubitemid 43801149)
18. Zhang, S. L., Yeromin, A. V., Zhang, X. H., Yu, Y., Safrina, O., Penna, A., Roos, J., Stauderman, K. A., and Cahalan, M. D. (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc. Natl. Acad. Sci. U. S. A. 103, 9357-9362 (Pubitemid 43902581)
19. Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S. H., Tanasa, B., Hogan, P. G., Lewis, R. S., Daly, M., and Rao, A. (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185
20. Yuan, J. P., Zeng, W., Huang, G. N., Worley, P. F., and Muallem, S. (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat. Cell Biol. 9, 636-645 (Pubitemid 47214725)
21. Vazquez, G., Wedel, B. J., Aziz, O., Trebak, M., and Putney, J. W., Jr. (2004) The mammalian TRPC cation channels. Biochim. Biophys. Acta 1742, 21-36 (Pubitemid 39610491)
22. Pedersen, S. F., Owsianik, G., and Nilius, B. (2005) TRP channels: an overview. Cell Calcium 38, 233-252 (Pubitemid 41283262)
23. Antigny, F., Norez, C., Dannhoffer, L., Bertrand, J., Raveau, D., Corbi, P., Jayle, C., Becq, F., and Vandebrouck, C. (2011) Transient receptor potential canonical channel 6 links Ca2+ mishandling to cystic fibrosis transmembrane conductance regulator channel dysfunction in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 44, 83-90
24. Bruscia, E., Sangiuolo, F., Sinibaldi, P., Goncz, K. K., Novelli, G., and Gruenert, D. C. (2002) Isolation of CF cell lines corrected at DeltaF508-CFTR locus by SFHR-mediated targeting. Gene Ther. 9, 683-685 (Pubitemid 34591465)
25. Illek, B., Maurisse, R., Wahler, L., Kunzelmann, K., Fischer, H., and Gruenert, D. C. (2008) Cl transport in complemented CF bronchial epithelial cells correlates with CFTR mRNA expression levels. Cell. Physiol. Biochem. 22, 57-68
26. Bebok, Z., Collawn, J. F., Wakefield, J., Parker, W., Li, Y., Varga, K., Sorscher, E. J., and Clancy, J. P. (2005) Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o- airway epithelial monolayers. J. Physiol. 569, 601-615 (Pubitemid 41830125)
27. Fulcher, M. L., Gabriel, S., Burns, K. A., Yankaskas, J. R., and Randell, S. H. (2005) Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107, 183-206
28. Randell, S. H., Walstad, L., Schwab, U. E., Grubb, B. R., and Yankaskas, J. R. (2001) Isolation and culture of airway epithelial cells from chronically infected human lungs. In Vitro Cell. Dev. Biol. Anim. 37, 480-489 (Pubitemid 32973237)
29. Larsen, E. H., Novak, I., and Pedersen, P. S. (1990) Cation transport by sweat ducts in primary culture. Ionic mechanism of cholinergically evoked current oscillations. J. Physiol. 424, 109-131 (Pubitemid 20175149)
30. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (Pubitemid 15114340)
31. Epps, D. E., Wolfe, M. L., and Groppi, V. (1994) Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3-dibutylbarbituric acid)trimethine oxonol (Dibac4(3)) in model systems and cells. Chem. Phys. Lipids. 69, 137-150
32. Motiani, R. K., Abdullaev, I. F., and Trebak, M. (2010) A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptorpositive versus estrogen receptor-negative breast cancer cells. J. Biol. Chem. 285, 19173-19183
33. Potier, M., Gonzalez, J. C., Motiani, R. K., Abdullaev, I. F., Bisaillon, J. M., Singer, H. A., and Trebak, M. (2009) Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J. 23, 2425-2437
34. Comeau, J. W., Costantino, S., and Wiseman, P. W. (2006) A guide to accurate fluorescence microscopy colocalization measurements. Biophys. J. 91, 4611-4622 (Pubitemid 44904246)
35. Wiseman, P. W., Squier, J. A., Ellisman, M. H., and Wilson, K. R. (2000) Two-photon image correlation spectroscopy and image cross-correlation spectroscopy. J. Microsc. 200, 14-25
