Nitric oxide promotes airway epithelial wound repair through enhanced activation of MMP-9

American Journal of Respiratory Cell and Molecular Biology

Volumn 36, Issue 2, 2007, Pages 138-146

  Bove, Peter F ^a   Wesley, Umadevi V ^a   Greul, Anne Katrin ^a   Hristova, Milena ^a   Dostmann, Wolfgang R ^a   Van Der Vliet, Albert ^a,b  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Cell migration; cGMP; DT 2; Guanylyl cyclase

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; GELATINASE B; GUANYLATE CYCLASE INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; KT 5823; N(G) METHYLARGININE; NITRIC OXIDE;

ARTICLE; CELL IMMORTALIZATION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; RESPIRATORY EPITHELIUM; WOUND CLOSURE; WOUND HEALING;

CELL MOVEMENT; CYCLIC GMP; ENZYME ACTIVATION; EPITHELIAL CELLS; GELATINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MATRIX METALLOPROTEINASE 9; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITROSO COMPOUNDS; OMEGA-N-METHYLARGININE; RESPIRATORY SYSTEM; RNA, MESSENGER; WOUND HEALING;

EID: 33846897407     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2006-0253SM     Document Type: Article

References (41)

1. Parks WC, Shapiro SD. Matrix metalloproteinases in lung biology. Respir Res 2001;2:10-19.
2. Van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002;37:375-536.
3. Atkinson JJ, Senior RM. Matrix metalloproteinase-9 in lung remodeling. Am J Respir Cell Mol Biol 2003;28:12-24.
4. McMillan SJ, Kearley J, Campbell JD, Zhu XW, Larbi KY, Shipley JM, Senior RM, Nourshargh S, Lloyd CM. Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation. J Immunol 2004;172:2586-2594.
5. Lanone S, Zheng T, Zhu Z, Liu W, Lee CG, Ma B, Chen Q, Homer RJ, Wang J, Rabach LA, et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Invest 2002;110:463-474.
6. Kobayashi T, Kishimoto J, Hattori S, Wachi H, Shinkai H, Burgeson RE. Matrix metalloproteinase 9 expression is coordinately modulated by the KRE-M9 and 12-O-tetradecanoyl-phorbol-13-acetate responsive elements. J Invest Dermatol 2004;122:278-285.
7. Ma Z, Shah RC, Chang MJ, Benveniste EN. Coordination of cell signaling, chromatin remodeling, histone modifications, and regulator recruitment in human matrix metalloproteinase 9 gene transcription. Mol Cell Biol 2004;24:5496-5509.
8. Fridman R, Toth M, Chvyrkova I, Meroueh SO, Mobashery S. Cell surface association of matrix metalloproteinase-9 (gelatinase B). Cancer Metastasis Rev 2003;22:153-166.
9. Legrand C, Gilles C, Zahm JM, Polette M, Buisson AC, Kaplan H, Birembaut P, Tournier JM. Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J Cell Biol 1999;146:517-529.
10. Mohan R, Chintala SK, Jung JC, Villar WV, McCabe F, Russo LA, Lee Y, McCarthy BE, Wollenberg KR, Jester JV, et al. Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration. J Biol Chem 2002;277:2065-2072.
11. Coraux C, Martinella-Catusse C, Nawrocki-Raby B, Hajj R, Burlet H, Escotte S, Laplace V, Birembaut P, Puchelle E. Differential expression of matrix metalloproteinases and interleukin-8 during regeneration of human airway epithelium in vivo. J Pathol 2005;206:160-169.
12. Xu W, Zheng S, Dweik RA, Erzurum SC. Role of epithelial nitric oxide in airway viral infection. Free Radic Biol Med 2006;41:19-28.
13. Duszyk M. Regulation of anion secretion by nitric oxide in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2001;281:L450-L457.
14. Hardiman KM, McNicholas-Bevensee CM, Fortenberry J, Myles CT, Malik B, Eaton DC, Matalon S. Regulation of amiloride-sensitive Na(+) transport by basal nitric oxide. Am J Respir Cell Mol Biol 2004;30:720-728.
15. Gookin JL, Rhoads JM, Argenzio RA. Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum. Am J Physiol Gastrointest Liver Physiol 2002;283:G157-G168.
16. Yamasaki K, Edington HD, McClosky C, Tzeng E, Lizonova A, Kovesdi I, Steed DL, Billiar TR. Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J Clin Invest 1998;101:967-971.
17. Lopez-Rivera E, Lizarbe TR, Martinez-Moreno M, Lopez-Novoa JM, Rodriguez-Barbero A, Rodrigo J, Fernandez AP, Alvarez-Barrientos A, Lamas S, Zaragoza C. Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci USA 2005;102:3685-3690.
18. Jadeski LC, Chakraborty C, Lala PK. Nitric oxide-mediated promotion of mammary tumour cell migration requires sequential activation of nitric oxide synthase, guanylate cyclase and mitogen-activated protein kinase. Int J Cancer 2003;106:496-504.
19. Kawasaki K, Smith RS Jr, Hsieh CM, Sun J, Chao J, Liao JK. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 2003;23:5726-5737.
