Tissue Kallikrein is essential for invasive capacity of circulating proangiogenic cells

Circulation Research

Volumn 108, Issue 3, 2011, Pages 284-293

  Spinetti, Gaia ^a   Fortunato, Orazio ^a   Cordella, Daniela ^a   Portararo, Paola ^a   Kränkel, Nicolle ^b   Katare, Rajesh ^b   Sala Newby, Graciela B ^b   Richer, Christine ^c   Vincent, Marie Pascale ^c   Alhenc Gelas, Francois ^c   Tonolo, Giancarlo ^d   Cherchi, Sara ^d   Emanueli, Costanza ^b   Madeddu, Paolo ^b  

^a IRCCS MULTIMEDICA   (Italy)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c INSERM   (France)

^d OC San Giovanni di Dio ^*  (Italy)

Author keywords

angiogenesis; cell invasion; circulating proangiogenic cells; kallikrein kinin system

Indexed keywords

GELATINASE A; INDUCIBLE NITRIC OXIDE SYNTHASE; KININ; MESSENGER RNA; SMALL INTERFERING RNA; TISSUE KALLIKREIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DIABETIC PATIENT; ENZYME ACTIVITY; GENE SILENCING; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; MONONUCLEAR CELL; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PERIPHERAL ISCHEMIA; PRIORITY JOURNAL; PROANGIOGENIC CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM;

ADULT; AGED; ANIMALS; CASE-CONTROL STUDIES; CELL MOVEMENT; DIABETES MELLITUS, TYPE 2; DOWN-REGULATION; FEMALE; HINDLIMB; HUMANS; ISCHEMIA; KALLIKREINS; KININS; LEUKOCYTES, MONONUCLEAR; MALE; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE; RECEPTOR, BRADYKININ B2; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 79751535384     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.236786     Document Type: Article

References (36)