36. Mehta, D., Ahmmed, G. U., Paria, B. C., Holinstat, M., Voyno-Yasenetskaya, T., Tiruppathi, C., Minshall, R. D., and Malik, A. B. (2003) RhoA interaction with inositol 1,4,5-trisphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. Role in signaling increased endothelial permeability. J. Biol. Chem. 278, 33492-33500 (Pubitemid 37055804)
37. Prakriya, M., and Lewis, R. S. (2001) Potentiation and inhibition of Ca(2+) release-activated Ca(2+) channels by 2-aminoethyldiphenyl borate (2-APB) occurs independently of IP(3) receptors. J. Physiol. 536, 3-19 (Pubitemid 32952214)
38. Walsh, C. M., Chvanov, M., Haynes, L. P., Petersen, O. H., Tepikin, A. V., and Burgoyne, R. D. (2010) Role of phosphoinositides in STIM1 dynamics and store-operated calcium entry. Biochem. J. 425, 159-168
39. Machen, T. E. (2006) Innate immune response in CF airway epithelia: hyperinflammatory? Am. J. Physiol. Cell Physiol. 291, C218-C230
40. Bakowski, D., and Parekh, A. B. (2002) Monovalent cation permeability and Ca(2+) block of the store-operated Ca(2+) current I(CRAC)in rat basophilic leukemia cells. Pflügers Arch. 443, 892-902 (Pubitemid 34234097)
41. Woodard, G. E., Salido, G. M., and Rosado, J. A. (2008) Enhanced exocytotic-like insertion of Orai1 into the plasma membrane upon intracellular Ca2+ store depletion. Am. J. Physiol. Cell Physiol. 294, C1323-C1331
42. Yu, F., Sun, L., and Machaca, K. (2010) Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis. J. Cell Biol. 191, 523-535
43. DiMango, E., Ratner, A. J., Bryan, R., Tabibi, S., and Prince, A. (1998) Activation of NF-kappaB by adherent Pseudomonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells. J. Clin. Invest. 101, 2598-2605
44. Divangahi, M., Balghi, H., Danialou, G., Comtois, A. S., Demoule, A., Ernest, S., Haston, C., Robert, R., Hanrahan, J. W., Radzioch, D., and Petrof, B. J. (2009) Lack of CFTR in skeletal muscle predisposes to muscle wasting and diaphragm muscle pump failure in cystic fibrosis mice. PLoS Genet. 5, e1000586
45. Michoud, M. C., Robert, R., Hassan, M., Moynihan, B., Haston, C., Govindaraju, V., Ferraro, P., Hanrahan, J. W., and Martin, J. G. (2009) Role of the cystic fibrosis transmembrane conductance channel in human airway smooth muscle. Am. J. Respir. Cell Mol. Biol. 40, 217-222
46. Galan, C., Zbidi, H., Bartegi, A., Salido, G. M., and Rosado, J. A. (2009) STIM1, Orai1 and hTRPC1 are important for thrombinand ADP-induced aggregation in human platelets. Arch. Biochem. Biophys. 490, 137-144
47. Huang, G. N., Zeng, W., Kim, J. Y., Yuan, J. P., Han, L., Muallem, S., and Worley, P. F. (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat. Cell Biol. 8, 1003-1010 (Pubitemid 44314732)
48. Singh, B. B., Lockwich, T. P., Bandyopadhyay, B. C., Liu, X., Bollimuntha, S., Brazer, S. C., Combs, C., Das, S., Leenders, A. G., Sheng, Z. H., Knepper, M. A., Ambudkar, S. V., and Ambudkar, I. S. (2004) VAMP2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Mol. Cell 15, 635-646 (Pubitemid 39141789)
49. Otsuguro, K., Tang, J., Tang, Y., Xiao, R., Freichel, M., Tsvilovskyy, V., Ito, S., Flockerzi, V., Zhu, M. X., and Zholos, A. V. (2008) Isoform-specific inhibition of TRPC4 channel by phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 283, 10026-10036
50. Martin, A. C., Willoughby, D., Ciruela, A., Ayling, L. J., Pagano, M., Wachten, S., Tengholm, A., and Cooper, D. M. (2009) Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol. Pharmacol. 75, 830-842
51. Prior, I. A., Harding, A., Yan, J., Sluimer, J., Parton, R. G., and Hancock, J. F. (2001) GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3, 368-375 (Pubitemid 32288444)
