Phosphoinositide 3-kinase γ gene knockout impairs postischemic neovascularization and endothelial progenitor cell functions

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 28, Issue 1, 2008, Pages 68-76

  Madeddu, Paolo ^a   Kraenkel, Nicolle ^a,c   Barcelos, Luciola S ^a   Siragusa, Mauro ^a   Campagnolo, Paola ^a   Oikawa, Atsuhiko ^a,c   Caporali, Andrea ^a   Herman, Andrew ^a   Azzolino, Ornella ^b   Barberis, Laura ^b   Perino, Alessia ^b   Damilano, Federico ^b   Emanueli, Costanza ^a   Hirsch, Emilio ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF TURIN   (Italy)

^c NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

Angiogenesis; Endothelial progenitor cells; Limb ischemia; Migration; Vasculogenesis

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENZYME; PHOSPHOINOSITIDE 3 KINASE GAMMA; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HYPOXIA; LIMB ISCHEMIA; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; EXTREMITIES; ISCHEMIA; ISOENZYMES; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH; NEOVASCULARIZATION, PHYSIOLOGIC; STEM CELLS; TRANSPLANTS;

EID: 37549023783     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.107.145573     Document Type: Article

References (40)

1. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6:389-395.
2. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343-353.
3. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535-602.
4. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399:601-605.
5. Jiang BH, Zheng JZ, Aoki M, Vogt PK. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc Natl Acad Sci U S A. 2000;97: 1749-1753.
6. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res. 2002;90:1243-1250.
7. Ahmad S, Hewett PW, Wang P, Al-Ani B, Cudmore M, Fujisawa T, Wang P, Haigh JJ, Le Noble F, Mukhopadhyay D, Ahmed A. Direct evidence for endothelial Flt-1 function in nitric oxide-mediated angiogenesis. Circ Res. 2006;99:715-722.
8. Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, Kollipara R, DePinho RA, Zeiher AM, Dimmeler S. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest. 2005;115:2382-2392.
9. Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, Rutten H, Fichtlscherer S, Martin H, Zeiher AM. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest. 2001;108:391-397.
10. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9:1370-1376.
11. Greif DM, Kou R, Michel T. Site specific dephosphorylation of endothelial nitric oxide synthase by protein phosphatase 2A: evidence for crosstalk between phosphorylation sites. Biochemistry. 2002;41: 15845-15853.
12. Vanhaesebroeck B, Ali K, Bilancio A, Geering B, Foukas LC. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem Sci. 2005;30:194-204.
13. Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, Silengo L, Sozzani S, Mantovani A, Altruda F, Wymann MP. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science. 2000;287:1049-1053.
14. Bondeva T, Pirola L, Bulgarelli-Leva G, Rubio I, Wetzker R, Wymann MP. Bifurcation of lipid and protein kinase signals of PI3Kgamma to the protein kinases PKB and MAPK. Science. 1998;282:293-296.
15. Patrucco E, Notte A, Barberis L, Selvetella G, Maffei A, Brancaccio M, Marengo S, Russo G, Azzolino O, Rybalkin SD, Silengo L, Altruda F, Wetzker R, Wymann MP, Lembo G, Hirsch E. PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell. 2004;118:375-387.
16. Crackower MA, Oudit GY, Kozieradzki I, Sarao R, Sun H, Sasaki T, Hirsch E, Suzuki A, Shioi T, Irie-Sasaki J, Sah R, Cheng HY, Rybin VO, Lembo G, Fratta L, Oliveira-dos-Santos AJ, Benovic JL, Kahn CR, Izumo S, Steinberg SF, Wymann MP, Backx PH, Penninger JM. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell. 2002;110:737-749.
17. Hirsch E, Lembo G, Montrucchio G, Rommel C, Costa C, Barberis L. Signaling through PI3Kgamma: a common platform for leukocyte, platelet and cardiovascular stress sensing. Thromb Haemost. 2006;95:29-35.
18. Go YM, Park H, Maland MC, Darley-Usmar VM, Stoyanov B, Wetzker R, Jo H. Phosphatidylinositol 3-kinase gamma mediates shear stress-dependent activation of JNK in endothelial cells. Am J Physiol. 1998; 275:H1898-H1904.