1. van Hinsbergh VW, Engelse MA, Quax PH. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol. 2006; 26:716-728. (Pubitemid 43732143)
2. Urbich C, Dernbach E, Rossig L, Zeiher AM, Dimmeler S. High glucose reduces cathepsin L activity and impairs invasion of circulating progenitor cells. J Mol Cell Cardiol. 2008;45:429-436.
3. Madeddu P, Emanueli C, El-Dahr S. Mechanisms of disease: the tissue kallikrein-kinin system in hypertension and vascular remodeling. Nat Clin Pract Nephrol. 2007;3:208-221. (Pubitemid 46496868)
4. Stone OA, Richer C, Emanueli C, van Weel V, Quax PH, Katare R, Kraenkel N, Campagnolo P, Barcelos LS, Siragusa M, Sala-Newby GB, Baldessari D, Mione M, Vincent MP, Benest AV, Al Haj Zen A, Gonzalez J, Bates DO, Alhenc-Gelas F, Madeddu P. Critical role of tissue kallikrein in vessel formation and maturation: implications for therapeutic revascularization. Arterioscler Thromb Vasc Biol. 2009;29:657-664.
5. Hayashi I, Amano H, Yoshida S, Kamata K, Kamata M, Inukai M, Fujita T, Kumagai Y, Furudate S, Majima M. Suppressed angiogenesis in kininogen- deficiencies. Lab Invest. 2002;82:871-880. (Pubitemid 34761662)
6. Emanueli C, Bonaria Salis M, Stacca T, Pintus G, Kirchmair R, Isner JM, Pinna A, Gaspa L, Regoli D, Cayla C, Pesquero JB, Bader M, Madeddu P. Targeting kinin B(1) receptor for therapeutic neovascularization. Circulation. 2002;105:360-366. (Pubitemid 34106186)
7. Silvestre JS, Bergaya S, Tamarat R, Duriez M, Boulanger CM, Levy BI. Proangiogenic effect of angiotensin-converting enzyme inhibition is mediated by the bradykinin B(2) receptor pathway. Circ Res. 2001;89: 678-683. (Pubitemid 34627067)
8. Westermann D, Walther T, Savvatis K, Escher F, Sobirey M, Riad A, Bader M, Schultheiss HP, Tschope C. Gene deletion of the kinin receptor B1 attenuates cardiac inflammation and fibrosis during the development of experimental diabetic cardiomyopathy. Diabetes. 2009;58:1373-1381.
9. Emanueli C, Salis MB, Van Linthout S, Meloni M, Desortes E, Silvestre JS, Clergue M, Figueroa CD, Gadau S, Condorelli G, Madeddu P. Akt/protein kinase B and endothelial nitric oxide synthase mediate muscular neovascularization induced by tissue kallikrein gene transfer. Circulation. 2004;110:1638-1644. (Pubitemid 39297987)
10. Emanueli C, Zacheo A, Minasi A, Chao J, Chao L, Salis MB, Stacca T, Straino S, Capogrossi MC, Madeddu P. Adenovirus-mediated human tissue kallikrein gene delivery induces angiogenesis in normoperfused skeletal muscle. Arterioscler Thromb Vasc Biol. 2000;20:2379-2385.
11. Chao J, Yin H, Gao L, Hagiwara M, Shen B, Yang Z-R, Chao L. Tissue kallikrein elicits cardioprotection by direct kinin B2 receptor activation independent of kinin formation. Hypertension. 2008;52:715-720.
12. Hecquet C, Tan F, Marcic BM, Erdos EG. Human bradykinin B(2) receptor is activated by kallikrein and other serine proteases. Mol Pharmacol. 2000;58:828-836.
13. Krankel N, Katare RG, Siragusa M, Barcelos LS, Campagnolo P, Mangialardi G, Fortunato O, Spinetti G, Tran N, Zacharowski K, Wojakowski W, Mroz I, Herman A, Manning Fox JE, MacDonald PE, Schanstra JP, Bascands JL, Ascione R, Angelini G, Emanueli C, Madeddu P. Role of kinin B2 receptor signaling in the recruitment of circulating progenitor cells with neovascularization potential. Circ Res. 2008;103:1335-1343.
14. Madeddu P, Kraenkel N, Barcelos LS, Siragusa M, Campagnolo P, Oikawa A, Caporali A, Herman A, Azzolino O, Barberis L, Perino A, Damilano F, Emanueli C, Hirsch E. Phosphoinositide 3-kinase gamma gene knockout impairs postischemic neovascularization and endothe-lial progenitor cell functions. Arterioscler Thromb Vasc Biol. 2008; 28:68-76.
15. Siragusa M, Katare R, Meloni M, Damilano F, Hirsch E, Emanueli C, Madeddu P. Involvement of phosphoinositide 3-kinase gamma in angio-genesis and healing of experimental myocardial infarction in mice. Circ Res. 106:757-768.
16. Meneton P, Bloch-Faure M, Hagege AA, Ruetten H, Huang W, Bergaya S, Ceiler D, Gehring D, Martins I, Salmon G, Boulanger CM, Nussberger J, Crozatier B, Gasc JM, Heudes D, Bruneval P, Doetschman T, Menard J, Alhenc-Gelas F. Cardiovascular abnormalities with normal blood pressure in tissue kallikrein-deficient mice. Proc Natl Acad Sci USA. 2001;98:2634-2639. (Pubitemid 32209534)
17. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343-353. (Pubitemid 39100452)
18. Spinetti G, Wang M, Monticone R, Zhang J, Zhao D, Lakatta EG. Rat aortic MCP-1 and its receptor CCR2 increase with age and alter vascular smooth muscle cell function. Arterioscler Thromb Vasc Biol. 2004;24: 1397-1402. (Pubitemid 39050431)
19. George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum Gene Ther. 1998;9:867-877. (Pubitemid 28197373)
20. Cheng XW, Kuzuya M, Nakamura K, Maeda K, Tsuzuki M, Kim W, Sasaki T, Liu Z, Inoue N, Kondo T, Jin H, Numaguchi Y, Okumura K, Yokota M, Iguchi A, Murohara T. Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metallopro-teinase 2-deficient mice. Circ Res. 2007;100:904-913. (Pubitemid 46555696)
21. Moncada S, Higgs A, Furchgott R. International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev. 1997;49: 137-142. (Pubitemid 27291031)
22. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN, Darley-Usmar VM, Kerby JD, Lang JD Jr, Kraus D, Ho C, Gladwin MT, Patel RP. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood. 2006;107:566-574. (Pubitemid 43076380)
23. Fadini GP, Sartore S, Albiero M, Baesso I, Murphy E, Menegolo M, Grego F, Vigili de Kreutzenberg S, Tiengo A, Agostini C, Avogaro A. Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler Thromb Vasc Biol. 2006; 26:2140-2146. (Pubitemid 44253800)
24. Loomans CJM, de Koning EJP, Staal FJT, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld A-J. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes. 2004;53: 195-199. (Pubitemid 38044715)
25. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786. (Pubitemid 35396976)
26. Krankel N, Adams V, Linke A, Gielen S, Erbs S, Lenk K, Schuler G, Hambrecht R. Hyperglycemia reduces survival and impairs function of circulating blood-derived progenitor cells. Arterioscler Thromb Vasc Biol. 2005;25:698-703. (Pubitemid 40463856)
27. Losordo DW, Schatz RA, White CJ, Udelson JE, Veereshwarayya V, Durgin M, Poh KK, Weinstein R, Kearney M, Chaudhry M, Burg A, Eaton L, Heyd L, Thorne T, Shturman L, Hoffmeister P, Story K, Zak V, Dowling D, Traverse JH, Olson RE, Flanagan J, Sodano D, Murayama T, Kawamoto A, Kusano KF, Wollins J, Welt F, Shah P, Soukas P, Asahara T, Henry TD. Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation. 2007;115:3165-3172. (Pubitemid 47018140)
28. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047. (Pubitemid 350179569)
29. Krankel N, Armstrong SP, McArdle CA, Dayan C, Madeddu P. Distinct kinin-induced functions are altered in circulating cells of young type 1 diabetic patients. PloS One. 2010;5:e11146.
30. Chavakis E, Carmona G, Urbich C, Gottig S, Henschler R, Penninger JM, Zeiher AM, Chavakis T, Dimmeler S. Phosphatidylinositol-3-kinase-gamma is integral to homing functions of progenitor cells. Circ Res. 2008;102:942-949. (Pubitemid 351591547)
31. Wang M, Lakatta EG. Altered regulation of matrix metalloproteinase-2 in aortic remodeling during aging. Hypertension. 2002;39:865-873. (Pubitemid 34437541)
32. Azizi M, Boutouyrie P, Bissery A, Agharazii M, Verbeke F, Stern N, Bura-Riviere A, Laurent S, Alhenc-Gelas F, Jeunemaitre X. Arterial and renal consequences of partial genetic deficiency in tissue kallikrein activity in humans. J Clin Invest. 2005;115:780-787. (Pubitemid 40322255)
33. Ii M, Takenaka H, Asai J, Ibusuki K, Mizukami Y, Maruyama K, Yoon YS, Wecker A, Luedemann C, Eaton E, Silver M, Thorne T, Losordo DW. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res. 2006;98:697-704.
34. Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes. 1999;48:1-9. (Pubitemid 29019345)
35. Couzin J. MicroRNAs make big impression in disease after disease. Science. 2008;319:1782-1784. (Pubitemid 351451552)
36. Chow TF, Crow M, Earle T, El-Said H, Diamandis EP, Yousef GM. Kallikreins as microRNA targets: an in silico and experimental-based analysis. Biol Chem. 2008;389:731-738. (Pubitemid 352009404)