Nitric oxide prevents aortic neointimal hyperplasia by controlling macrophage polarization

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 8, 2014, Pages 1739-1746

  Lavin, Begoña ^a   Gómez, Monica ^a   Pello, Oscar M ^a   Castejon, Borja ^a   Piedras, Maria J ^c   Saura, Marta ^b   Zaragoza, Carlos ^c  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b UNIVERSITY OF ALCALÁ   (Spain)

^c UNIVERSIDAD FRANCISCO DE VITORIA   (Spain)

Author keywords

Angioplasty; Entothelial nitric oxide synthase 3; Macrophage; Matrix metalloproteinase 13; Neointima

Indexed keywords

COLLAGENASE 3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 5; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; STEM CELL ANTIGEN 1; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA DISEASE; AORTIC NEOINTIMAL HYPERPLASIA; ARTICLE; CAROTID ARTERY; CAROTID ENDARTERECTOMY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; HYPERPLASIA; MACROPHAGE; MOUSE; NEOINTIMA; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPOLARIZATION; SMOOTH MUSCLE FIBER; STEM CELL; VASCULAR SMOOTH MUSCLE;

ANGIOPLASTY; ENTOTHELIAL NITRIC OXIDE SYNTHASE 3; MACROPHAGE; MATRIX METALLOPROTEINASE-13; NEOINTIMA;

AGED; AGED, 80 AND OVER; ANIMALS; AORTA; AORTIC DISEASES; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYPERPLASIA; INFLAMMATION MEDIATORS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-MYC; TIME FACTORS;

EID: 84904668397     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303866     Document Type: Article

References (41)

