Stem cell aging and age-related cardiovascular disease: perspectives of treatment by ex-vivo stem cell rejuvenation

Current Drug Targets

Volumn 16, Issue 8, 2015, Pages 780-785

  Madonna, Rosalinda ^a,h,i   Engel, Felix B ^b   Davidson, Sean M ^c   Ferdinandy, Péter ^d,e   Görbe, Anikó ^e,f   Sluijter, Joost P G ^g   Van Laake, Linda W ^g  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e PHARMAHUNGARY GROUP   (Hungary)

^f UNIVERSITY OF SZEGED   (Hungary)

^g UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^h TEXAS HEART INSTITUTE   (United States)

ⁱ UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Aging; Diabetes; Gene therapy; Hippo; Hyperlipidemia; Myocardin; Notch; Pim 1; Rejuvenation; Stem cell; Telomerase; YAP

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; HIPPO PROTEIN KINASE; MYOCARDIN; NOTCH RECEPTOR; PROTEIN; PROTEIN KINASE PIM 1; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; VASCULOTROPIN; YES ASSOCIATED PROTEIN;

ARTICLE; CARDIAC STEM CELL; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL AGING; CELL PROLIFERATION; CELL SURVIVAL; DNA MODIFICATION; HEART FAILURE; ISCHEMIC HEART DISEASE; LIMB ISCHEMIA; NONHUMAN; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; REGENERATION; SENESCENCE; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE REPAIR; AGING; ANIMAL; CARDIOVASCULAR DISEASES; HUMAN; PATHOLOGY; PHYSIOLOGY; PROCEDURES; REGENERATIVE MEDICINE; REJUVENATION;

AGING; ANIMALS; CARDIOVASCULAR DISEASES; CELL AGING; HUMANS; REGENERATIVE MEDICINE; REJUVENATION; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84940902140     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450116666141205153258     Document Type: Article

References (88)

