Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity

Circulation

Volumn 111, Issue 9, 2005, Pages 1114-1120

  Ii, Masaaki ^a   Nishimura, Hiromi ^b   Iwakura, Atsushi ^a   Wecker, Andrea ^a   Eaton, Elizabeth ^a   Asahara, Takayuki ^b   Losordo, Douglas W ^a,c  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

^c ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

Blood cells; Ischemia; Myocardial infarction; Nitric oxide synthase

Indexed keywords

CYTOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CELL ACTIVITY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HEART INFARCTION PREVENTION; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; BLOOD CELLS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CAPILLARIES; CELL HYPOXIA; CELL MOVEMENT; CELLS, CULTURED; CORONARY CIRCULATION; CYTOKINES; ENDOTHELIAL CELLS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RADIATION CHIMERA; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 14944371450     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000157144.24888.7E     Document Type: Article

References (42)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986; 74:1124-1136.
2. Bugge E, Ytrehus K. Ischaemic preconditioning is protein kinase C dependent but not through stimulation of alpha adrenergic or adenosine receptors in the isolated rat heart. Cardiovasc Res. 1995;29:401-406.
3. Ottani F, Galvani M, Ferrini D, Sorbello F, Limonetti P, Pantoli D, Rusticali F. Prodromal angina limits infarct size: a role for ischemic preconditioning. Circulation. 1995;91:291-297.
4. Kitakaze M, Node K, Minamino T, Komamura K, Funaya H, Shinozaki Y, Chujo M, Mori H, Inoue M, Hori M, Kamada T. Role of activation of protein kinase C in the infarct size-limiting effect of ischemic preconditioning through activation of ecto-5′-nucleotidase. Circulation. 1996;93:781-791.
5. Miller DL, Van Winkle DM. Ischemic preconditioning limits infarct size following regional ischemia-reperfusion in in situ mouse hearts. Cardiovasc Res. 1999;42:680-684.
6. Noda T, Minatoguchi S, Fujii K, Hori M, Ito T, Kanmatsuse K, Matsuzaki M, Miura T, Nonogi H, Tada M, Tanaka M, Fujiwara H. Evidence for the delayed effect in human ischemic preconditioning: prospective multicenter study for preconditioning in acute myocardial infarction. J Am Coll Cardiol. 1999;34:1966-1974.
7. Guo Y, Wu WJ, Qiu Y, Tang XL, Yang Z, Bolli R. Demonstration of an early and a late phase of ischemic preconditioning in mice. Am J Physiol. 1998;275:H1375-H1387.
8. Bolli R. The late phase of preconditioning. Circ Res. 2000;87:972-983.
9. Dawn B, Takano H, Tang XL, Kodani E, Banerjee S, Rezazadeh A, Qiu Y, Bolli R. Role of Src protein tyrosine kinases in late preconditioning against myocardial infarction. Am J Physiol Heart Circ Physiol. 2002;283:H549-H556.
10. Laude K, Favre J, Thuillez C, Richard V. NO produced by endothelial NO synthase is a mediator of delayed preconditioning-induced endothelial protection. Am J Physiol Heart Circ Physiol. 2003;284:H2053-H2060.
11. Banai S, Shweiki D, Pinson A, Chandra M, Lazarovici G, Keshet E. Upregulation of vascular endothelial growth factor expression induced by myocardial ischemia: implications for coronary angiogenesis. Cardiovasc Res. 1994;28:1176-1179.
12. Hashimoto E, Ogita T, Nakaoka T, Matsuoka R, Takao A, Kira Y. Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart. Am J Physiol. 1994;267:H1948-H1954.
13. Kawata H, Yoshida K, Kawamoto A, Kurioka H, Takase E, Sasaki Y, Hatanaka K, Kobayashi M, Ueyama T, Hashimoto T, Dohi K. Ischemic preconditioning upregulates vascular endothelial growth factor mRNA expression and neovascularization via nuclear translocation of protein kinase C epsilon in the rat ischemic myocardium. Circ Res. 2001;88:696-704.
14. Miura T, Kawamura S, Goto M, Sakamoto J, Tsuchida A, Matsuzaki M, Shimamoto K. Effect of protein kinase C inhibitors on cardioprotection by ischemic preconditioning depends on the number of preconditioning episodes. Cardiovasc Res. 1998;37:700-709.
