Homocysteine Disrupts Outgrowth of Microvascular Endothelium by an iNOS-Dependent Mechanism

Microcirculation

Volumn 21, Issue 6, 2014, Pages 541-550

  Mayo, Jamie N ^a   Chen, Cheng Hung ^a   Liao, Francesca Fang ^b   Bearden, Shawn E ^a  

^a Nucl Eng Idaho State University   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Actin; Angiogenesis; Endothelium; Homocysteine; Inducible nitric oxide synthase

Indexed keywords

F ACTIN; HOMOCYSTEINE; INDUCIBLE NITRIC OXIDE SYNTHASE; SMALL INTERFERING RNA; NOS2 PROTEIN, MOUSE;

ACTIN FILAMENT; ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL MIGRATION; CELL PROLIFERATION; CHOROID; CONTROLLED STUDY; ENZYME ACTIVITY; EXPLANT; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MALE; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM; ANIMAL; CELL LINE; CELL MOTION; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ACTIN CYTOSKELETON; ANIMALS; CELL LINE; CELL MOVEMENT; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; HOMOCYSTEINE; MALE; MICE; MICE, KNOCKOUT; MICROVESSELS; NITRIC OXIDE SYNTHASE TYPE II;

EID: 84905494698     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12133     Document Type: Article

References (35)

