Dipeptidyl peptidase-4 inhibition and vascular repair by mobilization of endogenous stem cells in diabetes and beyond

Atherosclerosis

Volumn 229, Issue 1, 2013, Pages 23-29

  Fadini, Gian Paolo ^a   Avogaro, Angelo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Angiogenesis; Atherosclerosis; Bone marrow; Endothelium; Regeneration

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DIPEPTIDYL PEPTIDASE IV; ERYTHROPOIETIN; GLUCAGON LIKE PEPTIDE 1; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 3; JANUS KINASE 2; JANUS KINASE 3; PLERIXAFOR; SITAGLIPTIN; STROMAL CELL DERIVED FACTOR 1ALPHA;

ADULT STEM CELL; ANGIOGENESIS; CELL MIGRATION; DIABETES MELLITUS; DIABETIC NEUROPATHY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HEMATOPOIESIS; HUMAN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL MOBILIZATION;

ATHEROSCLEROSIS; DIABETIC ANGIOPATHIES; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; REGENERATION;

EID: 84879416505     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2013.04.007     Document Type: Review

References (105)

1. Avogaro A., Fadini G.P., Gallo A., Pagnin E., de Kreutzenberg S. Endothelial dysfunction in type 2 diabetes mellitus. Nutr Metab Cardiovasc Dis 2006, 1(Suppl. 16):S39-S45.
2. Avogaro A., de Kreutzenberg S.V., Fadini G. Endothelial dysfunction: causes and consequences in patients with diabetes mellitus. Diabetes Res Clin Pract 2008, 2(Suppl. 82):S94-S101.
3. Hirsch E.Z., Chisolm G.M., White H.M. Reendothelialization and maintenance of endothelial integrity in longitudinal denuded tracks in the thoracic aorta of rats. Atherosclerosis 1983, 46:287-307.
4. Gade P.V., Andrades J.A., Nimni M.E., et al. Nitric oxide mediates hyperglycemia-induced defective migration in cultured endothelial cells. JVasc Surg 1997, 26:319-326.
5. Fadini G.P., Agostini C., Avogaro A. Endothelial progenitor cells and vascular biology in diabetes mellitus: current knowledge and future perspectives. Curr Diabetes Rev 2005, 1:41-58.
6. Fadini G.P., Agostini C., Sartore S., Avogaro A. Endothelial progenitor cells in the natural history of atherosclerosis. Atherosclerosis 2007, 194:46-54.
7. Foteinos G., Hu Y., Xiao Q., Metzler B., Xu Q. Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apolipoprotein E-deficient mice. Circulation 2008, 117:1856-1863.
8. Fadini G.P., Albiero M., Boscaro E., Agostini C., Avogaro A. Endothelial progenitor cells as resident accessory cells for post-ischemic angiogenesis. Atherosclerosis 2009, 204:20-22.
9. Ryu J.C., Davidson B.P., Xie A., et al. Molecular imaging of the paracrine proangiogenic effects of progenitor cell therapy in limb ischemia. Circulation 2013, 127:710-719.
10. Ingram D.A., Caplice N.M., Yoder M.C. Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells. Blood 2005, 106:1525-1531.
11. Rossig L., Urbich C., Dimmeler S. Endothelial progenitor cells at work: not mature yet, but already stress-resistant. Arterioscler Thromb Vasc Biol 2004, 24:1977-1979.
12. Asahara T., Kawamoto A., Masuda H. Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells 2011, 29:1650-1655.
13. Napoli C., Hayashi T., Cacciatore F., et al. Endothelial progenitor cells as therapeutic agents in the microcirculation: an update. Atherosclerosis 2011, 215:9-22.
14. Dimmeler S., Zeiher A.M. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis?. JMol Med (Berl) 2004, 82:671-677.
15. Nelson W.D., Zenovich A.G., Ott H.C., et al. Sex-dependent attenuation of plaque growth after treatment with bone marrow mononuclear cells. Circ Res 2007, 101:1319-1327.
16. George J., Afek A., Abashidze A., et al. Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 2005, 25:2636-2641.
