Functional interplay between endothelial nitric oxide synthase and membrane type 1-matrix metalloproteinase in migrating endothelial cells

Blood

Volumn 110, Issue 8, 2007, Pages 2916-2923

  Genís, Laura ^a   Gonzalo, Pilar ^a   Tutor, Antonio S ^a   Gálvez, Beatriz G ^a   Martínez Ruiz, Antonio ^a   Zaragoza, Carlos ^a   Lamas, Santiago ^b   Tryggvason, Karl ^c   Apte, Suneel S ^d   Arroyo, Alicia G ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c KAROLINSKA INSTITUTE   (Sweden)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MATRIX METALLOPROTEINASE 14; NEUTRALIZING ANTIBODY; NITRIC OXIDE;

ARTICLE; CAPILLARY; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; ENZYME SUBSTRATE; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UPREGULATION; VASCULARIZATION;

EID: 35548935247     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-01-068080     Document Type: Article

References (39)

1. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373-376.
2. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation. 2006;113:1708-1714.
3. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest. 1998;101:731-736.
4. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653-660.
5. Moulton KS, Vakili K, Zurakowski D, et al. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A. 2003;100:4736-4741.
6. van der Zee R, Murohara T, Luo Z, et al. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation. 1997;95:1030-1037.
7. Hood JD, Meininger CJ, Ziche M, Granger HJ. VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am J Physiol. 1998;274:H1054-1058.
8. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda F, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol. 1996;270:H411-415.
9. Murohara T, Horowitz JR, Silver M, et al. Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation. 1998;97:99-107.
10. Noiri E, Lee E, Testa J, et al. Podokinesis in endothelial cell migration: role of nitric oxide. Am J Physiol. 1998;274:C236-244.
11. Lee PC, Salyapongse AN, Bragdon GA, et al. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol. 1999;277:H1600-1608.
12. Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol. 2004;48:411-424.
13. Galvez BG, Matias-Roman S, Albar JP, Sanchez-Madrid F, Arroyo AG. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J Biol Chem. 2001;276:37491-37500.
14. Galvez BG, Genis L, Matias-Roman S, et al. Membrane type 1-matrix metalloproteinase is regulated by chemokines monocyte-chemoattractant protein-1/ccl2 and interleukin-8/CXCL8 in endothelial cells during angiogenesis. J Biol Chem. 2005;280:1292-1298.
15. Oblander SA, Zhou Z, Galvez BG, et al. Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev Biol. 2005;277:255-269.
16. Galvez BG, Matias-Roman S, Yanez-Mo M, Sanchez-Madrid F, Arroyo AG. ECM regulates MT1-MMP localization with beta1 or alphavbeta3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J Cell Biol. 2002;159:509-521.
17. Galvez BG, Matias-Roman S, Yanez-Mo M, Vicente-Manzanares M, Sanchez-Madrid F, Arroyo AG. Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. Mol Biol Cell. 2004;15:678-687.
18. Parton RG. Caveolae-from ultrastructure to molecular mechanisms. Nat Rev Mol Cell Biol. 2003;4:162-167.
19. Goligorsky MS, Li H, Brodsky S, Chen J. Relationships between caveolae and eNOS: everything in proximity and the proximity of everything. Am J Physiol Renal Physiol. 2002;283:F1-10.
20. Zhou Z, Apte SS, Soininen R, et al. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A. 2000;97:4052-4057.
21. Chun TH, Sabeh F, Ota I, et al. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J Cell Biol. 2004;167:757-767.
22. Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science. 2003;302:1704-1709.
23. Murohara T, Witzenbichler B, Spyridopoulos I, et al. Role of endothelial nitric oxide synthase in endothelial cell migration. Arterioscler Thromb Vasc Biol. 1999;19:1156-1161.
24. Ziche M, Morbidelli L, Masini E, et al. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest. 1994;94:2036-2044.
25. Griscavage JM, Hobbs AJ, Ignarro LJ. Negative modulation of nitric oxide synthase by nitric oxide and nitroso compounds. Adv Pharmacol. 1995;34:215-234.
26. Zhao X, Lu X, Feng Q. Deficiency in endothelial nitric oxide synthase impairs myocardial angiogenesis. Am J Physiol Heart Circ Physiol. 2002;283:H2371-2378.
27. Bulotta S, Cerullo A, Barsacchi R, et al. Endothelial nitric oxide synthase is segregated from caveolin-1 and localizes to the leading edge of migrating cells. Exp Cell Res. 2006;312:877-889.
28. Maniatis NA, Brovkovych V, Allen SE, et al. Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res. 2006;99:870-877.
29. Anilkumar N, Uekita T, Couchman JR, Nagase H, Seiki M, Itoh Y. Palmitoylation at Cys574 is essential for MT1-MMP to promote cell migration. Faseb J. 2005;19:1326-1328.
30. Fernandez-Hernando C, Fukata M, Bernatchez PN, et al. Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. J Cell Biol. 2006;174:369-377.
31. + waves preferentially originate at specific loci in caveolin-rich cell edges. Proc Natl Acad Sci U S A. 1998;95:5009-5014.
32. Price LS, Leng J, Schwartz MA, Bokoch GM. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell. 1998;9:1863-1871.
33. Eriksson A, Cao R, Roy J, et al. Small GTP-binding protein Rac is an essential mediator of vascular endothelial growth factor-induced endothelial fenestrations and vascular permeability. Circulation. 2003;107:1532-1538.
34. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399:601-605.
35. Ackah E, Yu J, Zoellner S, et al. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest. 2005;115:2119-2127.
36. Lowenstein CJ. Nitric oxide regulation of protein trafficking in the cardiovascular system. Cardiovasc Res. 2007;75:240-246.
37. Genis L, Galvez BG, Gonzalo P, Arroyo AG. MT1-MMP: universal or particular player in angiogenesis? Cancer Metastasis Rev. 2006;25:77-86.
38. Jones SP, Bolli R. The ubiquitous role of nitric oxide in cardioprotection. J Mol Cell Cardiol. 2006;40:16-23.
39. Filippov S, Koenig GC, Chun TH, et al. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med. 2005;202:663-671.