Influenza matrix protein 2 alters CFTR expression and function through its ion channel activity

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 304, Issue 9, 2013, Pages

  Londino, James D ^a,b,c   Lazrak, Ahmed ^a,c   Jurkuvenaite, Asta ^a,c   Collawn, James F ^b,c   Noah, James W ^c,d   Matalon, Sadis ^a,b,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^d SOUTHERN RESEARCH INSTITUTE   (United States)

Author keywords

16HBE14o ; Patch clamp; Secretory pH; Ubiquitin; Xenopus oocytes

Indexed keywords

AMMONIUM CHLORIDE; CONCANAMYCIN A; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FORSKOLIN; ION CHANNEL; PROTEIN M2; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL PH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INFLUENZA VIRUS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SECRETORY PATHWAY; XENOPUS;

EID: 84878645367     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00314.2012     Document Type: Article

References (58)

1. Acharya R, Carnevale V, Fiorin G, Levine BG, Polishchuk AL, Balannik V, Samish I, Lamb RA, Pinto LH, DeGrado WF, Klein ML. Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus. Proc Natl Acad Sci USA 107: 15075-15080, 2010.
2. Andersson H, Kappeler F, Hauri HP. Protein targeting to endoplasmic reticulum by dilysine signals involves direct retention in addition to retrieval. J Biol Chem 274: 15080-15084, 1999.
3. Axelsson MA, Karlsson NG, Steel DM, Ouwendijk J, Nilsson T, Hansson GC. Neutralization of pH in the Golgi apparatus causes redistribution of glycosyltransferases and changes in the O-glycosylation of mucins. Glycobiology 11: 633-644, 2001.
4. Baker K, Marcus CB, Huffman K, Kruk H, Malfroy B, Doctrow SR. Synthetic combined superoxide dismutase/catalase mimetics are protective as a delayed treatment in a rat stroke model: a key role for reactive oxygen species in ischemic brain injury. J Pharmacol Exp Ther 284: 215-221, 1998.
5. Balannik V, Carnevale V, Fiorin G, Levine BG, Lamb RA, Klein ML, DeGrado WF, Pinto LH. Functional studies and modeling of pore-lining residue mutants of the influenza a virus M2 ion channel. Biochemistry 49: 696-708, 2010.
6. Bartoszewski RA, Jablonsky M, Bartoszewska S, Stevenson L, Dai Q, Kappes J, Collawn JF, Bebok Z. A synonymous single nucleotide polymorphism in DeltaF508 CFTR alters the secondary structure of the mRNA and the expression of the mutant protein. J Biol Chem 285: 28741-28748, 2010.
7. Bauer CM, Pinto LH, Cross TA, Lamb RA. The influenza virus M2 ion channel protein: probing the structure of the transmembrane domain in intact cells by using engineered disulfide cross-linking. Virology 254: 196-209, 1999.
8. + secretion in airway epithelia. J Biol Chem 277: 43041-43049, 2002.
9. Berdiev BK, Qadri YJ, Benos DJ. Assessment of the CFTR and ENaC association. Mol Biosyst 5: 123-127, 2009.
10. Cantin AM, Bilodeau G, Ouellet C, Liao J, Hanrahan JW. Oxidant stress suppresses CFTR expression. Am J Physiol Cell Physiol 290: C262-C270, 2006.
11. + channel. J Biol Chem 284: 35495-35506, 2009.
12. Chen L, Bosworth CA, Pico T, Collawn JF, Varga K, Gao Z, Clancy JP, Fortenberry JA, Lancaster JR Jr, Matalon S. DETANO and nitrated lipids increase chloride secretion across lung airway cells. Am J Respir Cell Mol Biol 39: 150-162, 2008.
13. Chen L, Patel RP, Teng X, Bosworth CA, Lancaster JR Jr, Matalon S. Mechanisms of cystic fibrosis transmembrane conductance regulator activation by s-nitrosoglutathione. J Biol Chem 281: 9190-9199, 2006.
14. Chen XJ, Seth S, Yue G, Kamat P, Compans RW, Guidot D, Brown LA, Eaton DC, Jain L. Influenza virus inhibits ENaC and lung fluid clearance. Am J Physiol Lung Cell Mol Physiol 287: L366-L373, 2004.
15. Cohen TS, Prince A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat Med 18: 509-519, 2012.