1. Banan A, Fields JZ, Zhang Y, Keshavarzian A. iNOS upregulation mediates oxidant-induced disruption of F-actin and barrier of intestinal monolayers. Am J Physiol Gastrointest Liver Physiol 280: G1234-G1246, 2001.
2. Barth BM, Stewart-Smeets S, Kuhn TB. Proinflammatory cytokines provoke oxidative damage to actin in neuronal cells mediated by Rac1 and NADPH oxidase. Mol Cell Neurosci 41: 274-285, 2009.
3. Bayless KJ, Johnson GA. Role of the cytoskeleton in formation and maintenance of angiogenic sprouts. J Vasc Res 48: 369-385, 2011.
4. Beard RS, Jr, Reynolds JJ, Bearden SE. Hyperhomocysteinemia increases permeability of the blood-brain barrier by NMDA receptor-dependent regulation of adherens and tight junctions. Blood 118: 2007-2014, 2011.
5. Beard RS, Jr, Reynolds JJ, Bearden SE. Metabotropic glutamate receptor 5 mediates phosphorylation of vascular endothelial cadherin and nuclear localization of beta-catenin in response to homocysteine. Vascul Pharmacol 56: 159-167, 2012.
6. Bearden SE, Beard RS, Jr, Pfau JC. Extracellular transsulfuration generates hydrogen sulfide from homocysteine and protects endothelium from redox stress. Am J Physiol Heart Circ Physiol 299: H1568-H1576, 2010.
7. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271: C1424-C1437, 1996.
8. Bloor CM. Angiogenesis during exercise and training. Angiogenesis 8: 263-271, 2005.
9. Carmel R, Jacobsen DW. Homocysteine in Health and Disease, 1st edn. Cambridge, UK: Cambridge University Press, 2001.
10. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438: 932-936, 2005.
11. Chen CH, Beard RS, Bearden SE. Homocysteine impairs endothelial wound healing by activating metabotropic glutamate receptor 5. Microcirculation 19: 285-295, 2012.
12. Daniliuc S, Bitterman H, Rahat MA, Kinarty A, Rosenzweig D, Lahat N. Hypoxia inactivates inducible nitric oxide synthase in mouse macrophages by disrupting its interaction with alpha-actinin 4. J Immunol 171: 3225-3232, 2003.
13. Drew B, Leeuwenburgh C. Aging and the role of reactive nitrogen species. Ann N Y Acad Sci 959: 66-81, 2002.
14. Duan J, Murohara T, Ikeda H, Sasaki K, Shintani S, Akita T, Shimada T, Imaizumi T. Hyperhomocysteinemia impairs angiogenesis in response to hindlimb ischemia. Arterioscler Thromb Vasc Biol 20: 2579-2585, 2000.
15. Faraci FM. Hyperhomocysteinemia: a million ways to lose control. Arterioscler Thromb Vasc Biol 23: 371-373, 2003.
16. Garcin ED, Arvai AS, Rosenfeld RJ, Kroeger MD, Crane BR, Andersson G, Andrews G, Hamley PJ, Mallinder PR, Nicholls DJ, St-Gallay SA, Tinker AC, Gensmantel NP, Mete A, Cheshire DR, Connolly S, Stuehr DJ, Aberg A, Wallace AV, Tainer JA, Getzoff ED. Anchored plasticity opens doors for selective inhibitor design in nitric oxide synthase. Nat Chem Biol 4: 700-707, 2008.
17. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 272: 4959-4963, 1997.
18. Gu W, Gu C, Jiang W, Wester P. Neurotransmitter synthesis in poststroke cortical neurogenesis in adult rats. Stem cell research 4: 148-154, 2010.
19. Harris LK, McCormick J, Cartwright JE, Whitley GS, Dash PR. S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp Cell Res 314: 1765-1776, 2008.
20. Hedrick TL. Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 3: 034001, 2008.
21. Isenberg JS, Martin-Manso G, Maxhimer JB, Roberts DD. Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat Rev Cancer 9: 182-194, 2009.
22. Lijnen HR. Angiogenesis and obesity. Cardiovasc Res 78: 286-293, 2008.
23. Lindsay SL, Ramsey S, Aitchison M, Renne T, Evans TJ. Modulation of lamellipodial structure and dynamics by NO-dependent phosphorylation of VASP Ser239. J Cell Sci 120: 3011-3021, 2007.
24. Mayo JN, Beard RS, Jr, Price TO, Chen CH, Erickson MA, Ercal N, Banks WA, Bearden SE. Nitrative stress in cerebral endothelium is mediated by mGluR5 in hyperhomocysteinemia. J Cereb Blood Flow Metab 32: 825-834, 2012.
25. Mehta SL, Manhas N, Raghubir R. Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res Rev 54: 34-66, 2007.
26. Montesano R, Pepper MS, Mohle-Steinlein U, Risau W, Wagner EF, Orci L. Increased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogene. Cell 62: 435-445, 1990.
27. Nagai Y, Tasaki H, Takatsu H, Nihei S, Yamashita K, Toyokawa T, Nakashima Y. Homocysteine inhibits angiogenesis in vitro and in vivo. Biochem Biophys Res Commun 281: 726-731, 2001.
28. National Academy of Sciences. Guide for the Care and Use of Laboratory Animals. Washington, DC: The National Academies Press, 2011.
29. Oosterbaan AM, Steegers EA, Ursem NT. The effects of homocysteine and folic acid on angiogenesis and VEGF expression during chicken vascular development. Microvasc Res 83: 98-104, 2011.
30. Patel P, Qi WN, Allen DM, Chen LE, Seaber AV, Stamler JS, Urbaniak JR. Inhibition of iNOS with 1400W improves contractile function and alters nos gene and protein expression in reperfused skeletal muscle. Microsurgery 24: 324-331, 2004.
31. Rasband WS. Image J. U.S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997-2004.
32. Rezakhaniha R, Agianniotis A, Schrauwen JT, Griffa A, Sage D, Bouten CV, van de Vosse FN, Unser M, Stergiopulos N. Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11: 461-473, 2012.
33. Ridley AJ. Life at the leading edge. Cell 145: 1012-1022, 2011.
34. Uno K, Iuchi Y, Fujii J, Sugata H, Iijima K, Kato K, Shimosegawa T, Yoshimura T. In vivo study on cross talk between inducible nitric-oxide synthase and cyclooxygenase in rat gastric mucosa: effect of cyclooxygenase activity on nitric oxide production. J Pharmacol Exp Ther 309: 995-1002, 2004.
35. Zhu Y, Nikolic D, Van Breemen RB, Silverman RB. Mechanism of inactivation of inducible nitric oxide synthase by amidines. Irreversible enzyme inactivation without inactivator modification. J Am Chem Soc 127: 858-868, 2005.