Genetically modified endothelial progenitor cells in the therapy of cardiovascular disease and pulmonary hypertension

Current Vascular Pharmacology

Volumn 10, Issue 3, 2012, Pages 289-299

  Lavoie, Jessie R ^a   Stewart, Duncan J ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Endothelial progenitor cells; Gene therapy; Ischemic cardiovascular disease; Pulmonary hypertension; Vascular regeneration

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NITRIC OXIDE; STROMAL CELL DERIVED FACTOR 1ALPHA; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL CADHERIN;

ACUTE HEART INFARCTION; ANGIOGENESIS; APOPTOSIS; ARTERIAL WALL THICKNESS; ATHEROSCLEROSIS; CAPILLARY DENSITY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL ACTIVITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; COLONY FORMING UNIT; CORONARY ARTERY DISEASE; DNA MODIFICATION; ENDOTHELIAL PROGENITOR CELL; GENE OVEREXPRESSION; GENE THERAPY; HEART FUNCTION; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; ISCHEMIC CARDIOMYOPATHY; LECTIN BINDING; LIMB PERFUSION; METABOLIC SYNDROME X; MULTICENTER STUDY (TOPIC); MUSCLE PERFUSION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHAGOCYTOSIS; PREHYPERTENSION; PROTEOMICS; PULMONARY HYPERTENSION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; TRANSGENICS; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CARDIOVASCULAR DISEASES; ENDOTHELIAL CELLS; GENE THERAPY; GENETIC ENGINEERING; HUMANS; HYPERTENSION, PULMONARY; NEOVASCULARIZATION, PHYSIOLOGIC; RISK FACTORS; STEM CELL TRANSPLANTATION;

EID: 84860275424     PISSN: 15701611     EISSN: 18756212     Source Type: Journal    
DOI: 10.2174/157016112799959413     Document Type: Review

References (83)

1. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964-7.
2. Asahara T. Cell therapy and gene therapy using endothelial progenitor cells for vascular regeneration. Handb Exp Pharmacol 2007: 181-94.
3. Richardson MR, Yoder MC. Endothelial progenitor cells: quo vadis? J Mol Cell Cardiol 2011; 50: 266-72.
4. Yoder MC. Defining human endothelial progenitor cells. J Thromb Haemost 2009; 7 (Suppl 1): 49-52.
5. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2008; 28: 1584-95.
6. Alessandri G, Emanueli C, Madeddu P. Genetically engineered stem cell therapy for tissue regeneration. Ann N Y Acad Sci 2004; 271-84.
7. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 2000; 97: 3422-7.
8. Shintani S, Murohara T, Ikeda H, et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 2001; 103: 897-903.
9. Kawamoto A, Gwon HC, Iwaguro H, et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 2001; 103: 634-7.
10. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001; 7: 430-6.
11. Nagaya N, Kangawa K, Kanda M, et al. Hybrid cell-gene therapy for pulmonary hypertension based on phagocytosing action of endothelial progenitor cells. Circulation 2003; 108: 889-95.
12. Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res 2005; 96: 442-50.
13. Ormiston ML, Deng Y, Stewart DJ, Courtman DW. Innate immunity in the therapeutic actions of endothelial progenitor cells in pulmonary hypertension. Am J Respir Cell Mol Biol 2010; 43: 546-54.
14. Takahashi M, Nakamura T, Toba T, Kajiwara N, Kato H, Shimizu Y. Transplantation of endothelial progenitor cells into the lung to alleviate pulmonary hypertension in dogs. Tissue Eng 2004; 10: 771-9.
15. Assmus B, Honold J, Schachinger V, et al. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 2006; 355: 1222-32.
16. Assmus B, Rolf A, Erbs S, et al. Clinical outcome 2 years after intracoronary administration of bone marrow-derived progenitor cells in acute myocardial infarction. Circ Heart Fail 2010; 3: 89-96.
17. Janssens S, Dubois C, Bogaert J, et al. Autologous bone marrowderived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006; 367: 113-21.
18. Schachinger V, Erbs S, Elsasser A, et al. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 2006; 355: 1210-21.
19. Zhu JH, Wang XX, Zhang FR, et al. Safety and efficacy of autologous endothelial progenitor cells transplantation in children with idiopathic pulmonary arterial hypertension: open-label pilot study. Pediatr Transplant 2008; 12: 650-5.
20. Wang XX, Zhang FR, Shang YP, et al. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. J Am Coll Cardiol 2007; 49: 1566-71.
21. Loomans CJ, de Koning EJ, Staal FJ, et al. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004; 53: 195-9.
22. Sibal L, Aldibbiat A, Agarwal SC, et al. Circulating endothelial progenitor cells, endothelial function, carotid intima-media thickness and circulating markers of endothelial dysfunction in people with type 1 diabetes without macrovascular disease or microalbuminuria. Diabetologia 2009; 52: 1464-73.
23. Jialal I, Devaraj S, Singh U, Huet BA. Decreased number and impaired functionality of endothelial progenitor cells in subjects with metabolic syndrome: implications for increased cardiovascular risk. Atherosclerosis 2010; 211: 297-302.
24. Thum T, Fraccarollo D, Schultheiss M, et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 2007; 56: 666-74.
25. Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001; 89: E1-7.
26. Umemura T, Soga J, Hidaka T, et al. Aging and hypertension are independent risk factors for reduced number of circulating endothelial progenitor cells. Am J Hypertens 2008; 21: 1203-9.
27. Heeschen C, Lehmann R, Honold J, et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 2004; 109: 1615-22.
28. MacEneaney OJ, DeSouza CA, Weil BR, et al. Prehypertension and endothelial progenitor cell function. J Hum Hypertens 2011; 25: 57-62.
29. Oliveras A, Soler MJ, Martinez-Estrada OM, et al. Endothelial progenitor cells are reduced in refractory hypertension. J Hum Hypertens 2008; 22: 183-90.
30. Werner N, Kosiol S, Schiegl T, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353: 999-1007.
31. Schmidt-Lucke C, Rossig L, Fichtlscherer S, et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 2005; 111: 2981-7.