16. Collawn JF, Lazrak A, Bebok Z, Matalon S. The CFTR and ENaC debate: how important is ENaC in CF lung disease? Am J Physiol Lung Cell Mol Physiol 302: L1141-L1146, 2012.
17. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10: 38-47, 1994.
18. Drose S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200: 1-8, 1997.
19. Factor P, Mutlu GM, Chen L, Mohameed J, Akhmedov AT, Meng FJ, Jilling T, Lewis ER, Johnson MD, Xu A, Kass D, Martino JM, Bellmeyer A, Albazi JS, Emala C, Lee HT, Dobbs LG, Matalon S. Adenosine regulation of alveolar fluid clearance. Proc Natl Acad Sci USA 104: 4083-4088, 2007.
20. Henkel JR, Apodaca G, Altschuler Y, Hardy S, Weisz OA. Selective perturbation of apical membrane traffic by expression of influenza M2, an acid-activated ion channel, in polarized Madin-Darby canine kidney cells. Mol Biol Cell 9: 2477-2490, 1998.
21. Henkel JR, Popovich JL, Gibson GA, Watkins SC, Weisz OA. Selective perturbation of early endosome and/or trans-Golgi network pH but not lysosome pH by dose-dependent expression of influenza M2 protein. J Biol Chem 274: 9854-9860, 1999.
22. Hughey PG, Compans RW, Zebedee SL, Lamb RA. Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J Virol 66: 5542-5552, 1992.
23. Ji HL, Song W, Gao Z, Su XF, Nie HG, Jiang Y, Peng JB, He YX, Liao Y, Zhou YJ, Tousson A, Matalon S. SARS-CoV proteins decrease levels and activity of human ENaC via activation of distinct PKC isoforms. Am J Physiol Lung Cell Mol Physiol 296: L372-L383, 2009.
24. Ji HL, Su XF, Kedar S, Li J, Barbry P, Smith PR, Matalon S, Benos DJ. Delta-subunit confers novel biophysical features to alpha beta gammahuman epithelial sodium channel (ENaC) via a physical interaction. J Biol Chem 281: 8233-8241, 2006.
25. Jilling T, Haddad IY, Cheng SH, Matalon S. Nitric oxide inhibits heterologous CFTR expression in polarized epithelial cells. Am J Physiol Lung Cell Mol Physiol 277: L89-L96, 1999.
26. Kajikawa O, Goodman RB, Johnson MC, Konishi K, Martin TR. Sensitive and specific immunoassays to detect rabbit IL-8 and MCP-1: cytokines that mediate leukocyte recruitment to the lungs. J Immunol Methods 197: 19-29, 1996.
27. Kongsuphol P, Cassidy D, Romeiras F, Schreiber R, Mehta A, Kunzelmann K. Metformin treatment of diabetes mellitus increases the risk for pancreatitis in patients bearing the CFTR-mutation S573C. Cell Physiol Biochem 25: 389-396, 2010.
28. + channels in respiratory epithelia. Proc Natl Acad Sci USA 97: 10282-10287, 2000.
29. Lamb RA, Zebedee SL, Richardson CD. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40: 627-633, 1985.
30. Lazrak A, Iles KE, Liu G, Noah DL, Noah JW, Matalon S. Influenza virus M2 protein inhibits epithelial sodium channels by increasing reactive oxygen species. FASEB J 23: 3829-3842, 2009.
31. Lazrak A, Jurkuvenaite A, Chen L, Keeling KM, Collawn JF, Bedwell DM, Matalon S. Enhancement of alveolar epithelial sodium channel activity with decreased cystic fibrosis transmembrane conductance regulator expression in mouse lung. Am J Physiol Lung Cell Mol Physiol 301: L557-L567, 2011.
32. + transport in vitro and in vivo. Am J Respir Cell Mol Biol 41: 261-270, 2009.
33. - secretion across rat fetal distal lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 282: L650-L658, 2002.
34. Ma C, Polishchuk AL, Ohigashi Y, Stouffer AL, Schon A, Magavern E, Jing X, Lear JD, Freire E, Lamb RA, DeGrado WF, Pinto LH. Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel. Proc Natl Acad Sci USA 106: 12283-12288, 2009.
35. Matalon S, O'Brodovich H. Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 61: 627-661, 1999.
36. Muanprasat C, Sonawane ND, Salinas D, Taddei A, Galietta LJ, Verkman AS. Discovery of glycine hydrazide pore-occluding CFTR inhibitors: mechanism, structure-activity analysis, and in vivo efficacy. J Gen Physiol 124: 125-137, 2004.