1. Young JJ. Neointimal formation following drug-eluting stents: physiology, timeline, and the influence of drug delivery systems. Rev Cardiovasc Med. 2007;8(Suppl 1):S3-S10.
2. Popowich DA, Varu V, Kibbe MR. Nitric oxide: what a vascular surgeon needs to know. Vascular. 2007;15:324-335.
3. Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res. 1994;75:539-545.
4. Iaconetti C, Polimeni A, Sorrentino S, Sabatino J, Pironti G, Esposito G, Curcio A, Indolfi C. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res Cardiol. 2012;107:296.
5. Kim J, Zhang L, Peppel K, Wu JH, Zidar DA, Brian L, De Wire SM, Exum ST, Lefkowitz RJ, Freedman NJ. Beta-arrestins regulate atherosclerosis and neointimal hyperplasia by controlling smooth muscle cell proliferation and migration. Circ Res. 2008;103:70-79.
6. Zaidi SH, You XM, Ciura S, O' Blenes S, Husain M, Rabinovitch M. Suppressed smooth muscle proliferation and inflammatory cell invasion after arterial injury in elafin-overexpressing mice. J Clin Invest. 2000;105:1687-1695.
7. Cui B, Huang L, Fang Y, Guo R, Yin Y, Zhao X. Transplantation of endothelial progenitor cells overexpressing endothelial nitric oxide synthase enhances inhibition of neointimal hyp erplasia and restores endotheliumdependent vasodilatation. Microvasc Res. 2011;81:143-150.
8. Cooney R, Hynes SO, Sharif F, Howard L, O'Brien T. Effect of gene delivery of NOS isoforms on intimal hyperplasia and endothelial regeneration after balloon injury. Gene Ther. 2007;14:396-404.
9. Sharif F, Hynes SO, Cooney R, Howard L, McMahon J, Daly K, Crowley J, Barry F, O'Brien T. Gene- eluting stents: adenovirus-mediated delivery of eNOS to the blood vessel wall accelerates re-endothelialization and inhibits restenosis. Mol Ther. 2008;16:1674-1680.
10. Marks DS, Vita JA, Folts JD, Keaney JF Jr, Welch GN, Loscalzo J. Inhibition of neointimal proliferation in rabbits after vascular injury by a single treatment with a protein adduct of nitric oxide. J Clin Invest. 1995;96:2630-2638.
11. Le Tourneau T, Van Belle E, Corseaux D, Vallet B, Lebuffe G, Dupuis B, Lablanche JM, McFadden E, Bauters C, Bertrand ME. Role of nitric oxide in restenosis after experi mental balloon angioplasty in the hypercholesterolemic rabbit: effects on neointimal hyperplasia and vascular remodeling. J Am Coll Cardiol. 1999;33:876-882.
12. Stöger JL, Gijbels MJ, van der Velden S, Man ca M, van der Loos CM, Biessen EA, Daemen MJ, Lutgens E, de Winther MP. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis. 2012;225:461-468.
13. Hoeksema MA, Stöger JL, de Winther MP. Molecular pathways regulating macrophage polarization: implications for atherosclerosis. Curr Atheroscler Rep. 2012;14:254-263.
14. Baitsch D, Bock HH, Engel T, Telg mann R, Müller-Tidow C, Varga G, Bot M, Herz J, Robenek H, von Eckardstein A, Nofer JR. Apolipoprotein E induces antiinflammatory phenotype in macrophages. Arterioscler Thromb Vasc Biol. 2011;31:1160-1168.
15. Usher MG, Duan SZ, Ivaschenko CY, Frieler RA, Berger S, Schütz G, Lumeng CN, Mortensen RM. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest. 2010;120:3350-3364.
16. Kobayashi Y. The regulatory role of nitric oxide in proinflammatory cytokine expression during the induction and resolution of inflammation. J Leukoc Biol. 2010;88:1157-1162.
17. Tarín C, Gomez M, Calvo E, López JA, Zaragoza C. Endothelial nitric oxide deficiency reduces MMP-13-mediated cleavage of ICAM-1 in vascular endothelium: a role in atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:27-32.
18. Lizarbe TR, García-Rama C, Tarín C, Saura M, Calvo E, López JA, López- Otín C, Folgueras AR, Lamas S, Z aragoza C. Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair. FASEB J. 2008;22:3207-3215.
19. López-Rivera E, Lizarbe TR, Martínez-Moreno M, López-No voa JM, Rodríguez-Barbero A, Rodrigo J, Fernández AP, Alvarez-Barrientos A, Lamas S, Zaragoza C. Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci U S A. 2005;102:3685-3690.
20. Zaragoza C, Soria E, López E, Browning D, Balbín M, López-Otín 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.
21. Zaragoza C, Balbín M, López-Otín C, Lamas S. Nitric oxide regulates matrix metalloprotease-13 expression and activity in endothelium. Kidney Int. 2002;61:804-808.
22. Wang H, Keiser JA. Expression of membrane-type matrix metalloproteinase in rabbit neointimal tissue and its correlation with matrix-metalloproteinase- 2 activation. J Vasc Res. 1998;35:45-54.
