Restoring stem cell mobilization to promote vascular repair in diabetes

Vascular Pharmacology

Volumn 58, Issue 4, 2013, Pages 253-258

  Albiero, Mattia ^a   Avogaro, Angelo ^a,b   Fadini, Gian Paolo ^a,b  

^a VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Bone marrow; DPP 4; Gliptins; Regeneration

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; BENFOTIAMINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIPEPTIDYL PEPTIDASE IV; DIPEPTIDYL PEPTIDASE IV INHIBITOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIUM DERIVED HYPERPOLARIZING FACTOR; ERYTHROPOIETIN; GRANULOCYTE COLONY STIMULATING FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN; METFORMIN; OLMESARTAN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLERIXAFOR; PROSTACYCLIN; SITAGLIPTIN; STROMAL CELL DERIVED FACTOR 1ALPHA; THROMBOXANE A2; VASCULOTROPIN A;

ADIPOGENESIS; APOPTOSIS; BIOAVAILABILITY; BONE MARROW CELL; COMPETITIVE INHIBITION; DIABETES MELLITUS; DRUG MEGADOSE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HEART FAILURE; HUMAN; HYPERTENSION; INSULIN RELEASE; ISCHEMIC CARDIOMYOPATHY; LIFESTYLE MODIFICATION; LOW DRUG DOSE; NON INSULIN DEPENDENT DIABETES MELLITUS; OSTEOBLAST; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL MOBILIZATION; THROMBOSIS; UPREGULATION; VASCULAR ENDOTHELIUM; VASCULAR SURGERY; VASCULARIZATION;

ANIMALS; BONE MARROW; BONE MARROW CELLS; CARDIOVASCULAR DISEASES; CHEMOKINE CXCL12; DIABETES MELLITUS; DIPEPTIDYL PEPTIDASE 4; ENDOTHELIUM, VASCULAR; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; STEM CELLS;

EID: 84875371654     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2013.01.003     Document Type: Review

References (82)

1. Adams R.H., Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8:464-478.
2. Aicher A., Heeschen C., Mildner-Rihm C., Urbich C., Ihling C., Technau-Ihling K., Zeiher A.M., Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat. Med. 2003, 9:1370-1376.
3. Albiero M., Fadini G.P. Strategies for enhancing progenitor cell mobilization and function in diabetes. Curr. Vasc. Pharmacol. 2012, 10:310-321.
4. Albiero M., Menegazzo L., Boscaro E., Agostini C., Avogaro A., Fadini G.P. Defective recruitment, survival and proliferation of bone marrow-derived progenitor cells at sites of delayed diabetic wound healing in mice. Diabetologia 2011, 54:945-953.
5. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., Witzenbichler B., Schatteman G., Isner J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997, 275:964-967.
6. Asahara T., Masuda H., Takahashi T., Kalka C., Pastore C., Silver M., Kearne M., Magner M., Isner J.M. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85:221-228.
7. Avogaro A., Fadini G.P., Gallo A., Pagnin E., de Kreutzenberg S. Endothelial dysfunction in type 2 diabetes mellitus. Nutr. Metab. Cardiovasc. Dis. 2006, 16(Suppl. 1):S39-S45.
8. Avogaro A., de Kreutzenberg S.V., Fadini G. Endothelial dysfunction: causes and consequences in patients with diabetes mellitus. Diabetes Res. Clin. Pract. 2008, 82(Suppl. 2):S94-S101.
9. Avogaro A., de Kreutzenberg S.V., Fadini G.P. Oxidative stress and vascular disease in diabetes: is the dichotomization of insulin signaling still valid?. Free Radic. Biol. Med. 2008, 44:1209-1215.
10. Avogaro A., Albiero M., Menegazzo L., de Kreutzenberg S., Fadini G.P. Endothelial dysfunction in diabetes: the role of reparatory mechanisms. Diabetes Care 2011, 34(Suppl. 2):S285-S290.