1. MERIT-HF Study Group. Effect of metoprolol CR/XL in chronic heart failure: metoprolol CR/XL randomised intervention trial in congestive heart failure (MERIT-HF). Lancet 1999; 353: 2001-7.
2. Tooke JE. Possible pathophysiological mechanisms for diabetic angiopathy in type 2 diabetes. J Diabetes Complications 2000; 14(4): 197-200.
3. Hirsch AT, Haskal ZJ, Hertzer NR, et al. ACC/AHA 2005 Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation 2006; 113(11): e463-654.
4. Forrester JS, Price MJ, Makkar RR. Stem cell repair of infarcted myocardium: an overview for clinicians. Circulation 2003; 108(9): 1139-45.
5. Zimmermann WH, Didie M, Doker S, et al. Heart muscle engineering: an update on cardiac muscle replacement therapy. Cardiovasc Res 2006; 71(3): 419-29.
6. Sharma R, Raghubir R: Stem cell therapy: a hope for dying hearts. Stem Cells Dev 2007; 16(4): 517-36.
7. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391): 1145-7.
8. Moore KE, Mills JF, Thornton MM. Alternative sources of adult stem cells: a possible solution to the embryonic stem cell debate. Gend Med 2006; 3(3): 161-68.
9. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7(2): 211-28.
10. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131(5): 861-72.
11. Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans. Science 2009; 324(5923): 98-102.
12. Nadal-Ginard B, Ellison GM, Torella D. The cardiac stem cell compartment is indispensable for myocardial cell homeostasis, repair and regeneration in the adult. Stem Cell Res 2014.
13. Goumans MJ, de Boer TP, Smits AM, et al. TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res 2007; 1(2): 138-49.
14. Smits AM, van Laake LW, den Ouden K, et al. Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc Res 2009; 83(3): 527-35.
15. Servick K. Top heart lab comes under fire. Science 2014; 345(6194): 254.
16. Couzin-Frankel J. The elusive heart fix. Science 2014; 345(6194): 252-7.
17. van Berlo JH, Kanisicak O, Maillet M, et al. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 2014; 509(7500): 337-41.
18. Smart N, Bollini S, Dube KN, et al. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011; 474(7353): 640-4.
19. Dey D, Han L, Bauer M, et al. Dissecting the molecular relationship among various cardiogenic progenitor cells. Circ Res 2013; 112(9): 1253-62.
20. Gaetani R, Feyen DA, Doevendans P, et al. Different types of cultured human adult Cardiac Progenitor Cells have a high degree of transcriptome similarity. J Mol Cell Cardiol 2014, in press.
21. Rickard DJ, Kassem M, Hefferan TE, Sarkar G, Spelsberg TC, Riggs BL. Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 1996; 11(3): 312-24.
22. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284(5411): 143-7.
23. Madonna R, Geng YJ, De Caterina R. Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair. Arterioscler Thromb Vasc Biol 2009; 29(11): 1723-29.
24. Rohani L, Johnson AA, Arnold A, Stolzing A. The aging signature: a hallmark of induced pluripotent stem cells? Aging Cell 2014; 13(1): 2-7.
25. Wang B, Miyagoe-Suzuki Y, Yada E, et al. Reprogramming efficiency and quality of induced Pluripotent Stem Cells (iPSCs) generated from muscle-derived fibroblasts of mdx mice at different ages. PLoS Curr 2011; 3: RRN1274.
26. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003; 108(4): 457-63.
27. Wu KH, Mo XM, Han ZC, Zhou B. Stem cell engraftment and survival in the ischemic heart. Ann Thorac Surg 2011; 92(5): 1917- 25.
28. Pavo N, Charwat S, Nyolczas N, et al. Critical review and summary of the clinical experiences. J Mol Cell Cardiol 2014; 75C: 12- 24.
29. Go AS, Mozaffarian D, Roger VL, et al. Heart disease and stroke statistics--2014 update: a report from the American Heart Association. Circulation 2014; 129(3): e28-e292.
30. Madonna R, De Caterina R. Cellular and molecular mechanisms of vascular injury in diabetes--part II: cellular mechanisms and therapeutic targets. Vascul Pharmacol 2011; 54(3-6): 75-9.
31. Zenovich AG, Taylor DA. Atherosclerosis as a disease of failed endogenous repair. Front Biosci 2008; 13: 3621-36.
32. Park JA, Kwon YG. Could circulating progenitor cell count be a barometer for coronary artery disease progression? Circ J 2010; 74(9): 1804-5.
33. Werner N, Kosiol S, Schiegl T, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353(10): 999-1007.
34. Trensz F, Haroun S, Cloutier A, Richter MV, Grenier G. A muscle resident cell population promotes fibrosis in hindlimb skeletal muscles of mdx mice through the Wnt canonical pathway. Am J Physiol Cell Physiol 2010; 299(5): C939-47.
35. Brack AS, Conboy MJ, Roy S, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007; 317(5839): 807-10.
36. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005; 433(7027): 760-4.
37. Rando TA, Chang HY. Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 2012; 148(1-2): 46-57.