52. Dudez, T., Borot, F., Huang, S., Kwak, B. R., Bacchetta, M., Ollero, M., Stanton, B. A., and Chanson, M. (2008) CFTR in a lipid raft-TNFR1 complex modulates gap junctional intercellular communication and IL-8 secretion. Biochim. Biophys. Acta 1783, 779-788
53. Grassme, H., Jendrossek, V., Riehle, A., von Kurthy, G., Berger, J., Schwarz, H., Weller, M., Kolesnick, R., and Gulbins, E. (2003) Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9, 322-330 (Pubitemid 36362788)
54. Hong, J. H., Li, Q., Kim, M. S., Shin, D. M., Feske, S., Birnbaumer, L., Cheng, K. T., Ambudkar, I. S., and Muallem, S. (2011) Polarized but differential localization and recruitment of STIM1, Orai1 and TRPC channels in secretory cells. Traffic 12, 232-245
55. Kowalski, M. P., and Pier, G. B. (2004) Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-induced cellular activation. J. Immunol. 172, 418-425 (Pubitemid 38020496)
56. Bertrand, C. A., and Frizzell, R. A. (2003) The role of regulated CFTR trafficking in epithelial secretion. Am. J. Physiol. Cell Physiol. 285, C1-C18 (Pubitemid 36736331)
57. Peters, K. W., Qi, J., Johnson, J. P., Watkins, S. C., and Frizzell, R. A. (2001) Role of snare proteins in CFTR and ENaC trafficking. Pflügers Arch. 443(Suppl. 1), S65-S69 (Pubitemid 33086955)
58. Muhlebach, M. S., Stewart, P. W., Leigh, M. W., and Noah, T. L. (1999) Quantitation of inflammatory responses to bacteria in young cystic fibrosis and control patients. Am. J. Respir. Crit. Care Med. 160, 186-191 (Pubitemid 29326086)
59. Gwack, Y., Srikanth, S., Oh-Hora, M., Hogan, P. G., Lamperti, E. D., Yamashita, M., Gelinas, C., Neems, D. S., Sasaki, Y., Feske, S., Prakriya, M., Rajewsky, K., and Rao, A. (2008) Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol. Cell. Biol. 28, 5209-5222
60. McCarl, C. A., Khalil, S., Ma, J., Oh-hora, M., Yamashita, M., Roether, J., Kawasaki, T., Jairaman, A., Sasaki, Y., Prakriya, M., and Feske, S. (2010) Store-operated Ca2+ entry through ORAI1 is critical for T cell-mediated autoimmunity and allograft rejection. J. Immunol. 185, 5845-5858
61. Lloyd-Still, J. D. (1994) Crohn's disease and cystic fibrosis. Dig. Dis. Sci. 39, 880-885
62. Roussel, L., and Rousseau, S. IL-17 primes airway epithelial cells lacking functional cystic fibrosis transmembrane conductance regulator (CFTR) to increase NOD1 responses. Biochem. Biophys. Res. Commun. 391, 505-509
63. Ribeiro, C. M. (2006) The role of intracellular calcium signals in inflammatory responses of polarised cystic fibrosis human airway epithelia. Drugs R. D. 7, 17-31
64. Knowles, M. R., Stutts, M. J., Yankaskas, J. R., Gatzy, J. T., and Boucher, R. C., Jr. (1986) Abnormal respiratory epithelial ion transport in cystic fibrosis. Clin. Chest Med. 7, 285-297 (Pubitemid 16090984)
65. Di Sabatino, A., Rovedatti, L., Kaur, R., Spencer, J. P., Brown, J. T., Morisset, V. D., Biancheri, P., Leakey, N. A., Wilde, J. I., Scott, L., Corazza, G. R., Lee, K., Sengupta, N., Knowles, C. H., Gunthorpe, M. J., McLean, P. G., MacDonald, T. T., and Kruidenier, L. (2009) Targeting gut T cell Ca2+ release-activated Ca2+ channels inhibits T cell cytokine production and T-box transcription factor T-bet in inflammatory bowel disease. J. Immunol. 183, 3454-3462
66. Voynow, J. A., Fischer, B. M., Roberts, B. C., and Proia, A. D. (2005) Basal-like cells constitute the proliferating cell population in cystic fibrosis airways. Am. J. Respir. Crit. Care Med. 172, 1013-1018 (Pubitemid 41476539)
67. Gallagher, A. M., and Gottlieb, R. A. (2001) Proliferation, not apoptosis, alters epithelial cell migration in small intestine of CFTR null mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G681-G687