37. Noah JW, Noah DL, Matalon S. Influenza exerts continued pressure in an era of modern medicine. Am J Respir Cell Mol Biol 41: 3-7, 2009.
38. Okiyoneda T, Niibori A, Harada K, Kohno T, Hashimoto Y, Kusuhara H, Takada T, Shuto T, Suico MA, Sugiyama Y, Kai H. Bafilomycin A1-sensitive pathway is required for the maturation of cystic fibrosis transmembrane conductance regulator. Biochim Biophys Acta 1763: 1017-1023, 2006.
39. Perrone LA, Belser JA, Wadford DA, Katz JM, Tumpey TM. Inducible nitric oxide contributes to viral pathogenesis following highly pathogenic influenza virus infection in mice. J Infect Dis. 2013 Feb. 18 [Epub ahead of print]
40. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Banfi B, Horswill AR, Stoltz DA, McCray PB Jr, Welsh MJ, Zabner J. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487: 109-113, 2012.
41. Pinto LH, Holsinger LJ, Lamb RA. Influenza virus M2 protein has ion channel activity. Cell 69: 517-528, 1992.
42. Ratner D, Mueller C. Immune responses in cystic fibrosis: are they intrinsically defective? Am J Respir Cell Mol Biol 46: 715-722, 2012.
43. Sakaguchi T, Leser GP, Lamb RA. The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J Cell Biol 133: 733-747, 1996.
44. Shih SR, Nemeroff ME, Krug RM. The choice of alternative 5= splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci USA 92: 6324-6328, 1995.
45. + channel 3 and cystic fibrosis transmembrane conductance regulator. J Biol Chem 281: 36960-36968, 2006.
46. Takeda M, Pekosz A, Shuck K, Pinto LH, Lamb RA. Influenza a virus M2 ion channel activity is essential for efficient replication in tissue culture. J Virol 76: 1391-1399, 2002.
47. Takeuchi K, Lamb RA. Influenza virus M2 protein ion channel activity stabilizes the native form of fowl plague virus hemagglutinin during intracellular transport. J Virol 68: 911-919, 1994.
48. Tobler K, Kelly ML, Pinto LH, Lamb RA. Effect of cytoplasmic tail truncations on the activity of the M2 ion channel of influenza A virus. J Virol 73: 9695-9701, 1999.
49. Tradtrantip L, Sonawane ND, Namkung W, Verkman AS. Nanomolar potency pyrimido-pyrrolo-quinoxalinedione CFTR inhibitor reduces cyst size in a polycystic kidney disease model. J Med Chem 52: 6447-6455, 2009.
50. Traylor ZP, Aeffner F, Davis IC. Influenza A H1N1 induces declines in alveolar gas exchange in mice consistent with rapid post-infection progression from acute lung injury to ARDS. Influenza Other Respi Viruses. 2012 Aug 2. doi: 10.1111/j.1750-2659.2012.00414.x. [Epub ahead of print]
51. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171: 1215-1223, 2007.
52. Vij N, Mazur S, Zeitlin PL. CFTR is a negative regulator of NFkappaB mediated innate immune response. PLoS ONE 4: e4664, 2009.
53. Weiser N, Molenda N, Urbanova K, Bahler M, Pieper U, Oberleithner H, Schillers H. Paracellular permeability of bronchial epithelium is controlled by CFTR. Cell Physiol Biochem 28: 289-296, 2011.
54. Weisz OA. Acidification and protein traffic. Int Rev Cytol 226: 259-319, 2003.
55. Wolk KE, Lazarowski ER, Traylor ZP, Yu EN, Jewell NA, Durbin RK, Durbin JE, Davis IC. Influenza a virus inhibits alveolar fluid clearance in BALB/c mice. Am J Respir Crit Care Med 178: 969-976, 2008.
56. Xu W, Zheng S, Goggans TM, Kiser P, Quinones-Mateu ME, Janocha AJ, Comhair SA, Slee R, Williams BR, Erzurum SC. Cystic fibrosis and normal human airway epithelial cell response to influenza a viral infection. J Interferon Cytokine Res 26: 609-627, 2006.
57. Yang Y, Kitagaki J, Dai RM, Tsai YC, Lorick KL, Ludwig RL, Pierre SA, Jensen JP, Davydov IV, Oberoi P, Li CC, Kenten JH, Beutler JA, Vousden KH, Weissman AM. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res 67: 9472-9481, 2007.
58. Zhang W, Na T, Peng JB. WNK3 positively regulates epithelial calcium channels TRPV5 and TRPV6 via a kinase-dependent pathway. Am J Physiol Renal Physiol 295: F1472-F1484, 2008.