23. Wang Z, Kong L, Kang J, Vaughn D M, Bush GD, Walding AL, Grigorian AA, Robinson JS Jr, Nakayama DK. Interleukin-lβ induces migration of rat arterial smooth muscle cells through a mechanism involving increased matrix metalloproteinase-2 activity. J Surg Res. 2011;169:328-336.
24. Pello OM, De Pizzol M, Mirolo M, Soucek L, Zammataro L, Amabile A, Doni A, Nebuloni M, Swigart LB, Evan GI, Mantovani A, Locati M. Role of c-MYC in alte rnative activation of human macrophages and tumorassociated macrophage biology. Blood. 2012;119:411-421.
25. Ekshyyan VP, Hebert VY, Khandelwal A, Dugas TR. Resveratrol inhibits rat aortic vascular smooth muscle cell proliferation via estrogen receptor dependent nitric oxide production. J Cardiovasc Pharmacol. 2007;50:83-93.
26. Havelka GE, Moreira ES, Rodriguez MP, Tsihlis ND, Wang Z, Martínez J, Hrabie JA, Kiefer LK, Kibbe MR. Nitric oxide delivery via a permeable balloon catheter inhibits neointimal growth after arterial injury. J Surg Res. 2013;180:35-42.
27. Kapadia MR, Chow LW, Tsihlis ND, Ahanchi SS, Eng JW, Murar J, Martinez J, Popowich DA, Jiang Q, Hrabie JA, Saavedra JE, Keefer LK, Hulvat JF, Stupp SI, Kibbe MR. Nitric oxide and nanotechnology: a novel approach to inhibit neointi mal hyperplasia. J Vasc Surg. 2008;47:173-182.
28. Tsihlis ND, Kapadia MR, Vavra AK, Flannery WD, Oustwani CS, Jiang Q, Kibbe MR. Nitric oxide may inhibit neointimal hyperplasia by decreasing iso peptidase T levels and activity in the vasculature. J Vasc Surg. 2013;58:179-186.
29. Tsihlis ND, Kapadia MR, Vavra AK, Jiang Q, Fu B, Martinez J, Kibbe MR. Nitric oxide decreases activity and levels of the 11S proteasome activator PA28 in the vasculature. Nitric Oxide. 2012;27:50-58.
30. Tsihlis ND, Oustwani CS, Vavra AK, Jiang Q, Keefer LK, Kibbe MR. Nitric oxide inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia by increasing the ubiquitination and degradation of UbcH10. Cell Biochem Biophys. 2011;60:89-97.
31. Yu J, Zhang Y, Zhang X, Rudic RD, Bauer PM, Altieri DC, Sessa WC. Endothelium derived nitric oxide synthase negatively regulates the PDGFsurvivin pathway during flow-dependent vascular remodeling. PLoS One. 2012;7:e31495.
32. Kang WC, Il Moon C, Lee K, Han SH, Suh SY, Moon J, Shin MS, Ahn T, Shin EK. Comparison of inflammatory markers for the prediction of neointimal hyperplasia after drug-eluting st ent implantation. Coron Artery Dis. 2011;22:526-532.
33. Paulsson J, Dadfar E, Held C, Jacobson SH, Lundahl J. Activation of peripheral and in vivo transmigrated neutrophils in patients with stable coronary artery disease. Atherosclerosis. 2007;192:328-334.
34. Suzuki H, Kusuyama T, Sato R, Yokota Y, Tsunoda F, Sato T, Shoji M, Iso Y, Koba S, Katagiri T. Elevation of matrix metall oproteinases and interleukin-6 in the culprit coronary artery of myocardial infarction. Eur J Clin Invest. 2008;38:166-173.
35. Lindmark E, Diderholm E, Wallentin L, Siegbahn A. Relationship between interle ukin 6 and mortality in patients with unstable coronary artery disease: effects of an early invasive or noninvasive strategy. JAMA. 2001;286:2107-2113.
36. Tedgui A. The role of inflammation in atherothrombosis: implications for clinical practice. Vasc Med. 2005;10:45-53.
37. Weis M, Pehlivanli S, Meiser BM, von Scheidt W. Simvastatin treatment is associated with improvement in coronary endothelial function and decreased cytokine activation in patients after heart transplantation. J Am Coll Cardiol. 2001;38:814-818.
38. Myung SC, Han JH, Song KK, Kang GH, Lee SY, Kim TH, Lee MY, Kim HW, Kim SC. The effe cts of interleukin-6 on the contraction and relaxation responses of the cavernous smooth muscle from rats. Eur J Pharmacol. 2008;589:228-232.
39. Orshal JM, Khalil RA. Reduced endothelial NO-cGMP-mediated vascular relaxation and hypertension in IL-6-infused pregnant rats. Hypertension. 2004;43:434-444.
40. Kusano K, Miyaura C, Inada M, Tamura T, Ito A, Nagase H, Kamoi K, Suda T. Regulation of matrix m etalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology. 1998;139:1338-1345.
41. Solís-Herruzo JA, Rippe R A, Schrum LW, de La Torre P, García I, Jeffrey JJ, Muñoz-Yagüe T, Brenner DA. Interleukin-6 increases rat metalloproteinase-13 gene expression through stimulation of activator protein 1 transcription factor i n cultured fibroblasts. J Biol Chem. 1999;274:30919-30926.