11. Bahlmann F.H., De Groot K., Spandau J.-M., Landry A.L., Hertel B., Duckert T., Boehm S.M., Menne J., Haller H., Fliser D. Erythropoietin regulates endothelial progenitor cells. Blood 2004, 103:921-926.
12. Bahlmann F.H., de Groot K., Mueller O., Hertel B., Haller H., Fliser D. Stimulation of endothelial progenitor cells: a new putative therapeutic effect of angiotensin II receptor antagonists. Hypertension 2005, 45:526-529.
13. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
14. Broxmeyer H.E., Hoggatt J., O'Leary H.A., Mantel C., Chitteti B.R., Cooper S., Messina-Graham S., Hangoc G., Farag S., Rohrabaugh S.L., Ou X., Speth J., Pelus L.M., Srour E.F., Campbell T.B. Dipeptidylpeptidase 4 negatively regulates colony-stimulating factor activity and stress hematopoiesis. Nat. Med. 2012, 18:1786-1796.
15. Bruedigam C., Eijken M., Koedam M., van de Peppel J., Drabek K., Chiba H., van Leeuwen J.P.T.M. A new concept underlying stem cell lineage skewing that explains the detrimental effects of thiazolidinediones on bone. Stem Cells 2010, 28:916-927.
16. Busik J.V., Tikhonenko M., Bhatwadekar A., Opreanu M., Yakubova N., Caballero S., Player D., Nakagawa T., Afzal A., Kielczewski J., Sochacki A., Hasty S., Li Calzi S., Kim S., Duclas S.K., Segal M.S., Guberski D.L., Esselman W.J., Boulton M.E., Grant M.B. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. J. Exp. Med. 2009, 206:2897-2906.
17. Ceradini D.J., Kulkarni A.R., Callaghan M.J., Tepper O.M., Bastidas N., Kleinman M.E., Capla J.M., Galiano R.D., Levine J.P., Gurtner G.C. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 2004, 10:858-864.
18. Chen Y.-H., Lin S.-J., Lin F.-Y., Wu T.-C., Tsao C.-R., Huang P.-H., Liu P.-L., Chen Y.-L., Chen J.-W. 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.
19. Christopherson K.W., Cooper S., Broxmeyer H.E. Cell surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood 2003, 101:4680-4686.
20. De Clercq E. The AMD3100 story: the path to the discovery of a stem cell mobilizer (Mozobil). Biochem. Pharmacol. 2009, 77:1655-1664.
21. Deindl E., Zaruba M.M., Brunner S., Huber B., Assmann G., Hoefer I.E., Mueller-Hoecker J., Franz W.M. Application of G-CSF after myocardial infarction enhances arterial growth and improves cardiac function in mice. Vasc. Pharmacol. 2006, 45:e62-e63.
22. DiPersio J.F. Diabetic stem-cell "mobilopathy". N. Engl. J. Med. 2011, 365:2536-2538.
23. Drucker D.J. The biology of incretin hormones. Cell Metab. 2006, 3:153-165.
24. Engelmann M.G., Theiss H.D., Hennig-Theiss C., Huber A., Wintersperger B.J., Werle-Ruedinger A.-E., Schoenberg S.O., Steinbeck G., Franz W.-M. Autologous bone marrow stem cell mobilization induced by granulocyte colony-stimulating factor after subacute ST-segment elevation myocardial infarction undergoing late revascularization: final results from the G-CSF-STEMI (granulocyte colony-stimulating factor ST-segment elevation myocardial infarction) trial. J. Am. Coll. Cardiol. 2006, 48:1712-1721.
25. Fadini G.P. Is bone marrow another target of diabetic complications?. Eur. J. Clin. Invest. 2011, 41:457-463.
26. Fadini G.P., Avogaro A. Potential manipulation of endothelial progenitor cells in diabetes and its complications. Diabetes Obes. Metab. 2010, 12:570-583.
27. Fadini G.P., Avogaro A. Cardiovascular effects of DPP-4 inhibition: beyond GLP-1. Vascul. Pharmacol. 2011, 55:10-16.
28. Fadini, G.P., Avogaro, A., in press. Diabetes impairs mobilization of stem cells for the treatment of cardiovascular disease: a meta-regression analysis. Int. J. Cardiol. (pii: S0167-5273(12)01522-7). http://dx.doi.org/10.1016/j.ijcard.2012.10.089.
29. Fadini G.P., Sartore S., Schiavon M., Albiero M., Baesso I., Cabrelle A., Agostini C., Avogaro A. Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats. Diabetologia 2006, 49:3075-3084.
30. Fadini G.P., de Kreutzenberg S., Albiero M., Coracina A., Pagnin E., Baesso I., Cignarella A., Bolego C., Plebani M., Nardelli G.B., Sartore S., Agostini C., Avogaro A. Gender differences in endothelial progenitor cells and cardiovascular risk profile: the role of female estrogens. Arterioscler. Thromb. Vasc. Biol. 2008, 28:997-1004.
31. Fadini G.P., Agostini C., Avogaro A. Autologous stem cell therapy for peripheral arterial disease meta-analysis and systematic review of the literature. Atherosclerosis 2010, 209:10-17.
32. Fadini G.P., Albiero M., Boscaro E., Menegazzo L., Cabrelle A., Piliego T., Federici M., Agostini C., Avogaro A. Rosuvastatin stimulates clonogenic potential and anti-inflammatory properties of endothelial progenitor cells. Cell Biol. Int. 2010, 34:709-715.
33. Fadini G.P., Boscaro E., de Kreutzenberg S., Agostini C., Seeger F., Dimmeler S., Zeiher A., Tiengo A., Avogaro A. Time course and mechanisms of circulating progenitor cell reduction in the natural history of type 2 diabetes. Diabetes Care 2010, 33:1097-1102.
34. Fadini G.P., de Kreutzenberg S.V., Mariano V., Boscaro E., Bertolini F., Mancuso P., Quarna J., Marescotti M., Agostini C., Tiengo A., Avogaro A. Optimized glycaemic control achieved with add-on basal insulin therapy improves indexes of endothelial damage and regeneration in type 2 diabetic patients with macroangiopathy: a randomized cross-over trial comparing detemir versus glargine. Diabetes Obes. Metab. 2011, 13:718-725.
35. Fadini G.P., Albiero M., Menegazzo L., de Kreutzenberg S.V., Avogaro A. The increased dipeptidyl peptidase-4 activity is not counteracted by optimized glucose control in type 2 diabetes, but is lower in metformin-treated patients. Diabetes Obes. Metab. 2012, 14:518-522.
36. Fadini G.P., Mancuso P., Bertolini F., de Kreutzenberg S., Avogaro A. Amelioration of glucose control mobilizes circulating pericyte progenitor cells in type 2 diabetic patients with microangiopathy. Exp. Diabetes Res. 2012, 2012:274363.
37. Fadini, G.P., Albiero, M., Vigili de Kreutzenberg, S., Boscaro, E., Cappellari, R., Marescotti, M., Poncina, N., Agostini, C., Avogaro, A., in press. Diabetes impairs stem cell and proangiogenic cell mobilization in humans. Diabetes Care. http://dx.doi.org/10.2337/dc12-1084.
38. Fadini G.P., Albiero M., Seeger F., Poncina N., Menegazzo L., Angelini A., Castellani C., Thiene G., Agostini C., Cappellari R., Boscaro E., Zeiher A., Dimmeler S., Avogaro A. Stem cell compartmentalization in diabetes and high cardiovascular risk reveals the role of DPP-4 in diabetic stem cell mobilopathy. Basic Research in Cardiol. 2013, 108:313. 10.1007/s00395-012-0313-1.
39. Falk E. Pathogenesis of atherosclerosis. J. Am. Coll. Cardiol. 2006, 47:C7-C12.
40. Ferraro F., Lymperi S., Méndez-Ferrer S., Saez B., Spencer J.A., Yeap B.Y., Masselli E., Graiani G., Prezioso L., Rizzini E.L., Mangoni M., Rizzoli V., Sykes S.M., Lin C.P., Frenette P.S., Quaini F., Scadden D.T. Diabetes impairs hematopoietic stem cell mobilization by altering niche function. Sci. Transl. Med. 2011, 3:104ra101.
41. Fox C.S. Cardiovascular disease risk factors, type 2 diabetes mellitus, and the Framingham Heart Study. Trends Cardiovasc. Med. 2010, 20:90-95.
42. Hellström M., Phng L.-K., Hofmann J.J., Wallgard E., Coultas L., Lindblom P., Alva J., Nilsson A.-K., Karlsson L., Gaiano N., Yoon K., Rossant J., Iruela-Arispe M.L., Kalén M., Gerhardt H., Betsholtz C. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445:776-780.
43. Hristov M., Fach C., Becker C., Heussen N., Liehn E.A., Blindt R., Hanrath P., Weber C. Reduced numbers of circulating endothelial progenitor cells in patients with coronary artery disease associated with long-term statin treatment. Atherosclerosis 2007, 192:413-420.
44. Huang P., Li S., Han M., Xiao Z., Yang R., Han Z.C. Autologous transplantation of granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells improves critical limb ischemia in diabetes. Diabetes Care 2005, 28:2155-2160.
45. Humpert P.M., Djuric Z., Zeuge U., Oikonomou D., Seregin Y., Laine K., Eckstein V., Nawroth P.P., Bierhaus A. Insulin stimulates the clonogenic potential of angiogenic endothelial progenitor cells by IGF-1 receptor-dependent signaling. Mol. Med. 2008, 14:301-308.
46. Ii M., Takenaka H., Asai J., Ibusuki K., Mizukami Y., Maruyama K., Yoon Y.-S., Wecker A., Luedemann C., Eaton E., Silver M., Thorne T., Losordo D.W. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ. Res. 2006, 98:697-704.
47. Jeong J.-O., Kim M.-O., Kim H., Lee M.-Y., Kim S.-W., Ii M., Lee J.-U., Lee J., Choi Y.J., Cho H.-J., Lee N., Silver M., Wecker A., Kim D.-W., Yoon Y.-S. Dual angiogenic and neurotrophic effects of bone marrow-derived endothelial progenitor cells on diabetic neuropathy. Circulation 2009, 119:699-708.
48. Jung C., Rafnsson A., Shemyakin A., Böhm F., Pernow J. Different subpopulations of endothelial progenitor cells and circulating apoptotic progenitor cells in patients with vascular disease and diabetes. Int. J. Cardiol. 2010, 143:368-372.
49. Kränkel 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.
50. Landmesser U., Engberding N., Bahlmann F.H., Schaefer A., Wiencke A., Heineke A., Spiekermann S., Hilfiker-Kleiner D., Templin C., Kotlarz D., Mueller M., Fuchs M., Hornig B., Haller H., Drexler H. Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation 2004, 110:1933-1939.
51. Lebovitz H.E. Differentiating members of the thiazolidinedione class: a focus on safety. Diabetes Metab. Res. Rev. 2002, 18(Suppl. 2):S23-S29.
52. Llevadot J., Murasawa S., Kureishi Y., Uchida S., Masuda H., Kawamoto A., Walsh K., Isner J.M., Asahara T. HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J. Clin. Invest. 2001, 108:399-405.
53. Madonna R., De Caterina R. Cellular and molecular mechanisms of vascular injury in diabetes-part I: pathways of vascular disease in diabetes. Vascul. Pharmacol. 2011, 54:68-74.
54. Marchetti V., Menghini R., Rizza S., Vivanti A., Feccia T., Lauro D., Fukamizu A., Lauro R., Federici M. Benfotiamine counteracts glucose toxicity effects on endothelial progenitor cell differentiation via Akt/FoxO signaling. Diabetes 2006, 55:2231-2237.