17. Ii M., Nishimura H., Iwakura A., et al. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation 2005, 111:1114-1120.
18. Landmesser U., Engberding N., Bahlmann F.H., et al. 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.
19. Fadini G.P., Losordo D., Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 2012, 110:624-637.
20. Albiero M., Menegazzo L., Avogaro A., Fadini G.P. Pharmacologic targeting of endothelial progenitor cells. Cardiovasc Hematol Disord Drug Targets 2010, 10:16-32.
21. Fadini G.P., Avogaro A. Potential manipulation of endothelial progenitor cells in diabetes and its complications. Diabetes Obes Metab 2010, 12:570-583.
22. Teraa M., Sprengers R.W., van der Graaf Y., et al. Autologous bone marrow-derived cell therapy in patients with critical limb ischemia: a meta-analysis of randomized controlled clinical trials. Ann Surg 2013 Feb 19, [Epub ahead of print].
23. 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.
24. Clifford D.M., Fisher S.A., Brunskill S.J., et al. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev 2012, 2:CD006536.
25. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. NEngl J Med 2005, 352:1685-1695.
26. Majesky M.W., Dong X.R., Hoglund V., Mahoney W.M., Daum G. The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol 2011, 31:1530-1539.
27. Albiero M., Menegazzo L., Fadini G.P. Circulating smooth muscle progenitors and atherosclerosis. Trends Cardiovasc Med 2010, 20:133-140.
28. Stoehr R., Federici M. Do stem cells cause aging-related intimal medial thickening?. Atherosclerosis 2012, 224:39-40.
29. Zoll J., Fontaine V., Gourdy P., et al. Role of human smooth muscle cell progenitors in atherosclerotic plaque development and composition. Cardiovasc Res 2008, 77:471-480.
30. Yu H., Stoneman V., Clarke M., et al. Bone marrow-derived smooth muscle-like cells are infrequent in advanced primary atherosclerotic plaques but promote atherosclerosis. Arterioscler Thromb Vasc Biol 2011, 31:1291-1299.
31. Imamura H., Ohta T., Tsunetoshi K., et al. Transdifferentiation of bone marrow-derived endothelial progenitor cells into the smooth muscle cell lineage mediated by transforming growth factor-beta1. Atherosclerosis 2010, 211:114-121.
32. Fledderus J.O., van Oostrom O., de Kleijn D.P., et al. Increased amount of bone marrow-derived smooth muscle-like cells and accelerated atherosclerosis in diabetic apoE-deficient mice. Atherosclerosis 2013, 226:341-347.
33. Fadini G.P., Tjwa M. Arole for TGF-beta in transforming endothelial progenitor cells into neointimal smooth muscle cells. Atherosclerosis 2010, 211:32-35.
34. Fadini G.P. Adiseased bone marrow fuels atherosclerosis in diabetes. Atherosclerosis 2012.
35. Aicher A., Zeiher A.M., Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension 2005, 45:321-325.
36. Augustyns K., Bal G., Thonus G., et al. The unique properties of dipeptidyl-peptidase IV (DPP IV/CD26) and the therapeutic potential of DPP IV inhibitors. Curr Med Chem 1999, 6:311-327.
37. Iwata S., Yamaguchi N., Munakata Y., et al. CD26/dipeptidyl peptidase IV differentially regulates the chemotaxis of T cells and monocytes toward RANTES: possible mechanism for the switch from innate to acquired immune response. Int Immunol 1999, 11:417-426.
38. Shah Z., Pineda C., Kampfrath T., et al. Acute DPP-4 inhibition modulates vascular tone through GLP-1 independent pathways. Vascul Pharmacol 2011, 55:2-9.
39. Campbell T.B., Broxmeyer H.E. CD26 inhibition and hematopoiesis: a novel approach to enhance transplantation. Front Biosci 2008, 13:1795-1805.