38. Porrello ER, Mahmoud AI, Simpson E, et al. Transient regenerative potential of the neonatal mouse heart. Science 2011; 331(6020): 1078-80.
39. Andersen DC, Ganesalingam S, Jensen CH, Sheikh SP. Do Neonatal Mouse Hearts Regenerate following Heart Apex Resection? Stem Cell Reports 2014; 2(4): 406-13.
40. Don CW, Murry CE. Improving survival and efficacy of pluripotent stem cell-derived cardiac grafts. J Cell Mol Med 2013; 17(11): 1355-62.
41. Gorbe A, Giricz Z, Szunyog A, Csont T, Burley DS, Baxter GF, Ferdinandy P. Role of cGMP-PKG signaling in the protection of neonatal rat cardiac myocytes subjected to simulated ischemia/ reoxygenation. Basic Res Cardiol 2010; 105(5): 643-50.
42. Gorbe A, Varga ZV, Paloczi J, et al.Cytoprotection by the NOdonor SNAP against ischemia/reoxygenation injury in mouse embryonic stem cell-derived cardiomyocytes. Mol Biotechnol 2014; 56(3): 258-64.
43. Madonna R, Renna FV, Cellini C, et al. Age-dependent impairment of number and angiogenic potential of adipose tissue-derived progenitor cells. Eur J Clin Invest 2011; 41(2): 126-33.
44. Madonna R, Geng YJ, Shelat H, Ferdinandy P, De Caterina R. High glucose-induced hyperosmolarity impacts proliferation, cytoskeleton remodeling and migration of human induced pluripotent stem cells via aquaporin-1. 2014; 1842(11): 2266-75.
45. Ferdinandy P, Schulz R, Baxter GF. Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 2007; 59(4): 418-58.
46. Ferdinandy P, Hausenloy D, Heusch G, Baxter GF, Schulz R. Interaction of risk factors, comorbidities and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 2014; 66(4): 1142-74.
47. Sluijter JP, Condorelli G, Davidson SM, et al. Novel therapeutic strategies for cardioprotection. Pharmacol Ther 2014; 144(1): 60- 70.
48. Madonna R, Taylor DA, Geng YJ, et al. Transplantation of mesenchymal cells rejuvenated by the overexpression of telomerase and myocardin promotes revascularization and tissue repair in a murine model of hindlimb ischemia. Circ Res 2013; 113(7): 902-14.
49. Sinha M, Jang YC, Oh J, et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014; 344(6184): 649-52.
50. Fischer KM, Cottage CT, Wu W, et al. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation 2009; 120: 2077-87.
51. Mohsin S, Khan M, Nguyen J, et al. Rejuvenation of human cardiac progenitor cells with Pim-1 kinase. Circ Res 2013; 113(10): 1169-79.
52. Choudhery MS, Khan M, Mahmood R, et al. Mesenchymal stem cells conditioned with glucose depletion augments their ability to repair-infarcted myocardium. J Cell Mol Med 2012; 16(10): 2518- 29.
53. Zippo A, De Robertis A, Bardelli M, Galvagni F, Oliviero S. Identification of Flk-1 target genes in vasculogenesis: Pim-1 is required for endothelial and mural cell differentiation in vitro. Blood 2004; 103(12): 4536-44.
54. Borillo GA, Mason M, Quijada P, et al. Pim-1 kinase protects mitochondrial integrity in cardiomyocytes. Circ Res 2010; 106(7): 1265-74.
55. Yan B, Zemskova M, Holder S, et al. The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death. J Biol Chem 2003; 278(46): 45358-67.
56. Mohsin S, Khan M, Toko H, et al. Human cardiac progenitor cells engineered with Pim-I kinase enhance myocardial repair. J Am Coll Cardiol 2012; 60(14): 1278-87.
57. Carlson ME, Suetta C, Conboy MJ, et al. Molecular aging and rejuvenation of human muscle stem cells. EMBO Mol Med 2009; 1(8-9): 381-91.
58. Zhao C, Guo H, Li J, et al. Numb family proteins are essential for cardiac morphogenesis and progenitor differentiation. Development 2014; 141(2): 281-95.
59. Nemir M, Metrich M, Plaisance I, et al. The Notch pathway controls fibrotic and regenerative repair in the adult heart. Eur Heart J 2014; 35(32): 2174-85.
60. Yang J, Bucker S, Jungblut B, et al. Inhibition of Notch2 by Numb/Numblike controls myocardial compaction in the heart. Cardiovasc Res 2012; 96(2): 276-285.
61. Zhao L, Borikova AL, Ben-Yair R, et al. Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci USA 2014, 111(4): 1403-08.
62. Bodnar AG, Ouellette M, Frolkis M, et al. Extension of life-span by introduction of telomerase into normal human cells. Science 1998; 279(5349): 349-52.
63. Brandt S: TERT over-expression affects the growth of myocardial tissue derived from mouse embryonic stem cells. Differentiation 2010; 79(1): 1-8.
64. Wong LS, Oeseburg H, de Boer RA, van Gilst WH, van Veldhuisen DJ, van der Harst P. Telomere biology in cardiovascular disease: the TERC-/- mouse as a model for heart failure and ageing. Cardiovasc Res 2009; 81(2): 244-52.
65. Jan HM, Wei MF, Peng CL, Lin SJ, Lai PS, Shieh MJ. The use of polyethylenimine-DNA to topically deliver hTERT to promote hair growth. Gene Ther 2011; 19(1): 86-93.
66. Qu Y, Duan Z, Zhao F, et al. Telomerase reverse transcriptase upregulation attenuates astrocyte proliferation and promotes neuronal survival in the hypoxic-ischemic rat brain. