Novel role of reactive oxygen species-activated trp melastatin channel-2 in mediating angiogenesis and postischemic neovascularization

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 4, 2015, Pages 877-887

  Mittal, Manish ^a   Urao, Norifumi ^a   Hecquet, Claudie M ^a   Zhang, Min ^a   Sudhahar, Varadarajan ^a   Gao, Xiao Pei ^a   Komarova, Yulia ^a   Ushio Fukai, Masuko ^a   Malik, Asrar B ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

angiogenesis effects; cadherin 5; endothelial cells; hindlimb ischemia; TRPM2 protein, mouse

Indexed keywords

CALCIUM; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SODIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL M3; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; CADHERIN; CYBB PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; PROTEIN KINASE P60; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM2 PROTEIN, HUMAN; TRPM2 PROTEIN, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL JUNCTION; CELL STRESS; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; ISCHEMIC NEOVASCULARIZATION; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; ONCOGENE SRC; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; CELL CULTURE; CELL MOTION; DEFICIENCY; DISEASE MODEL; GENETIC TRANSFECTION; GENETICS; HINDLIMB; IMPEDANCE; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; MUTATION; PATHOPHYSIOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SKELETAL MUSCLE; TIME FACTOR; VASCULARIZATION;

ANIMALS; ANTIGENS, CD; CADHERINS; CALCIUM; CALCIUM SIGNALING; CELL MOVEMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; HINDLIMB; HUMANS; ISCHEMIA; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUTATION; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS PP60(C-SRC); REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TRPM CATION CHANNELS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84927666881     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304802     Document Type: Article

References (49)

1. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. 2011;146:873-887. doi: 10.1016/j.cell.2011.08.039.
2. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6:389-395. doi: 10.1038/74651.
3. Limbourg A, Korff T, Napp LC, Schaper W, Drexler H, Limbourg FP. Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat Protoc. 2009;4:1737-1746. doi: 10.1038/nprot.2009.185.
4. Urao N, Sudhahar V, Kim SJ, Chen GF, McKinney RD, Kojda G, Fukai T, Ushio-Fukai M. Critical role of endothelial hydrogen peroxide in postischemic neovascularization. PLoS One. 2013;8:e57618. doi: 10.1371/ journal.pone.0057618.
5. Urao N, Razvi M, Oshikawa J, McKinney RD, Chavda R, Bahou WF, Fukai T, Ushio-Fukai M. IQGAP1 is involved in post-ischemic neovascularization by regulating angiogenesis and macrophage infiltration. PLoS One. 2010;5:e13440. doi: 10.1371/journal.pone.0013440.
6. Ferrara N. Vascular endothelial growth factor. Arterioscler Thromb Vasc Biol. 2009;29:789-791. doi: 10.1161/ATVBAHA.108.179663.
7. Bravi L, Dejana E, Lampugnani MG. VE-cadherin at a glance. Cell Tissue Res. 2014;355:515-522. doi: 10.1007/s00441-014-1843-7.
8. Bentley K, Franco CA, Philippides A, Blanco R, Dierkes M, Gebala V, Stanchi F, Jones M, Aspalter IM, Cagna G, Weström S, Claesson-Welsh L, Vestweber D, Gerhardt H. The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat Cell Biol. 2014;16:309-321. doi: 10.1038/ncb2926.
9. Lambeng N, Wallez Y, Rampon C, Cand F, Christé G, Gulino-Debrac D, Vilgrain I, Huber P. Vascular endothelial-cadherin tyrosine phosphorylation in angiogenic and quiescent adult tissues. Circ Res. 2005;96:384-391. doi: 10.1161/01.RES.0000156652.99586.9f.
10. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111(Pt 13):1853-1865.
11. Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120-and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem. 2005;280:31906-31912. doi: 10.1074/jbc.M505568200.
12. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem. 2009;284:25602-25611. doi: 10.1074/ jbc.M109.009894.
13. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation. 2005;111:2347-2355. doi: 10.1161/01.CIR.0000164261.62586.14.
14. Urao N, Inomata H, Razvi M, Kim HW, Wary K, McKinney R, Fukai T, Ushio-Fukai M. Role of nox2-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia. Circ Res. 2008;103:212-220. doi: 10.1161/ CIRCRESAHA.108.176230.
15. Li J, Cubbon RM, Wilson LA, et al. Orai1 and CRAC channel dependence of VEGF-activated Ca2+ entry and endothelial tube formation. Circ Res. 2011;108:1190-1198. doi: 10.1161/CIRCRESAHA.111.243352.
16. Yu PC, Gu SY, Bu JW, Du JL. TRPC1 is essential for in vivo angiogenesis in zebrafish. Circ Res. 2010;106:1221-1232. doi: 10.1161/ CIRCRESAHA.109.207670.
17. Hecquet CM, Ahmmed GU, Vogel SM, Malik AB. Role of TRPM2 channel in mediating H2O2-induced Ca2+ entry and endothelial hyperpermeability. Circ Res. 2008;102:347-355. doi: 10.1161/CIRCRESAHA.107.160176.
18. Takahashi N, Kozai D, Kobayashi R, Ebert M, Mori Y. Roles of TRPM2 in oxidative stress. Cell Calcium. 2011;50:279-287. doi: 10.1016/j. ceca.2011.04.006.
19. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature. 2001;411:595-599. doi: 10.1038/35079100.
20. Shah A, Xia L, Goldberg H, Lee KW, Quaggin SE, Fantus IG. Thioredoxininteracting protein mediates high glucose-induced reactive oxygen species generation by mitochondria and the NADPH oxidase, Nox4, in mesangial cells. J Biol Chem. 2013;288:6835-6848. doi: 10.1074/jbc.M112.419101.
21. Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, Furuichi K. Immunocyte Ca2+ influx system mediated by LTRPC2. Science. 2001;293:1327-1330. doi: 10.1126/science.1062473.
22. Mei ZZ, Mao HJ, Jiang LH. Conserved cysteine residues in the pore region are obligatory for human TRPM2 channel function. Am J Physiol Cell Physiol. 2006;291:C1022-C1028. doi: 10.1152/ajpcell.00606.2005.
23. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell. 1999;4:915-924.
24. Söderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006;3:995-1000. doi: 10.1038/nmeth947.
25. Harvey R, Hehir KM, Smith AE, Cheng SH. pp60c-src variants containing lesions that affect phosphorylation at tyrosines 416 and 527. Mol Cell Biol. 1989;9:3647-3656.
26. Nanes BA, Chiasson-MacKenzie C, Lowery AM, Ishiyama N, Faundez V, Ikura M, Vincent PA, Kowalczyk AP. p120-catenin binding masks an endocytic signal conserved in classical cadherins. J Cell Biol. 2012;199:365-380. doi: 10.1083/jcb.201205029.
27. Keese CR, Wegener J, Walker SR, Giaever I. Electrical wound-healing assay for cells in vitro. Proc Natl Acad Sci USA. 2004;101:1554-1559. doi: 10.1073/pnas.0307588100.
28. Baker M, Robinson SD, Lechertier T, Barber PR, Tavora B, D'Amico G, Jones DT, Vojnovic B, Hodivala-Dilke K. Use of the mouse aortic ring assay to study angiogenesis. Nat Protoc. 2012;7:89-104. doi: 10.1038/nprot.2011.435.