40. Takasawa W., Ohnuma K., Hatano R., et al. Inhibition of dipeptidyl peptidase 4 regulates microvascular endothelial growth induced by inflammatory cytokines. Biochem Biophys Res Commun 2010, 401:7-12.
41. Drucker D.J. Dipeptidyl peptidase-4 inhibition and the treatment of type 2 diabetes: preclinical biology and mechanisms of action. Diabetes Care 2007, 30:1335-1343.
42. Drucker D.J. The biology of incretin hormones. Cell Metab 2006, 3:153-165.
43. 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.
44. Zhong J., Rao X., Rajagopalan S. An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: potential implications in cardiovascular disease. Atherosclerosis 2013, 226:305-314.
45. Fadini G.P., Avogaro A. Cardiovascular effects of DPP-4 inhibition: beyond GLP-1. Vascul Pharmacol 2011, 55:10-16.
46. Matheeussen V., Jungraithmayr W., De Meester I. Dipeptidyl peptidase 4 as a therapeutic target in ischemia/reperfusion injury. Pharmacol Ther 2012, 136:267-282.
47. De La Luz Sierra M., Yang F., Narazaki M., et al. Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood 2004, 103:2452-2459.
48. Crump M.P., Gong J.H., Loetscher P., et al. Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 1997, 16:6996-7007.
49. Proost P., Struyf S., Schols D., et al. Processing by CD26/dipeptidyl-peptidase IV reduces the chemotactic and anti-HIV-1 activity of stromal-cell-derived factor-1alpha. FEBS Lett 1998, 432:73-76.
50. Shigeta T., Aoyama M., Bando Y.K., et al. Dipeptidyl peptidase-4 modulates left ventricular dysfunction in chronic heart failure via angiogenesis-dependent and -independent actions. Circulation 2012, 126:1838-1851.
51. Aicher A., Rentsch M., Sasaki K., et al. Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 2007, 100:581-589.
52. Zhang Y., Huang B. Peripheral blood stem cells: phenotypic diversity and potential clinical applications. Stem Cell Rev 2012, 8:917-925.
53. Hoggatt J., Scadden D.T. The stem cell niche: tissue physiology at a single cell level. JClin Invest 2012, 122:3029-3034.
54. Lucas D., Battista M., Shi P.A., Isola L., Frenette P.S. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 2008, 3:364-366.
55. Lapidot T., Dar A., Kollet O. How do stem cells find their way home?. Blood 2005, 106:1901-1910.
56. Petit I., Szyper-Kravitz M., Nagler A., et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 2002, 3:687-694.
57. 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.
58. Katayama Y., Battista M., Kao W.M., et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006, 124:407-421.
59. Lucas D., Bruns I., Battista M., et al. Norepinephrine reuptake inhibition promotes mobilization in mice: potential impact to rescue low stem cell yields. Blood 2012, 119:3962-3965.
60. Yamaguchi J., Kusano K.F., Masuo O., et al. Stromal cell-derived factor-1 effects on exvivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 2003, 107:1322-1328.
61. De Falco E., Porcelli D., Torella A.R., et al. SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells. Blood 2004, 104:3472-3482.
62. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10:858-864.
63. Amadesi S., Reni C., Katare R., et al. Role for substance p-based nociceptive signaling in progenitor cell activation and angiogenesis during ischemia in mice and in human subjects. Circulation 2012, 125:1774-1786. S1771-1719.
64. Cooper K.G., Zarnowski R., Woods J.P. Histoplasma capsulatum encodes a dipeptidyl peptidase active against the mammalian immunoregulatory peptide, substance P. PLoS One 2009, 4:e5281.
65. Guieu R., Fenouillet E., Devaux C., et al. CD26 modulates nociception in mice via its dipeptidyl-peptidase IV activity. Behav Brain Res 2006, 166:230-235.
66. Ceradini D.J., Gurtner G.C. Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 2005, 15:57-63.
