Inhibition of PAI-1 induces neutrophil-driven neoangiogenesis and promotes tissue regeneration via production of angiocrine factors in mice

Blood

Volumn 119, Issue 26, 2012, Pages 6382-6393

  Tashiro, Yoshihiko ^a,b   Nishida, Chiemi ^a   Sato Kusubata, Kaori ^c   Ohki Koizumi, Makiko ^a   Ishihara, Makoto ^a   Sato, Aki ^a   Gritli, Ismael ^a   Komiyama, Hiromitsu ^a,b   Sato, Yayoi ^a   Dan, Takashi ^d   Miyata, Toshio ^d   Okumura, Ko ^b   Tomiki, Yuichi ^b   Sakamoto, Kazuhiro ^b   Nakauchi, Hiromitsu ^a   Heissig, Beate ^a,b,c   Hattori, Koichi ^a,b  

^a THE UNIVERSITY OF TOKYO   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

5 CHLORO 2 [[2 [4 (DIPHENYLMETHYL)PIPERAZIN 1 YL] 2 OXOETHOXYACETYL]AMINO]BENZOATE; FIBROBLAST GROWTH FACTOR 2; GELATINASE B; GRANULOCYTE COLONY STIMULATING FACTOR; PIPERAZINE DERIVATIVE; PLASMINOGEN ACTIVATOR INHIBITOR 1; STEM CELL FACTOR; TISSUE PLASMINOGEN ACTIVATOR; TM 5275; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; GASTROCNEMIUS MUSCLE; GENE INACTIVATION; IMMUNOHISTOCHEMISTRY; LEG ISCHEMIA; MOUSE; MUSCLE NECROSIS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN SYNTHESIS; TISSUE REGENERATION;

EID: 84863533516     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-399659     Document Type: Article

References (38)

1. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6(4):389.
2. Heissig B, Nishida C, Tashiro Y, et al. Role of neutrophil-derived matrix metalloproteinase-9 in tissue regeneration. Histol Histopathol. 2010;25(6):765-770.
3. Simons M, Ware JA. Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov. 2003;2(11):863-871. (Pubitemid 37407792)
4. Heissig B, Hattori K, Friedrich M, Rafii S, Werb Z. Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr Opin Hematol. 2003;10(2):136-141. (Pubitemid 36207969)
5. Dellas C, Loskutoff DJ. Historical analysis of PAI-1 from its discovery to its potential role in cell motility and disease. Thromb Haemost. 2005;93(4):631-640. (Pubitemid 40485397)
6. Stefansson S, Lawrence DA. The serpin PAI-1 inhibits cell migration by blocking integrin alpha V beta 3 binding to vitronectin. Nature. 1996;383(6599):441-443. (Pubitemid 26330833)
7. Cao C, Lawrence DA, Li Y, et al. Endocytic receptor LRP together with tPA and PAI-1 coordinates Mac-1-dependent macrophage migration. EMBO J. 2006;25(9):1860-1870.
8. Carmeliet P, Moons L, Lijnen R, et al. Inhibitory role of plasminogen activator inhibitor-1 in arterial wound healing and neointima formation: a gene targeting and gene transfer study in mice. Circulation. 1997;96(9):3180-3191. (Pubitemid 27500124)
9. Fay WP, Shapiro AD, Shih JL, Schleef RR, Ginsburg D. Brief report: complete deficiency of plasminogen-activator inhibitor type 1 due to a frame-shift mutation. N Engl J Med. 1992;327(24):1729-1733.
10. Sawdey MS, Loskutoff DJ. Regulation of murine type 1 plasminogen activator inhibitor gene expression in vivo. Tissue specificity and induction by lipopolysaccharide, tumor necrosis factor-alpha, and transforming growth factor-beta. J Clin Invest. 1991;88(4):1346-1353.
11. Sakamoto T, Yasue H, Ogawa H, Misumi I, Masuda T. Association of patency of the infarct-related coronary artery with plasma levels of plasminogen activator inhibitor activity in acute myocardial infarction. Am J Cardiol. 1992;70(3):271-276.
12. Juhan-Vague I, Pyke SD, Alessi MC, Jespersen J, Haverkate F, Thompson SG. Fibrinolytic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. ECAT Study Group. European Concerted Action on Thrombosis and Disabilities. Circulation. 1996;94(9):2057-2063. (Pubitemid 26360493)
13. Diebold I, Kraicun D, Bonello S, Gorlach A. The 'PAI-1 paradox' in vascular remodeling. Thromb Haemost. 2008;100(6):984-991.
14. Stefansson S, McMahon GA, Petitclerc E, Lawrence DA. Plasminogen activator inhibitor-1 in tumor growth, angiogenesis and vascular remodeling. Curr Pharm Des. 2003;9(19):1545-1564. (Pubitemid 36763492)
15. McMahon GA, Petitclerc E, Stefansson S, et al. Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis. J Biol Chem. 2001;276(36):33964-33968.
16. van Meijer M, Smilde A, Tans G, Nesheim ME, Pannekoek H, Horrevoets AJG. The suicide substrate reaction between plasminogen activator inhibitor 1 and thrombin is regulated by the cofactors vitronectin and heparin. Blood. 1997;90(5):1874-1882. (Pubitemid 27377297)
17. Lijnen HR, Arza B, Van Hoef B, Collen Ds Declerck PJ. Inactivation of plasminogen activator inhibitor-1 by specific proteolysis with stromelysin-1 (MMP-3). J Biol Chem. 2000;275(48):37645-37650. (Pubitemid 32004876)
18. Izuhara Y, Yamaoka N, Kodama H, et al. A novel inhibitor of plasminogen activator inhibitor-1 provides antithrombotic benefits devoid of bleeding effect in non-human primates. J Cereb Blood Flow Metab. 2010;30(5):904-912.
19. Ohki M, Ohki Y, Ishihara M, et al. Tissue type plasminogen activator regulates myeloid-cell dependent neoangiogenesis during tissue regeneration. Blood. 2010;115(21):4302-4312.
20. Loskutoff DJ, Sawdey M, Keeton M, Schneiderman J. Regulation of PAI-1 gene expression in vivo. Thromb Haemost. 1993;70(1):135-137. (Pubitemid 23225465)
21. Ohki Y, Heissig B, Sato Y, et al. Granulocyte colony-stimulating factor promotes neovascularization by releasing vascular endothelial growth factor from neutrophils. FASEB J. 2005;19(14):2005-2007. (Pubitemid 41759746)
22. Drinane M, Walsh J, Mollmark J, Simons M, Mulligan-Kehoe MJ. The anti-angiogenic activity of rPAI-1(23) inhibits fibroblast growth factor-2 functions. J Biol Chem. 2006;281(44):33336-33344. (Pubitemid 46036715)
23. Ardi VC, Van den Steen PE, Opdenakker G, Schweighofer B, Deryugina EI, Quigley JP. Neutrophil MMP-9 proenzyme, unencumbered by TIMP-1, undergoes efficient activation in vivo and catalytically induces angiogenesis via a basic fibroblast growth factor (FGF-2)/FGFR-2 pathway. J Biol Chem. 2009;284(38):25854-25866.
24. Murakami M, Simons M. Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol. 2008;15(3):215-220. (Pubitemid 351507574)
25. Gregory AD, Capoccia BJ, Woloszynek JR, Link DC. Systemic levels of G-CSF and interleukin-6 determine the angiogenic potential of bone marrow resident monocytes. J Leukoc Biol. 2010;88(1):123-131.
26. Magnusson PU, Dimberg A, Mellberg S, Lukinius A, Claesson-Welsh L. FGFR-1 regulates angiogenesis through cytokines interleukin-4 and pleiotrophin. Blood. 2007;110(13):4214-4222. (Pubitemid 351377785)
27. Jin DK, Shido K, Kopp HG, et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med. 2006;12(5):557-567.
28. Heissig B, Werb Z, Rafii S, Hattori K. Role of c-kit/Kit ligand signaling in regulating vasculogenesis. Thromb Haemost. 2003;90(4):570-576. (Pubitemid 37287623)
29. Heissig B, Rafii S, Akiyama H, et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med. 2005;202(6):739-750. (Pubitemid 41345963)
30. Heissig B, Lund LR, Akiyama H, et al. The plasminogen fibrinolytic pathway is required for hematopoietic regeneration. Cell Stem Cell. 2007;1(6):658-670. (Pubitemid 350215332)
31. Renckens R, Roelofs JJTH, De Waard V, et al. The role of plasminogen activator inhibitor type 1 in the inflammatory response to local tissue injury. J Thromb Haemost. 2005;3(5):1018-1025. (Pubitemid 41632834)
32. Park K-W, Kwon Y-W, Cho H-J, et al. G-CSF exerts dual effects on endothelial cells-Opposing actions of direct eNOS induction versus indirect CRP elevation. J Mol Cell Cardiol. 2008;45(5):670-678.
33. Kanellakis P, Slater NJ, Du XJ, Bobik A, Curtis DJ. Granulocyte colony-stimulating factor and stem cell factor improve endogenous repair after myocardial infarction. Cardiovasc Res. 2006;70(1):117-125.
34. Minnerup J, Heidrich J,Wellmann J, Rogalewski A, Schneider A, Schabitz WR. Meta-analysis of the efficacy of granulocyte-colony stimulating factor in animal models of focal cerebral ischemia. Stroke. 2008;39(6):1855-1861.
35. Muhs BE, Gagne P, Plitas G, Shaw JP, Shamamian P. Experimental hindlimb ischemia leads to neutrophil-mediated increases in gastrocnemius MMP-2 and -9 activity: a potential mechanism for ischemia induced MMPactivation. J Surg Res. 2004;117(2):249-254. (Pubitemid 38393650)
36. May AE, Kanse SM, Lund LR, Gisler RH, Imhof BA, Preissner KT. Urokinase receptor (CD87) regulates leukocyte recruitment via beta 2 integrins in vivo. J Exp Med. 1998;188(6):1029-1037. (Pubitemid 28443326)
37. Zhao Y, Sharma AK, LaPar DJ, et al. Depletion of tissue plasminogen activator attenuates lung ischemia-reperfusion injury via inhibition of neutrophil extravasation. Am J Physiol Lung Cell Mol Physiol. 2011;300(5):L718-L729.
38. Reichel CA, Lerchenberger M, Uhl B, et al. Plasmin inhibitors prevent leukocyte accumulation and remodeling events in the postischemic microvasculature. PLoS One. 2011;6(2):e17229.