Leptin promotes the mobilization of vascular progenitor cells and neovascularization by NOX2-mediated activation of MMP9

Cardiovascular Research

Volumn 93, Issue 1, 2012, Pages 170-180

  Schroeter, Marco R ^a   Stein, Susanne ^a   Heida, Nana Maria ^a   Leifheit Nestler, Maren ^a   Cheng, I Fen ^a   Gogiraju, Rajinikanth ^a   Christiansen, Hans ^a   Maier, Lars S ^a   Shah, Ajay M ^b   Hasenfuss, Gerd ^a   Konstantinides, Stavros ^a,c   Schfer, Katrin ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

Author keywords

Angiogenesis; Foetal liver kinase 1; Leptin; NADPH oxidase; Progenitor cell mobilization

Indexed keywords

ATAXIN 1; CD31 ANTIGEN; GELATINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; BONE MARROW; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; FEMORAL ARTERY; LIMB ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL;

ANIMALS; BONE MARROW TRANSPLANTATION; ENZYME ACTIVATION; HEMATOPOIETIC STEM CELLS; HINDLIMB; ISCHEMIA; LEPTIN; MALE; MATRIX METALLOPROTEINASE 9; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; REACTIVE OXYGEN SPECIES; RECEPTORS, LEPTIN; RNA, MESSENGER; STEM CELL FACTOR;

EID: 84555177776     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr275     Document Type: Article

References (41)

1. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 2000;97:3422-3427. (Pubitemid 30183318)
2. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M et al. Ischemia-and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999;5:434-438. (Pubitemid 29180584)
3. Kong D, Melo LG, Gnecchi M, Zhang L, Mostoslavsky G, Liew CC et al. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation 2004;110:2039-2046. (Pubitemid 39331919)
4. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85:221-228. (Pubitemid 29377293)
5. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue [published erratum appears in Nature 1995;374:479]. Nature 1994;372:425-432. (Pubitemid 24365442)
6. Sierra-Honigmann MR, Nath AK, Murakami C, Garcia-Cardena G, Papapetropoulos A, Sessa WC et al. Biological action of leptin as an angiogenic factor. Science 1998;281:1683-1686. (Pubitemid 28435586)
7. Bouloumie A, Drexler HC, Lafontan M, Busse R. Leptin, the product of Ob gene, promotes angiogenesis. Circ Res 1998;83:1059-1066. (Pubitemid 28520935)
8. Suganami E, Takagi H, Ohashi H, Suzuma K, Suzuma I, Oh H et al. Leptin stimulates ischemia-induced retinal neovascularization: possible role of vascular endothelial growth factor expressed in retinal endothelial cells. Diabetes 2004;53:2443-2448. (Pubitemid 39145601)
9. Iversen PO, Drevon CA, Reseland JE. Prevention of leptin binding to its receptor suppresses rat leukemic cell growth by inhibiting angiogenesis. Blood 2002;100: 4123-4128. (Pubitemid 35402054)
10. Schiekofer S, Galasso G, Sato K, Kraus BJ, Walsh K. Impaired revascularization in a mouse model of type 2 diabetes is associated with dysregulation of a complex angiogenic-regulatory network. Arterioscler Thromb Vasc Biol 2005;25:1603-1609. (Pubitemid 41098928)
11. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008;28:1584-1595.
12. Heida NM, Leifheit-Nestler M, Schroeter MR, Müller JP, Cheng IF, Henkel S et al. Leptin enhances the potency of circulating angiogenic cells via src kinase and integrin alphaVbeta5: implications for angiogenesis in human obesity. Arterioscler Thromb Vasc Biol 2010;30:200-206.
13. Schroeter MR, Leifheit M, Sudholt P, Heida NM, Dellas C, Rohm I et al. Leptin enhances the recruitment of endothelial progenitor cells into neointimal lesions after vascular injury by promoting integrin-mediated adhesion. Circ Res 2008;103: 536-544.
14. Gainsford T, Willson TA, Metcalf D, Handman E, McFarlane C, Ng A et al. Leptin can induce proliferation, differentiation, and functional activation of hemopoietic cells. Proc Natl Acad Sci USA 1996;93:14564-14568. (Pubitemid 26419007)
15. Byrne JA, Grieve DJ, Bendall JK, Li JM, Gove C, Lambeth JD et al. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ Res 2003;93:802-805.
16. Konstantinides S, Schäfer K, Koschnick S, Loskutoff DJ. Leptin-dependent platelet aggregation and arterial thrombosis suggests a mechanism for atherothrombotic disease in obesity. J Clin Invest 2001;108:1533-1540. (Pubitemid 33091991)
17. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 2002;3:687-694. (Pubitemid 34752479)
18. Leifheit-Nestler M, Conrad G, Heida NM, Limbourg A, Limbourg FP, Seidler T et al. Overexpression of integrin beta 5 enhances the paracrine properties of circulating angiogenic cells via Src kinase-mediated activation of STAT3. Arterioscler Thromb Vasc Biol 2010;30:1398-1406.
19. Schröder K, Kohnen A, Aicher A, Liehn EA, Buchse T, Stein S et al. NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ Res 2009;105:537-544.
20. Heissig B, Hatto ri K, Dias S, Friedrich M, Ferris B, Hackett NR et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002;109:625-637. (Pubitemid 34628725)
21. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003;9:702-712. (Pubitemid 36749219)
22. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 2004;104:2084-2086. (Pubitemid 39297861)
23. Park HY, Kwon HM, Lim HJ, Hong BK, Lee JY, Park BE et al. Potential role of leptin in angiogenesis: leptin induces endothelial cell proliferation and expression of matrix metalloproteinases in vivo and in vitro. Exp Mol Med 2001;33:95-102. (Pubitemid 32655888)
24. Bouloumie A, Marumo T, Lafontan M, Busse R. Leptin induces oxidative stress in human endothelial cells. FASEB J 1999;13:1231-1238. (Pubitemid 29300368)
25. Jin F, Zhai Q, Qiu L, Meng H, Zou D, Wang Y et al. Degradation of BM SDF-1 by MMP-9: the role in G-CSF-induced hematopoietic stem/progenitor cell mobilization. Bone Marrow Transplant 2008;42:581-588.
26. Jose VJ, Mariappan P, George PV, Selvakumar, Selvakumar D. Serum leptin levels in acute myocardial infarction. Indian Heart J 2005;57:39-43. (Pubitemid 40562493)
27. Meisel SR, Ellis M, Pariente C, Pauzner H, Liebowitz M, David D et al. Serum leptin levels increase following acute myocardial infarction. Cardiology 2001;95:206-211. (Pubitemid 34701480)
28. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001;7:430-436. (Pubitemid 32298545)
29. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E et al. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 2000;86:1198-1202. (Pubitemid 30436658)
30. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 2003;102:1340-1346. (Pubitemid 36988041)
31. Schroeter MR, Humboldt T, Schäfer K, Konstantinides S. Rosuvastatin reduces atherosclerotic lesions and promotes progenitor cell mobilisation and recruitment in apolipoprotein E knockout mice. Atherosclerosis 2009;205:63-73.
32. Huang PH, Chen YH, Wang CH, Chen JS, Tsai HY, Lin FY et al. Matrix metalloproteinase-9 is essential for ischemia-induced neovascularization by modulating bone marrow-derived endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2009;29:1179-1184.
33. Chabot B, Stephenson DA, Chapman VM, Besmer P, Bernstein A. The protooncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 1988;335:88-89.
34. Iwakura A, Shastry S, Luedemann C, Hamada H, Kawamoto A, Kishore R et al. Estradiol enhances recovery after myocardial infarction by augmenting incorporation of bone marrow-derived endothelial progenitor cells into sites of ischemia-induced neovascularization via endothelial nitric oxide synthase-mediated activation of matrix metalloproteinase-9. Circulation 2006;113:1605-1614. (Pubitemid 43739420)
35. Kim SY, Lee JG, Cho WS, Cho KH, Sakong J, Kim JR et al. Role of NADPH oxidase-2 in lipopolysaccharide-induced matrix metalloproteinase expression and cell migration. Immunol Cell Biol 2010;88:197-204.
36. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245-313. (Pubitemid 46209993)
37. Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S, Waltenberger J et al. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem 2002;277:3101-3108. (Pubitemid 34953170)
38. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M et al. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factorinduced signaling and angiogenesis. Circ Res 2002;91:1160-1167. (Pubitemid 36076365)
39. Urao N, Inomata H, Razvi M, Kim HW, Wary K, McKinney R et al. 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.
40. Li L, Mamputu JC, Wiernsperger N, Renier G. Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin. Diabetes 2005;54:2227-2234. (Pubitemid 40911288)
41. Yamagishi SI, Edelstein D, Du XL, Kaneda Y, Guzman M, Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase A. J Biol Chem 2001;276:25096-25100.