32. Werner N, Wassmann S, Ahlers P, et al. Endothelial progenitor cells correlate with endothelial function in patients with coronary artery disease. Basic Res Cardiol 2007; 102: 565-71.
33. Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348: 593-600.
34. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C. Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 2005; 45: 1441-8.
35. Edelberg JM, Tang L, Hattori K, Lyden D, Rafii S. Young adult bone marrow-derived endothelial precursor cells restore agingimpaired cardiac angiogenic function. Circ Res 2002; 90: E89-93.
36. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003; 108: 457-63.
37. Tepper OM, Galiano RD, Capla JM, et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002; 106: 2781-6.
38. Ward MR, Thompson KA, Isaac K, et al. Nitric oxide synthase gene transfer restores activity of circulating angiogenic cells from patients with coronary artery disease. Mol Ther 2011; 19: 1323-30.
39. Giannotti G, Doerries C, Mocharla PS, et al. Impaired endothelial repair capacity of early endothelial progenitor cells in prehypertension: relation to endothelial dysfunction. Hypertension 2010; 55: 1389-97.
40. Diller GP, Thum T, Wilkins MR, Wharton J. Endothelial progenitor cells in pulmonary arterial hypertension. Trends Cardiovasc Med 2010; 20: 22-9.
41. Satoh K, Kagaya Y, Nakano M, et al. Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation 2006; 113: 1442-50.
42. Davie NJ, Crossno JT Jr, Frid MG, et al. Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol 2004; 286: L668-78.
43. Hayashida K, Fujita J, Miyake Y, et al. Bone marrow-derived cells contribute to pulmonary vascular remodeling in hypoxia-induced pulmonary hypertension. Chest 2005; 127: 1793-8.
44. Junhui Z, Xingxiang W, Guosheng F, Yunpeng S, Furong Z, Junzhu C. Reduced number and activity of circulating endothelial progenitor cells in patients with idiopathic pulmonary arterial hypertension. Respir Med 2008; 102: 1073-9.
45. Diller GP, van Eijl S, Okonko DO, et al. Circulating endothelial progenitor cells in patients with Eisenmenger syndrome and idio pathic pulmonary arterial hypertension. Circulation 2008; 117: 3020-30.
46. Fadini GP, Schiavon M, Rea F, Avogaro A, Agostini C. Depletion of endothelial progenitor cells may link pulmonary fibrosis and pulmonary hypertension. Am J Respir Crit Care Med 2007; 176: 724-5; author reply 5.
47. Asosingh K, Aldred MA, Vasanji A, et al. Circulating angiogenic precursors in idiopathic pulmonary arterial hypertension. Am J Pathol 2008; 172: 615-27.
48. Toshner M, Voswinckel R, Southwood M, et al. Evidence of dysfunction of endothelial progenitors in pulmonary arterial hypertension. Am J Respir Crit Care Med 2009; 180: 780-7.
49. Smadja DM, Gaussem P, Mauge L, et al. Circulating endothelial cells: a new candidate biomarker of irreversible pulmonary hypertension secondary to congenital heart disease. Circulation 2009; 119: 374-81.
50. Frid MG, Brunetti JA, Burke DL, et al. Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol 2006; 168: 659-69.
51. Nikam VS, Schermuly RT, Dumitrascu R, et al. Treprostinil inhibits the recruitment of bone marrow-derived circulating fibrocytes in chronic hypoxic pulmonary hypertension. Eur Respir J 2010; 36: 1302-14.
52. Marsboom G, Pokreisz P, Gheysens O, et al. Sustained endothelial progenitor cell dysfunction after chronic hypoxia-induced pulmonary hypertension. Stem Cells 2008; 26: 1017-26.
53. Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, et al. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res 2006; 98: 209-17.
54. Lane KB, Machado RD, Pauciulo MW, et al. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Nat Genet 2000; 26: 81-4.
55. Thomson JR, Machado RD, Pauciulo MW, et al. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet 2000; 37: 741-5.
56. Machado RD, Pauciulo MW, Thomson JR, et al. BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am J Hum Genet 2001; 68: 92-102.
57. Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 1994; 144: 275-85.
58. Atkinson C, Stewart S, Upton PD, et al. Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 2002; 105: 1672-8.
59. Reynolds PN. Gene therapy for pulmonary hypertension: prospects and challenges. Expert Opin Biol Ther 2011; 11: 133-43.
60. Chen HK, Hung HF, Shyu KG, et al. Combined cord blood stem cells and gene therapy enhances angiogenesis and improves cardiac performance in mouse after acute myocardial infarction. Eur J Clin Invest 2005; 35: 677-86.
