PDGF-Induced migration of vascular smooth muscle cells is inhibited by heme oxygenase-1 Via VEGFR2 upregulation and subsequent assembly of inactive VEGFR2/PDGFRβ heterodimers

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 5, 2012, Pages 1289-1298

  Cheng, Caroline ^a   Haasdijk, Remco A ^a   Tempel, Dennie ^a   Den Dekker, Wijnand K ^a   Chrifi, Ihsan ^a   Blonden, Lau A J ^a   Van De Kamp, Esther H M ^a   De Boer, M ^a   Bürgisser, Petra E ^a   Noorderloos, Annemarie ^a   Rens, Joost A P ^a   Ten Hagen, Timo L M ^a   Duckers, Henricus J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Heme oxygenase; Migration; PDGF; Vascular smooth muscle cell

Indexed keywords

ADENOVIRUS VECTOR; COMPLEMENTARY DNA; FOCAL ADHESION KINASE; HEME OXYGENASE 1; HETERODIMER; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMALL INTERFERING RNA; SYNAPTOPHYSIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA BLOOD VESSEL; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

CELL MOVEMENT; CELL PROLIFERATION; HEME OXYGENASE-1; HUMANS; MUSCLE, SMOOTH, VASCULAR; PLATELET-DERIVED GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84860217635     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.245530     Document Type: Article

References (25)

1. Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation. 2008;117:231-241.
2. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol. 50:323-354.
3. Cheng C, Noorderloos M, van Deel ED, Tempel D, den Dekker W, Wagtmans K, Duncker DJ, Soares MP, Laman JD, Duckers HJ. Dendritic cell function in transplantation arteriosclerosis is regulated by heme oxygenase 1. Circ Res. 2010;106:1656-1666.
4. Larsen K, Cheng C, Duckers HJ. Regulation of vulnerable plaque development by the heme oxygenase/carbon monoxide system. Trends Cardiovasc Med. 20:58-65.
5. Deshane J, Chen S, Caballero S, Grochot-Przeczek A, Was H, Li Calzi S, Lach R, Hock TD, Chen B, Hill-Kapturczak N, Siegal GP, Dulak J, Jozkowicz A, Grant MB, Agarwal A. Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J Exp Med. 2007;204:605-618. (Pubitemid 46457083)
6. Morsi WG, Shaker OG, Ismail EF, Ahmed HH, El-Serafi TI, Maklady FA, Abdel-Aziz MT, El-Asmar MF, Atta HM. HO-1 and VGEF gene expression in human arteries with advanced atherosclerosis. Clin Biochem. 2006;39:1057-1062. (Pubitemid 44737476)
7. Yet SF, Layne MD, Liu X, Chen YH, Ith B, Sibinga NE, Perrella MA. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003;17:1759-1761.
8. Ishikawa K, Sugawara D, Goto J, Watanabe Y, Kawamura K, Shiomi M, Itabe H, Maruyama Y. Heme oxygenase-1 inhibits atherogenesis in Watanabe heritable hyperlipidemic rabbits. Circulation. 2001;104:1831-1836. (Pubitemid 32963350)
9. Cheng C, Noordeloos AM, Jeney V, Soares MP, Moll F, Pasterkamp G, Serruys PW, Duckers HJ. Heme oxygenase 1 determines atherosclerotic lesion progression into a vulnerable plaque. Circulation. 2009;119:3017-3027.
10. Nakao A, Murase N, Ho C, Toyokawa H, Billiar TR, Kanno S. Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation. 2005;112:587-591. (Pubitemid 41060800)
11. Duckers HJ, Boehm M, True AL, Yet SF, San H, Park JL, Clinton Webb R, Lee ME, Nabel GJ, Nabel EG. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med. 2001;7:693-698. (Pubitemid 32588025)
12. Cheng C, Tempel D, Oostlander A, Helderman F, Gijsen F, Wentzel J, van Haperen R, Haitsma DB, Serruys PW, van der Steen AF, de Crom R, Krams R. Rapamycin modulates the eNOS vs shear stress relationship. Cardiovasc Res. 2008;78:123-129. (Pubitemid 351430952)
13. Palazzo AF, Joseph HL, Chen YJ, Dujardin DL, Alberts AS, Pfister KK, Vallee RB, Gundersen GG. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol. 2001;11:1536-1541. (Pubitemid 32931017)
14. Li W, Tanaka K, Morioka K, Uesaka T, Yamada N, Takamori A, Handa M, Tanabe S, Ihaya A. Thymidine phosphorylase gene transfer inhibits vascular smooth muscle cell proliferation by upregulating heme oxygenase-1 and p27KIP1. Arterioscler Thromb Vasc Biol. 2005;25:1370-1375. (Pubitemid 40923354)
15. Rodriguez AI, Gangopadhyay A, Kelley EE, Pagano PJ, Zuckerbraun BS, Bauer PM. HO-1 and CO decrease platelet-derived growth factor-induced vascular smooth muscle cell migration via inhibition of Nox1. Arterioscler Thromb Vasc Biol.30:98-104.
16. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R, Dulak J. Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal. 2003;5:155-162. (Pubitemid 36457591)
17. Dorrell MI, Aguilar E, Friedlander M. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci. 2002;43:3500-3510. (Pubitemid 35334359)
18. Greenberg JI, Shields DJ, Barillas SG, Acevedo LM, Murphy E, Huang J, Scheppke L, Stockmann C, Johnson RS, Angle N, Cheresh DA. A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature. 2008;456:809-813.
19. Dulak J, Jozkowicz A. Nitric oxide and angiogenic activity of endothelial cells: direct or VEGF-dependent effect? Cardiovasc Res. 2002;56:487-488. (Pubitemid 35351571)
20. Dulak J, Jozkowicz A, Foresti R, Kasza A, Frick M, Huk I, Green CJ, Pachinger O, Weidinger F, Motterlini R. Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal. 2002;4:229-240. (Pubitemid 34517174)
21. Morita T, Kourembanas S. Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J Clin Invest. 1995;96:2676-2682.
22. Vitali SH, Mitsialis SA, Liang OD, Liu X, Fernandez-Gonzalez A, Christou H, Wu X, McGowan FX, Kourembanas S. Divergent cardiopulmonary actions of heme oxygenase enzymatic products in chronic hypoxia. PLoS One. 2009;4:e5978.
23. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol. 2000;2:249-256.
24. Rosenfeldt HM, Hobson JP, Maceyka M, Olivera A, Nava VE, Milstien S, Spiegel S. EDG-1 links the PDGF receptor to Src and focal adhesion kinase activation leading to lamellipodia formation and cell migration. FASEB J. 2001;15:2649-2659. (Pubitemid 33131091)
25. Togane Y, Morita T, Suematsu M, Ishimura Y, Yamazaki JI, Katayama S. Protective roles of endogenous carbon monoxide in neointimal development elicited by arterial injury. Am J Physiol Heart Circ Physiol. 2000;278:H623-H632. (Pubitemid 30131264)