67. Zernecke A., Schober A., Bot I., et al. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 2005, 96:784-791.
68. Xu Q., Wang J., He J., et al. Impaired CXCR4 expression and cell engraftment of bone marrow-derived cells from aged atherogenic mice. Atherosclerosis 2011, 219:92-99.
69. Broxmeyer H.E., Hoggatt J., O'Leary H.A., et al. Dipeptidylpeptidase 4 negatively regulates colony-stimulating factor activity and stress hematopoiesis. Nat Med 2012, 18:1786-1796.
70. Menegazzo L., Albiero M., Avogaro A., Fadini G.P. Endothelial progenitor cells in diabetes mellitus. Biofactors 2012, 38:194-202.
71. Avogaro A., Albiero M., Menegazzo L., de Kreutzenberg S., Fadini G.P. Endothelial dysfunction in diabetes: the role of reparatory mechanisms. Diabetes Care 2011, 2(Suppl. 34):S285-S290.
72. Mangialardi G., Katare R., Oikawa A., et al. Diabetes causes bone marrow endothelial barrier dysfunction by activation of the RhoA-Rho-associated kinase signaling pathway. Arterioscler Thromb Vasc Biol 2013, 33:555-564.
73. Spinetti G., Cordella D., Fortunato O., et al. Global remodeling of the vascular stem cell niche in bone marrow of diabetic Patients: Implication of the miR-155/FOXO3a signaling pathway. Circ Res 2012, 112:510-522.
74. Mangialardi G., Oikawa A., Reni C., Madeddu P. Bone marrow microenvironment: a newly recognized target for diabetes-induced cellular damage. Endocr Metab Immune Disord Drug Targets 2012, 12:159-167.
75. Fadini G.P. Is bone marrow another target of diabetic complications?. Eur J Clin Invest 2011, 41:457-463.
76. Orlandi A., Chavakis E., Seeger F., et al. Long-term diabetes impairs repopulation of hematopoietic progenitor cells and dysregulates the cytokine expression in the bone marrow microenvironment in mice. Basic Res Cardiol 2010, 105:703-712.
77. Oikawa A., Siragusa M., Quaini F., et al. Diabetes mellitus induces bone marrow microangiopathy. Arterioscler Thromb Vasc Biol 2010, 30:498-508.
78. Busik J.V., Tikhonenko M., Bhatwadekar A., et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. JExp Med 2009, 206:2897-2906.
79. Ferraro F., Lymperi S., Mendez-Ferrer S., et al. Diabetes impairs hematopoietic stem cell mobilization by altering niche function. Sci Transl Med 2011, 3. 104ra101.
80. Fadini G.P., Albiero M., Seeger F., et al. Stem cell compartmentalization in diabetes and high cardiovascular risk reveals the role of DPP-4 in diabetic stem cell mobilopathy. Basic Res Cardiol 2013, 108:313.
81. Fadini G.P., Albiero M., Vigili de Kreutzenberg S., et al. Diabetes impairs stem cell and proangiogenic cell mobilization in humans. Diabetes Care 2013 Apr, 36(4):943-949. [Epub 2012 Oct 30]. 10.2337/dc12-1084.
82. Ling L., Shen Y., Wang K., et al. Worse clinical outcomes in acute myocardial infarction patients with type 2 diabetes mellitus: relevance to impaired endothelial progenitor cells mobilization. PLoS One 2012, 7:e50739.
83. Fadini G.P., Sartore S., Schiavon M., et al. Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats. Diabetologia 2006, 49:3075-3084.
84. Fadini G.P., Boscaro E., Albiero M., et al. The oral dipeptidyl peptidase-4 inhibitor sitagliptin increases circulating endothelial progenitor cells in patients with type 2 diabetes: possible role of stromal-derived factor-1alpha. Diabetes Care 2010, 33:1607-1609.
85. Goncalves A., Leal E., Paiva A., et al. Protective effects of the dipeptidyl peptidase IV inhibitor sitagliptin in the blood-retinal barrier in a type 2 diabetes animal model. Diabetes Obes Metab 2012, 14:454-463.
86. Vinik A.I., Maser R.E., Mitchell B.D., Freeman R. Diabetic autonomic neuropathy. Diabetes Care 2003, 26:1553-1579.