15. Qiu Y, Ping P, Tang XL, Manchikalapudi S, Rizvi A, Zhang J, Takano H, Wu WJ, Teschner S, Bolli R. Direct evidence that protein kinase C plays an essential role in the development of late preconditioning against myocardial stunning in conscious rabbits and that epsilon is the isoform involved. J Clin Invest. 1998;101:2182-2198.
16. Zhao J, Renner O, Wightman L, Sugden PH, Stewart L, Miller AD, Latchman DS, Marber MS. The expression of constitutively active isotypes of protein kinase C to investigate preconditioning. J Biol Chem. 1998;273:23072-23079.
17. Belli R, Bhatti ZA, Tang XL, Qiu Y, Zhang Q, Guo Y, Jadoon AK. Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide. Circ Res. 1997;81:42-52.
18. Zhao T, Xi L, Chelliah J, Levasseur JE, Kukreja RC. Inducible nitric oxide synthase mediates delayed myocardial protection induced by activation of adenosine A(1) receptors: evidence from gene-knockout mice. Circulation. 2000;102:902-907.
19. Dawn B, Bolli R. Role of nitric oxide in myocardial preconditioning. Ann NY Acad Sci. 2002;962:18-41.
20. Bolli R, Shinmura K, Tang XL, Kodani E, Xuan YT, Guo Y, Dawn B. Discovery of a new function of cyclooxygenase (COX)-2: COX-2 is a cardioprotective protein that alleviates ischemia/reperfusion injury and mediates the late phase of preconditioning. Cardiovasc Res. 2002;55:506-519.
21. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
22. Shi Q, Rafii S, Wu MH-D, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MAS, Storb RF, Hammond WP. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998;92:362-367.
23. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
24. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18:3964-3972.
25. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434-438.
26. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A. 2000;97:3422-3427.
27. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. 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.
28. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001;103:634-637.
29. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature. 2004;428:668-673.
30. Mallat Z, Silvestre JS, Le Ricousse-Roussanne S, Lecomte-Raclet L, Corbaz A, Clergue M, Duriez M, Barateau V, Akira S, Tedgui A, Tobelem G, Chvatchko Y, Levy BI. Interleukin-18/interleukin-18 binding protein signaling modulates ischemia-induced neovascularization in mice hindlimb. Circ Res. 2002;91:441-448.
31. Schratzberger P, Schratzberger G, Silver M, Curry C, Kearney M, Magner M, Alroy J, Adelman LS, Weinberg DH, Ropper AH, Isner JM. Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy. Nat Med. 2000;6:405-413.
32. Sato TN, Qin Y, Kozak CA, Audus KL. Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc Natl Acad Sci U S A. 1993;90:9355-9358.
33. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gentron-Maguire M, Gridley T, Wolburg H, Risau W, Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature. 1995;376:70-74.
34. Akita T, Murohara T, Ikeda H, Sasaki K, Shimada T, Egami K, Imaizumi T. Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Lab Invest. 2003;83:65-73.
35. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434-438.
36. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002;106:3009-3017.
37. Bell RM, Yellon DM. The contribution of endothelial nitric oxide synthase to early ischaemic preconditioning: the lowering of the preconditioning threshold: an investigation in eNOS knockout mice. Cardiovasc Res. 2001;52:274-280.
38. Kanno S, Lee PC, Zhang Y, Ho C, Griffith BP, Shears LL II, Billiar TR. Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation. 2000;101:2742-2748.
39. Zingarelli B, Hake PW, Yang Z, O'Connor M, Denenberg A, Wong HR. Absence of inducible nitric oxide synthase modulates early reperfusion-induced NF-kappaB and AP-1 activation and enhances myocardial damage. FASEB J. 2002;16:327-342.
40. Wang Y, Guo Y, Zhang SX, Wu WJ, Wang J, Bao W, Bolli R. Ischemic preconditioning upregulates inducible nitric oxide synthase in cardiac myocyte. J Mol Cell Cardiol. 2002;34:5-15.
41. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol. 2001;33:1897-1918.
42. Vasa M, Fichtischerer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:E1-E7.