19. Puri KD, Doggett TA, Huang CY, Douangpanya J, Hayflick JS, Turner M, Penninger J, Diacovo TG. The role of endothelial PI3Kgamma activity in neutrophil trafficking. Blood. 2005;106:150-157.
20. Emanueli C, Minasi A, Zacheo A, Chao J, Chao L, Salis MB, Straino S, Tozzi MG, Smith R, Gaspa L, Bianchini G, Stillo F, Capogrossi MC, Madeddu P. Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia. Circulation. 2001;103:125-132.
21. Emanueli C, Graiani G, Salis MB, Gadau S, Desortes E, Madeddu P. Prophylactic gene therapy with human tissue kallikrein ameliorates limb ischemia recovery in type 1 diabetic mice. Diabetes. 2004;53:1096-1103.
22. Madeddu P, Emanueli C, Pelosi E, Salis MB, Cerio AM, Bonanno G, Patti M, Stassi G, Condorelli G, Peschle C. Transplantation of low dose CD34+KDR+ cells promotes vascular and muscular regeneration in ischemic limbs. Faseb J. 2004;18:1737-1739.
23. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, Hattori K, Zhang F, Hicklin DJ, Wu Y, Zhu Z, Dunn A, Salari H, Werb Z, Hackett NR, Crystal RG, Lyden D, Rafii S. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med. 2006; 12:557-567.
24. De Falco E, Porcelli D, Torella AR, Straino S, Iachininoto MG, Orlandi A, Truffa S, Biglioli P, Napolitano M, Capogrossi MC, Pesce M. SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells. Blood. 2004;104:3472-3482.
25. Hamada K, Sasaki T, Koni PA, Natsui M, Kishimoto H, Sasaki J, Yajima N, Horie Y, Hasegawa G, Naito M, Miyazaki J, Suda T, Itoh H, Nakao K, Mak TW, Nakano T, Suzuki A. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev. 2005; 19:2054-2065.
26. Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res. 1997;80:829-837.
27. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I, Joza N, Mak TW, Ohashi PS, Suzuki A, Penninger JM. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science. 2000;287:1040-1046.
28. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler HE. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation. 2005;111: 2198-2202.
29. Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, Tribulova S, Kuziel WA, Bachmann G, Schaper W. Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res. 2004;94:671-677.
30. Khmelewski E, Becker A, Meinertz T, Ito WD. Tissue resident cells play a dominant role in arteriogenesis and concomitant macrophage accumulation. Circ Res. 2004;95:E56-E64.
31. Urbich C, Knau A, Fichtlscherer S, Walter DH, Bruhl T, Potente M, Hofmann WK, de Vos S, Zeiher AM, Dimmeler S. FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. Faseb J. 2005;19:974-976.
32. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96:857-868.
33. Chen YH, Lin SJ, Lin FY, Wu TC, Tsao CR, Huang PH, Liu PL, Chen YL, Chen JW. High glucose impairs early and late endothelial progenitor cells by modifying nitric oxide-related but not oxidative stress-mediated mechanisms. Diabetes. 2007;56:1559-1568.
34. Vogt PK, Jiang H, Aoki M. Triple layer control: phosphorylation, acetylation and ubiquitination of FOXO proteins. Cell Cycle. 2005;4: 908-913.
35. Partovian C, Zhuang Z, Moodie K, Lin M, Ouchi N, Sessa WC, Walsh K, Simons M. PKCα activates eNOS and increases arterial Blood flow in vivo. Circ Res. 2005;97:482-487.
36. Urbich Reissner A, Chavakis E, Dernbach E, Haendeler J, Fleming I, Zeiher AM, Kaszkin M, Dimmeler S. Dephosphorylation of endothelial nitric oxide synthase contributes to the anti-angiogenic effects of endostatin. FASEB J. 2002;16:706-708.
37. Favot L, Keravis T, Holl V, Le Bec A, Lugnier C. VEGF-induced HUVEC migration and proliferation are decreased by PDE2 and PDE4 inhibitors. Thromb Haemost. 2003;90:334-343.
38. Kim S, Bakre M, Yin H, Varner JA. Inhibition of endothelial cell survival and angiogenesis by protein kinase A. J Clin Invest. 2002; 110:933-941.
39. Ruckle T, Schwarz MK, Rommel C. PI3Kgamma inhibition: towards an 'aspirin of the 21st century'? Nat Rev Drug Discov. 2006;5:903-918.
40. Doukas J, Wrasidlo W, Noronha G, Dneprovskaia E, Fine R, Weis S, Hood J, Demaria A, Soll R, Cheresh D. Phosphoinositide 3-kinase gamma/delta inhibition limits infarct size after myocardial ischemia/reperfusion injury. Proc Natl Acad Sci U S A. 2006;103:19866-19871.