87. Fiorina P., Jurewicz M., Vergani A., et al. Targeting the CXCR4-CXCL12 axis mobilizes autologous hematopoietic stem cells and prolongs isletallograft survival via programmed death ligand 1. JImmunol 2011, 186:121-131.
88. Tepper O.M., Carr J., Allen R.J., et al. Decreased circulating progenitor cell number and failed mechanisms of stromal cell-derived factor-1alpha mediated bone marrow mobilization impair diabetic tissue repair. Diabetes 2010, 59:1974-1983.
89. Paganessi L.A., Walker A.L., Tan L.L., et al. Effective mobilization of hematopoietic progenitor cells in G-CSF mobilization defective CD26-/- mice through AMD3100-induced disruption of the CXCL12-CXCR4 axis. Exp Hematol 2011, 39:384-390.
90. Huang C.Y., Shih C.M., Tsao N.W., et al. Dipeptidyl peptidase-4 inhibitor improves neovascularization by increasing circulating endothelial progenitor cells. Br J Pharmacol 2012, 167:1506-1519.
91. Segers V.F., Revin V., Wu W., et al. Protease-resistant stromal cell-derived factor-1 for the treatment of experimental peripheral artery disease. Circulation 2011, 123:1306-1315.
92. Hocher B., Sharkovska Y., Mark M., Klein T., Pfab T. The novel DPP-4 inhibitors linagliptin and BI 14361 reduce infarct size after myocardial ischemia/reperfusion in rats. Int J Cardiol 2012 Jan 2.
93. Kanki S., Segers V.F., Wu W., et al. Stromal cell-derived factor-1 retention and cardioprotection for ischemic myocardium. Circ Heart Fail 2011, 4:509-518.
94. Zaruba M.M., Zhu W., Soonpaa M.H., et al. Granulocyte colony-stimulating factor treatment plus dipeptidylpeptidase-IV inhibition augments myocardial regeneration in mice expressing cyclin D2 in adult cardiomyocytes. Eur Heart J 2012, 33:129-137.
95. Zaruba M.M., Theiss H.D., Vallaster M., et al. Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell 2009, 4:313-323.
96. Theiss H.D., Vallaster M., Rischpler C., et al. Dual stem cell therapy after myocardial infarction acts specifically by enhanced homing via the SDF-1/CXCR4 axis. Stem Cell Res 2011, 7:244-255.
97. Theiss H.D., Brenner C., Engelmann M.G., et al. 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.
98. Wang C.H., Verma S., Hsieh I.C., et al. Enalapril increases ischemia-induced endothelial progenitor cell mobilization through manipulation of the CD26 system. JMol Cell Cardiol 2006, 41:34-43.
99. Huber B.C., Brunner S., Segeth A., et al. Parathyroid hormone is a DPP-IV inhibitor and increases SDF-1-driven homing of CXCR4(+) stem cells into the ischaemic heart. Cardiovasc Res 2011, 90:529-537.
100. Wu J.Y., Scadden D.T., Kronenberg H.M. Role of the osteoblast lineage in the bone marrow hematopoietic niches. JBone Miner Res 2009, 24:759-764.
101. Ervinna N., Mita T., Yasunari E., et al. Anagliptin, a DPP-4 inhibitor, suppresses proliferation of vascular smooth muscles and monocyte inflammatory reaction and attenuates atherosclerosis in male apo e-deficient mice. Endocrinology 2013, 154:1260-1270.
102. Smith R.J., Bryant R.G. Metal substitutions incarbonic anhydrase: a halide ion probe study. Biochem Biophys Res Commun 1975, 66:1281-1286.
103. Ta N.N., Schuyler C.A., Li Y., Lopes-Virella M.F., Huang Y. DPP-4 (CD26) inhibitor alogliptin inhibits atherosclerosis in diabetic apolipoprotein E-deficient mice. JCardiovasc Pharmacol 2011, 58:157-166.
104. Tokgozoglu L., Yorgun H., Gurses K.M., et al. The association between circulating endothelial progenitor cells and coronary collateral formation. Atherosclerosis 2011, 219:851-854.
105. Raz I., Hanefeld M., Xu L., et al. Efficacy and safety of the dipeptidyl peptidase-4 inhibitor sitagliptin as monotherapy in patients with type 2 diabetes mellitus. Diabetologia 2006, 49:2564-2571.