29. Deng Y, Larrivée B, Zhuang ZW, Atri D, Moraes F, Prahst C, Eichmann A, Simons M. Endothelial RAF1/ERK activation regulates arterial morphogenesis. Blood. 2013;121:3988-96, S1. doi: 10.1182/ blood-2012-12-474601.
30. Semenza GL. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med. 2003;54:17-28. doi: 10.1146/annurev.med.54.101601.152418.
31. Faber JE, Chilian WM, Deindl E, van Royen N, Simons M. A brief etymology of the collateral circulation. Arterioscler Thromb Vasc Biol. 2014;34:1854-1859. doi: 10.1161/ATVBAHA.114.303929.
32. Poteser M, Graziani A, Rosker C, Eder P, Derler I, Kahr H, Zhu MX, Romanin C, Groschner K. TRPC3 and TRPC4 associate to form a redoxsensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J Biol Chem. 2006;281:13588-13595. doi: 10.1074/jbc.M512205200.
33. Balzer M, Lintschinger B, Groschner K. Evidence for a role of Trp proteins in the oxidative stress-induced membrane conductances of porcine aortic endothelial cells. Cardiovasc Res. 1999;42:543-549.
34. Gong H, Gao X, Feng S, Siddiqui MR, Garcia A, Bonini MG, Komarova Y, Vogel SM, Mehta D, Malik AB. Evidence of a common mechanism of disassembly of adherens junctions through Gα13 targeting of VE-cadherin. J Exp Med. 2014;211:579-591. doi: 10.1084/jem.20131190.
35. Ha CH, Bennett AM, Jin ZG. A novel role of vascular endothelial cadherin in modulating c-Src activation and downstream signaling of vascular endothelial growth factor. J Biol Chem. 2008;283:7261-7270. doi: 10.1074/jbc.M702881200.
36. Hatanaka K, Simons M, Murakami M. Phosphorylation of VE-cadherin controls endothelial phenotypes via p120-catenin coupling and Rac1 activation. Am J Physiol Heart Circ Physiol. 2011;300:H162-H172. doi: 10.1152/ajpheart.00650.2010.
37. Haidari M, Zhang W, Caivano A, Chen Z, Ganjehei L, Mortazavi A, Stroud C, Woodside DG, Willerson JT, Dixon RA. Integrin α2β1 mediates tyrosine phosphorylation of vascular endothelial cadherin induced by invasive breast cancer cells. J Biol Chem. 2012;287:32981-32992. doi: 10.1074/jbc.M112.395905.
38. Nakamura Y, Patrushev N, Inomata H, Mehta D, Urao N, Kim HW, Razvi M, Kini V, Mahadev K, Goldstein BJ, McKinney R, Fukai T, Ushio-Fukai M. Role of protein tyrosine phosphatase 1B in vascular endothelial growth factor signaling and cell-cell adhesions in endothelial cells. Circ Res. 2008;102:1182-1191. doi: 10.1161/CIRCRESAHA.107.167080.
39. Lanahan AA, Lech D, Dubrac A, Zhang J, Zhuang ZW, Eichmann A, Simons M. PTP1b is a physiologic regulator of vascular endothelial growth factor signaling in endothelial cells. Circulation. 2014;130:902-909. doi: 10.1161/CIRCULATIONAHA.114.009683.
40. Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell. 2002;9:387-399.
41. Lee M, Choy WC, Abid MR. Direct sensing of endothelial oxidants by vascular endothelial growth factor receptor-2 and c-Src. PLoS One. 2011;6:e28454. doi: 10.1371/journal.pone.0028454.
42. Tiozzo R, Monti D, Straface E, Capri M, Croce MA, Rainaldi G, Franceschi C, Malorni W. Antiproliferative activity of 3-aminobenzamide in A431 carcinoma cells is associated with a target effect on cytoskeleton. Biochem Biophys Res Commun. 1996;225:826-832. doi: 10.1006/ bbrc.1996.1258.
43. Kim SY, Moon KA, Jo HY, Jeong S, Seon SH, Jung E, Cho YS, Chun E, Lee KY. Anti-inflammatory effects of apocynin, an inhibitor of NADPH oxidase, in airway inflammation. Immunol Cell Biol. 2012;90:441-448. doi: 10.1038/icb.2011.60.
44. Bogeski I, Bozem M, Sternfeld L, Hofer HW, Schulz I. Inhibition of protein tyrosine phosphatase 1B by reactive oxygen species leads to maintenance of Ca2+ influx following store depletion in HEK 293 cells. Cell Calcium. 2006;40:1-10. doi: 10.1016/j.ceca.2006.03.003.
45. Sternfeld L, Krause E, Schmid A, Anderie I, Latas A, Al-Shaldi H, Köhl A, Evers K, Hofer HW, Schulz I. Tyrosine phosphatase PTP1B interacts with TRPV6 in vivo and plays a role in TRPV6-mediated calcium influx in HEK293 cells. Cell Signal. 2005;17:951-960. doi: 10.1016/j. cellsig.2004.11.012.
46. Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, Keaney JF Jr. NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation. 2011;124:731-740. doi: 10.1161/CIRCULATIONAHA.111.030775.
47. Scholz D, Ziegelhoeffer T, Helisch A, Wagner S, Friedrich C, Podzuweit T, Schaper W. Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol. 2002;34:775-787.
48. Di A, Gao XP, Qian F, Kawamura T, Han J, Hecquet C, Ye RD, Vogel SM, Malik AB. The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat Immunol. 2012;13:29-34. doi: 10.1038/ni.2171.
49. Hecquet CM, Zhang M, Mittal M, Vogel SM, Di A, Gao X, Bonini MG, Malik AB. Cooperative interaction of trp melastatin channel TRPM2 with its splice variant TRPM2-S is essential for endothelial cell apoptosis. Circ Res. 2014;114:469-479.