20. Bogdan C. Nitric oxide and the regulation of gene expression. Trends Cell Biol 2001;11:66-75.
21. Hemish J, Nakaya N, Mittal V, Enikolopov G. Nitric oxide activates diverse signaling pathways to regulate gene expression. J Biol Chem 2003;278:42321-42329.
22. Akool el S, Kleinert H, Hamada FM, Abdelwahab MH, Forstermann U, Pfeilschifter J, Eberhardt W. Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol Cell Biol 2003;23:4901-4916.
23. Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, Strongin A, Smith JW, Liddington RC, Lipton SA. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 2002;297:1186-1190.
24. Knipp BS, Ailawadi G, Ford JW, Peterson DA, Eagleton MJ, Roelofs KJ, Hannawa KK, Deogracias MP, Ji B, Logsdon C, et al. Increased MMP-9 expression and activity by aortic smooth muscle cells after nitric oxide synthase inhibition is associated with increased nuclear factor-kappaB and activator protein-1 activity. J Surg Res 2004;116:70-80.
25. Marcet-Palacios M, Graham K, Cass C, Befus AD, Mayers I, Radomski MW. Nitric oxide and cyclic GMP increase the expression of matrix metalloproteinase-9 in vascular smooth muscle. J Pharmacol Exp Ther 2003;307:429-436.
26. Okamoto T, Valacchi G, Gohil K, Akaike T, van der Vliet A. S-nitrosothiols inhibit cytokine-mediated induction of matrix metalloproteinase-9 in airway epithelial cells. Am J Respir Cell Mol Biol 2002;27:463-473.
27. Guo FH, Comhair SA, Zheng S, Dweik RA, Eissa NT, Thomassen MJ, Calhoun W, Erzurum SC. Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J Immunol 2000;164:5970-5980.
28. Taylor MS, Okwuchukwuasanya C, Nickl CK, Tegge W, Brayden JE, Dostmann WR. Inhibition of cGMP-dependent protein kinase by the cell-permeable peptide DT-2 reveals a novel mechanism of vasoregulation. Mol Pharmacol 2004;65:1111-1119.
29. White SR, Tse R, Marroquin BA. Stress-activated protein kinases mediate cell migration in human airway epithelial cells. Am J Respir Cell Mol Biol 2005;32:301-310.
30. Zahm JM, Kaplan H, Herard AL, Doriot F, Pierrot D, Somelette P, Puchelle E. Cell migration and proliferation during the in vitro wound repair of the respiratory epithelium. Cell Motil Cytoskeleton 1997;37:33-43.
31. Yan C, Wang H, Aggarwal B, Boyd DD. A novel homologous recombination system to study 92 kDa type IV collagenase transcription demonstrates that the NF-kappaB motif drives the transition from a repressed to an activated state of gene expression. FASEB J 2004;18:540-541.
32. Smolenski A, Poller W, Walter U, Lohmann SM. Regulation of human endothelial cell focal adhesion sites and migration by cGMP-dependent protein kinase I. J Biol Chem 2000;275:25723-25732.
33. Jackson AL, Linsley PS. Noise amidst the silence: off-target effects of siRNAs? Trends Genet 2004;20:521-524.
34. Legrand C, Polette M, Tournier JM, de Bentzmann S, Huet E, Monteau M, Birembaut P. uPA/plasmin system-mediated MMP-9 activation is implicated in bronchial epithelial cell migration. Exp Cell Res 2001;264:326-336.
35. Eriksson U, Egermann U, Bihl MP, Gambazzi F, Tamm M, Holt PG, Bingisser RM. Human bronchial epithelium controls TH2 responses by TH1-induced, nitric oxide-mediated STAT5 dephosphorylation: implications for the pathogenesis of asthma. J Immunol 2005;175:2715-2720.
36. Rose F, Guthmann B, Tenenbaum T, Fink L, Ghofrani A, Weissmann N, Konig P, Ermert L, Dahlem G, Haenze J, et al. Apical, but not basolateral, endotoxin preincubation protects alveolar epithelial cells against hydrogen peroxide-induced loss of barrier function: the role of nitric oxide synthesis. J Immunol 2002;169:1474-1481.
37. Zaragoza C, Soria E, Lopez E, Browning D, Balbin M, Lopez-Otin C, Lamas S. Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol Pharmacol 2002;62:927-935.
38. Li D, Shirakami G, Zhan X, Johns RA. Regulation of ciliary beat frequency by the nitric oxide-cyclic guanosine monophosphate signaling pathway in rat airway epithelial cells. Am J Respir Cell Mol Biol 2000;23:175-181.
39. Xu W, Leung S, Wright J, Guggino SE. Expression of cyclic nucleotide-gated cation channels in airway epithelial cells. J Membr Biol 1999;171:117-126.
40. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phox-dependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 2005;97:533-540.
41. Leir SH, Baker JE, Holgate ST, Lackie PM. Increased CD44 expression in human bronchial epithelial repair after damage or plating at low cell densities. Am J Physiol Lung Cell Mol Physiol 2000;278:L1129-L1137.