55. Menegazzo L., Albiero M., Avogaro A., Fadini G.P. Endothelial progenitor cells in diabetes mellitus. Biofactors 2012, 38:194-202.
56. Murohara T., Asahara T., Silver M., Bauters C., Masuda H., Kalka C., Kearney M., Chen D., Symes J.F., Fishman M.C., Huang P.L., Isner J.M. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 1998, 101:2567-2578.
57. Oikawa A., Siragusa M., Quaini F., Mangialardi G., Katare R.G., Caporali A., van Buul J.D., van Alphen F.P.J., Graiani G., Spinetti G., Kraenkel N., Prezioso L., Emanueli C., Madeddu P. Diabetes mellitus induces bone marrow microangiopathy. Arterioscler. Thromb. Vasc. Biol. 2010, 30:498-508.
58. Petrelli A., Maestroni A., Fadini G.P., Belloni D., Venturini M., Albiero M., Kleffel S., Mfarrej B.G., Maschio A.D., Maffi P., Avogaro A., Ferrero E., Zerbini G., Secchi A., Fiorina P. Improved function of circulating angiogenic cells is evident in type 1 diabetic islet-transplanted patients. Am. J. Transplant. 2010, 10:2690-2700.
59. Pistrosch F., Herbrig K., Oelschlaegel U., Richter S., Passauer J., Fischer S., Gross P. PPARgamma-agonist rosiglitazone increases number and migratory activity of cultured endothelial progenitor cells. Atherosclerosis 2005, 183:163-167.
60. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146:873-887.
61. Pradhan A.D., Manson J.E., Rifai N., Buring J.E., Ridker P.M. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001, 286:327-334.
62. Ramirez R., Carracedo J., Nogueras S., Buendia P., Merino A., Cañadillas S., Rodríguez M., Tetta C., Martin-Malo A., Aljama P. Carbamylated darbepoetin derivative prevents endothelial progenitor cell damage with no effect on angiogenesis. J. Mol. Cell. Cardiol. 2009, 47:781-788.
63. Risau W. Mechanisms of angiogenesis. Nature 1997, 386:671-674.
64. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340:115-126.
65. Schröder K., Kohnen A., Aicher A., Liehn E.A., Büchse T., Stein S., Weber C., Dimmeler S., Brandes R.P. NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ. Res. 2009, 105:537-544.
66. Seeger F.H., Sedding D., Langheinrich A.C., Haendeler J., Zeiher A.M., Dimmeler S. Inhibition of the p38 MAP kinase in vivo improves number and functional activity of vasculogenic cells and reduces atherosclerotic disease progression. Basic Res. Cardiol. 2010, 105:389-397.
67. Shah Z., Pineda C., Kampfrath T., Maiseyeu A., Ying Z., Racoma I., Deiuliis J., Xu X., Sun Q., Moffatt-Bruce S., Villamena F., Rajagopalan S. Acute DPP-4 inhibition modulates vascular tone through GLP-1 independent pathways. Vascul. Pharmacol. 2011, 55:2-9.
68. Shepherd R.M., Capoccia B.J., Devine S.M., Dipersio J., Trinkaus K.M., Ingram D., Link D.C. Angiogenic cells can be rapidly mobilized and efficiently harvested from the blood following treatment with AMD3100. Blood 2006, 108:3662-3667.
69. Sorrentino S.A., Bahlmann F.H., Besler C., Müller M., Schulz S., Kirchhoff N., Doerries C., Horváth T., Limbourg A., Limbourg F., Fliser D., Haller H., Drexler H., Landmesser U. Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation 2007, 116:163-173.
70. Theiss H.D., Brenner C., Engelmann M.G., Zaruba M.-M., Huber B., Henschel V., Mansmann U., Wintersperger B., Reiser M., Steinbeck G., Franz W.-M. Safety and efficacy of SITAgliptin plus GRanulocyte-colony-stimulating factor in patients suffering from Acute Myocardial Infarction (SITAGRAMI-trial)-rationale, design and first interim analysis. Int. J. Cardiol. 2010, 145:282-284.
