Combination of the angiotensin-converting enzyme inhibitor perindopril and the diuretic indapamide activate postnatal vasculogenesis in spontaneously hypertensive rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 325, Issue 3, 2008, Pages 766-773

  You, Dong ^a   Cochain, Clément ^a   Loinard, Céline ^a   Vilar, José ^a   Mees, Barend ^b   Duriez, Micheline ^a   Lévy, Bernard I ^a   Silvestre, Jean Sébastien ^a,c  

^a INSERM   (France)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c HÔPITAL LARIBOISIÈRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDAPAMIDE; PERINDOPRIL; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIHYPERTENSIVE THERAPY; ARTICLE; BONE MARROW TRANSPLANTATION; CELL COUNT; CELL DIFFERENTIATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; ENDOTHELIUM CELL; ESSENTIAL HYPERTENSION; IN VITRO STUDY; MALE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; STEM CELL; STRAIN DIFFERENCE; WISTAR KYOTO RAT;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; ANTIGENS, CD34; ANTIHYPERTENSIVE AGENTS; DIURETICS; DRUG THERAPY, COMBINATION; FEMORAL ARTERY; HEMATOPOIETIC STEM CELLS; HYPERTENSION; INDAPAMIDE; MALE; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE II; PERINDOPRIL; PROTO-ONCOGENE PROTEINS C-KIT; RATS; RATS, INBRED SHR; RATS, INBRED WKY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 44249126231     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.107.131532     Document Type: Article

References (46)

1. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, and Dimmeler S (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9:1370-1376.
2. Aicher A, Rentsch M, Sasaki K, Ellwart JW, Fandrich F, Siebert R, Cooke JP, Dimmeler S, and Heeschen C (2007) Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circ Res 100:581-589.
3. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9:653-660.
4. Chen JZ, Zhang FR, Tao QM, Wang XX, Zhu JH, and Zhu JH (2004) Number and activity of endothelial progenitor cells from peripheral blood in patients with hypercholesterolaemia. Clin Sci (Lond) 107:273-280.
5. -/- mice. Circulation 99:3188-3198.
6. Dimmeler S and Zeiher AM (2000) Akt takes center stage in angiogenesis signaling. Circ Res 86:4-5.
7. Ebrahimian TG, Heymes C, You D, Blanc-Brude O, Mees B, Waeckel L, Duriez M, Vilar J, Brandes RP, Levy BI, et al. (2006) NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am J Pathol 169:719-728.
8. Emanueli C, Salis MB, Stacca T, Gaspa L, Chao J, Chao L, Piana A, and Madeddu P (2001) Rescue of impaired angiogenesis in spontaneously hypertensive rats by intramuscular human tissue kallikrein gene transfer. Hypertension 38:136-141.
9. Fabre JE, Rivard A, Magner M, Silver M, and Isner JM (1999) Tissue inhibition of angiotensin-converting enzyme activity stimulates angiogenesis in vivo. Circulation 99:3043-3049.
10. Fazel S, Cimini M, Chen L, Li S, Angoulvant D, Fedak P, Verma S, Weisel RD, Keating A, and Li RK (2006) Cardioprotective c-kit cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 116:1865-1877.
11. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, and Ferrara N (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway: requirement for Flk-1/KDR activation. J Biol Chem 273:30336-30343.
12. Hadrava V, Kruppa U, Russo RC, Lacourciere Y, Tremblay J, and Hamet P (1991) Vascular smooth muscle cell proliferation and its therapeutic modulation in hypertension. Am Heart J 122:1198-1203.
13. Hayakawa H, Coffee K, and Raij L (1997) Endothelial dysfunction and cardiorenal injury in experimental salt-sensitive hypertension: effects of antihypertensive therapy. Circulation 96:2407-2413.
14. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, and Kalka C (2005) Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 45:1441-1448.
15. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, and Finkel T (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348:593-600.
16. Imanishi T, Hano T, Sawamura T, and Nishio I (2004) Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin Exp Pharmacol Physiol 31:407-413.
17. Imanishi T, Moriwaki C, Hano T, and Nishio I (2005) Endothelial progenitor cell senescence is accelerated in both experimental hypertensive rats and patients with essential hypertension. J Hypertens 23:1831-1837.
18. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, et al. (2006) Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4 hemangiocytes. Nat Med 12:557-567.
19. Junquero DC, Schini VB, and Vanhoutte PM (1991) Indapamide potentiates the endothelium-dependent production of cyclic guanosine monophosphate by bradykinin in the canine femoral artery. Am Heart J 122:1204-1209.
20. Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y, and Murohara T (2004) Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol 24:1442-1447.
21. Konishi M and Su C (1983) Role of endothelium in dilator responses of spontaneously hypertensive rat arteries. Hypertension 5:881-886.
22. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, Lefer DJ, Sessa WC, and Walsh K (2000) The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6:1004-1010.
23. Levy BI, Duriez M, and Samuel JL (2001) Coronary microvasculature alteration in hypertensive rats: effect of treatment with a diuretic and an ACE inhibitor. Am J Hypertens 14:7-13.
24. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, and van Zonneveld AJ (2004) Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53:195-199.
25. Lüscher TF, Vanhoutte PM, and Raij L (1987) Antihypertensive treatment normalizes decreased endothelium-dependent relaxations in rats with salt-induced hypertension. Hypertension 9:III193-III197.
26. Matsunaga T, Warltier DC, Weihrauch DW, Moniz M, Tessmer J, and Chilian WM (2000) Ischemia-induced coronary collateral growth is dependent on vascular endothelial growth factor and nitric oxide. Circulation 102:3098-3103.
27. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101:2567-2578.
28. Nakano N, Moriguchi A, Morishita R, Kida I, Tomita N, Matsumoto K, Nakamura T, Higaki J, and Ogihara T (1997) Role of angiotensin II in the regulation of a novel vascular modulator, hepatocyte growth factor (HGF), in experimental hypertensive rats. Hypertension 30:1448-1454.
29. Panza JA, Quyyumi AA, Brush JE Jr, and Epstein SE (1990) Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. N Engl J Med 323:22-27.
30. Patel A, MacMahon S, Chalmers J, Neal B, Woodward M, Billot L, Harrap S, Poulter N, Marre M, Cooper M, et al. (2007) Effects of a fixed combination of perindopril and indapamide on macrovascular and microvascular outcomes in patients with type 2 diabetes mellitus (the ADVANCE trial): a randomised controlled trial. Lancet 370:829-840.
31. Pickkers P, Hughes AD, Russel FG, Thien T, and Smits P (1998) Thiazide-induced vasodilation in humans is mediated by potassium channel activation. Hypertension 32:1071-1076.
32. Rakusan K, Cicutti N, Maurin A, Guez D, and Schiavi P (2000) The effect of treatment with low dose ACE inhibitor and/or diuretic on coronary microvasculature in stroke-prone spontaneously hypertensive rats. Microvasc Res 59:243-254.
33. Schini VB, Dewey J, and Vanhoutte PM (1990) Effects of indapamide on endothelium-dependent relaxations in isolated canine femoral arteries. Am J Cardiol 65:6H-10H.
34. Shimada T, Takeshita Y, Murohara T, Sasaki K, Egami K, Shintani S, Katsuda Y, Ikeda H, Nabeshima Y, and Imaizumi T (2004) Angiogenesis and vasculogenesis are impaired in the precocious-aging klotho mouse. Circulation 110:1148-1155.
35. Silvestre JS, Bergaya S, Tamarat R, Duriez M, Boulanger CM, and Levy BI (2001) Proangiogenic effect of angiotensin-converting enzyme inhibition is mediated by the bradykinin B(2) receptor pathway. Circ Res 89:678-683.
36. Silvestre JS, Kamsu-Kom N, Clergue M, Duriez M, and Levy BI (2002) Very-low-dose combination of the angiotensin-converting enzyme inhibitor perindopril and the diuretic indapamide induces an early and sustained increase in neovascularization in rat ischemic legs. J Pharmacol Exp Ther 303:1038-1043.
37. Silvestre JS, Thery C, Hamard G, Boddaert J, Aguilar B, Delcayre A, Houbron C, Tamarat R, Blanc-Brude O, Heeneman S, et al. (2005) Lactadherin promotes VEGF-dependent neovascularization. Nat Med 11:499-506.
38. Smith RS Jr, Lin KF, Agata J, Chao L, and Chao J (2002) Human endothelial nitric oxide synthase gene delivery promotes angiogenesis in a rat model of hindlimb ischemia. Arterioscler Thromb Vasc Biol 22:1279-1285.
39. Takeshita S, Tomiyama H, Yokoyama N, Kawamura Y, Furukawa T, Ishigai Y, Shibano T, Isshiki T, and Sato T (2001) Angiotensin-converting enzyme inhibition improves defective angiogenesis in the ischemic limb of spontaneously hypertensive rats. Cardiovasc Res 52:314-320.
40. Tamarat R, Silvestre JS, Le Ricousse-Roussanne S, Barateau V, Lecomte-Raclet L, Clergue M, Duriez M, Tobelem G, and Levy BI (2004) Impairment in ischemia-induced neovascularization in diabetes: bone marrow mononuclear cell dysfunction and therapeutic potential of placenta growth factor treatment. Am J Pathol 164:457-466.
41. Tea BS, Dam TV, Moreau P, Hamet P, and deBlois D (1999) Apoptosis during regression of cardiac hypertrophy in spontaneously hypertensive rats: temporal regulation and spatial heterogeneity. Hypertension 34:229-235.
42. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, and Gurtner GC (2002) Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106:2781-2786.
43. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, and DuBois RN (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93:705-716.
44. Turnbull F (2003) Effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet 362:1527-1535.
45. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, and Dimmeler S (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89:E1-E7.
46. You D, Waeckel L, Ebrahimian TG, Blanc-Brude O, Foubert P, Barateau V, Duriez M, Lericousse-Roussanne S, Vilar J, Dejana E, et al. (2006) Increase in vascular permeability and vasodilation are critical for proangiogenic effects of stem cell therapy. Circulation 114:328-338.