61. Iwaguro H, Yamaguchi J, Kalka C, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 2002; 105: 732-8.
62. Yi C, Xia W, Zheng Y, et al. Transplantation of endothelial progenitor cells transferred by vascular endothelial growth factor gene for vascular regeneration of ischemic flaps. J Surg Res 2006; 135: 100-6.
63. Ikeda Y, Fukuda N, Wada M, et al. Development of angiogenic cell and gene therapy by transplantation of umbilical cord blood with vascular endothelial growth factor gene. Hypertens Res 2004; 27: 119-28.
64. Murasawa S, Llevadot J, Silver M, Isner JM, Losordo DW, Asahara T. Constitutive human telomerase reverse transcriptase expression enhances regenerative properties of endothelial progenitor cells. Circulation 2002; 106: 1133-9.
65. Choi JH, Hur J, Yoon CH, et al. Augmentation of therapeutic angiogenesis using genetically modified human endothelial progenitor cells with altered glycogen synthase kinase-3beta activity. J Biol Chem 2004; 279: 49430-8.
66. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004; 29: 95-102.
67. Cho HJ, Youn SW, Cheon SI, et al. Regulation of endothelial cell and endothelial progenitor cell survival and vasculogenesis by integrin-linked kinase. Arterioscler Thromb Vasc Biol 2005; 25: 1154-60.
68. Morishita R, Nakamura S, Hayashi S, et al. Therapeutic angiogenesis induced by human recombinant hepatocyte growth factor in rabbit hind limb ischemia model as cytokine supplement therapy. Hypertension 1999; 33: 1379-84.
69. Bussolino F, Di Renzo MF, Ziche M, et al. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol 1992; 119: 629-41.
70. Comoglio PM, Trusolino L. Invasive growth: from development to metastasis. J Clin Invest 2002; 109: 857-62.
71. Yamamoto Y, Matsuura T, Narazaki G, et al. Synergistic effects of autologous cell and hepatocyte growth factor gene therapy for neovascularization in a murine model of hindlimb ischemia. Am J Physiol Heart Circ Physiol 2009; 297: H1329-36.
72. Jiang M, Wang B, Wang C, et al. Angiogenesis by transplantation of HIF-1 alpha modified EPCs into ischemic limbs. J Cell Biochem 2008; 103: 321-34.
73. Jiang M, Wang B, Wang C, et al. In vivo enhancement of angiogenesis by adenoviral transfer of HIF-1alpha-modified endothelial progenitor cells (Ad-HIF-1alpha-modified EPC for angiogenesis). Int J Biochem Cell Biol 2008; 40: 2284-95.
74. Kong D, Melo LG, Gnecchi M, et al. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation 2004; 110: 2039-46.
75. Chen SY, Wang F, Yan XY, et al. Autologous transplantation of EPCs encoding FGF1 gene promotes neovascularization in a porcine model of chronic myocardial ischemia. Int J Cardiol 2009; 135: 223-32.
76. Marrotte EJ, Chen DD, Hakim JS, Chen AF. Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 2010; 120: 4207-19.
77. Tamarat R, Silvestre JS, Le Ricousse-Roussanne S, et al. Impairment in ischemia-induced neovascularization in diabetes: bone marrow mononuclear cell dysfunction and therapeutic potential of placenta growth factor treatment. Am J Pathol 2004; 164: 457-66.
78. Chen F, Tan Z, Dong CY, et al. Combination of VEGF(165)/ Angiopoietin-1 gene and endothelial progenitor cells for therapeutic neovascularization. Eur J Pharmacol 2007; 568: 222-30.
79. Yu JX, Huang XF, Lv WM, et al. Combination of stromal-derived factor-1alpha and vascular endothelial growth factor gene-modified endothelial progenitor cells is more effective for ischemic neovascularization. J Vasc Surg 2009; 50: 608-16.
80. Das H, George JC, Joseph M, et al. Stem cell therapy with overexpressed VEGF and PDGF genes improves cardiac function in a rat infarct model. PLoS One 2009; 4: e7325.
81. Zhao Q, Liu Z, Wang Z, Yang C, Liu J, Lu J. Effect of preprocalcitonin gene-related peptide-expressing endothelial progenitor cells on pulmonary hypertension. Ann Thorac Surg 2007; 84: 544-52.
82. van Oostrom O, de Kleijn DP, Fledderus JO, et al. Folic acid supplementation normalizes the endothelial progenitor cell transcriptome of patients with type 1 diabetes: a case-control pilot study. Cardiovasc Diabetol 2009; 8: 47.
83. Seeger FH, Chen L, Spyridopoulos I, Altschmied J, Aicher A, Haendeler J. Downregulation of ETS rescues diabetes-induced reduction of endothelial progenitor cells. PLoS One 2009; 4: e4529.