71. Urao N., Okigaki M., Yamada H., Aadachi Y., Matsuno K., Matsui A., Matsunaga S., Tateishi K., Nomura T., Takahashi T., Tatsumi T., Matsubara H. Erythropoietin-mobilized endothelial progenitors enhance reendothelialization via Akt-endothelial nitric oxide synthase activation and prevent neointimal hyperplasia. Circ. Res. 2006, 98:1405-1413.
72. Urbich C., Dernbach E., Zeiher A.M., Dimmeler S. Double-edged role of statins in angiogenesis signaling. Circ. Res. 2002, 90:737-744.
73. Van Belle E., Bauters C., Asahara T., Isner J.M. Endothelial regrowth after arterial injury: from vascular repair to therapeutics. Cardiovasc. Res. 1998, 38:54-68.
74. Vasa M., Fichtlscherer S., Adler K., Aicher A., Martin H., Zeiher A.M., Dimmeler S. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 2001, 103:2885-2890.
75. Walter D.H., Rittig K., Bahlmann F.H., Kirchmair R., Silver M., Murayama T., Nishimura H., Losordo D.W., Asahara T., Isner J.M. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 2002, 105:3017-3024.
76. Wang C.-H., Verma S., Hsieh I.-C., Chen Y.-J., Kuo L.-T., Yang N.-I., Wang S.-Y., Wu M.-Y., Hsu C.-M., Cheng C.-W., Cherng W.-J. Enalapril increases ischemia-induced endothelial progenitor cell mobilization through manipulation of the CD26 system. J. Mol. Cell. Cardiol. 2006, 41:34-43.
77. Wang C.-H., Ting M.-K., Verma S., Kuo L.-T., Yang N.-I., Hsieh I.-C., Wang S.-Y., Hung A., Cherng W.-J. Pioglitazone increases the numbers and improves the functional capacity of endothelial progenitor cells in patients with diabetes mellitus. Am. Heart J. 2006, 152:1051.e1-1051.e8.
78. Yoder M.C., Ingram D.A. The definition of EPCs and other bone marrow cells contributing to neoangiogenesis and tumor growth: is there common ground for understanding the roles of numerous marrow-derived cells in the neoangiogenic process?. Biochim. Biophys. Acta 2009, 1796:50-54.
79. Zaruba M.-M., Theiss H.D., Vallaster M., Mehl U., Brunner S., David R., Fischer R., Krieg L., Hirsch E., Huber B., Nathan P., Israel L., Imhof A., Herbach N., Assmann G., Wanke R., Mueller-Hoecker J., Steinbeck G., Franz W.-M. Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell 2009, 4:313-323.
80. Zhou B., Bi Y.Y., Han Z.B., Ren H., Fang Z.H., Yu X.F., Poon M.-C., Han Z.C. G-CSF-mobilized peripheral blood mononuclear cells from diabetic patients augment neovascularization in ischemic limbs but with impaired capability. J. Thromb. Haemost. 2006, 4:993-1002.
81. Ziebart T., Yoon C.-H., Trepels T., Wietelmann A., Braun T., Kiessling F., Stein S., Grez M., Ihling C., Muhly-Reinholz M., Carmona G., Urbich C., Zeiher A.M., Dimmeler S. Sustained persistence of transplanted proangiogenic cells contributes to neovascularization and cardiac function after ischemia. Circ. Res. 2008, 103:1327-1334.
82. Zohlnhöfer D., Ott I., Mehilli J., Schömig K., Michalk F., Ibrahim T., Meisetschläger G., von Wedel J., Bollwein H., Seyfarth M., Dirschinger J., Schmitt C., Schwaiger M., Kastrati A., Schömig A., REVIVAL-2 Investigators Stem cell mobilization by granulocyte colony-stimulating factor in patients with acute myocardial infarction: a randomized controlled trial. JAMA 2006, 295:1003-1010.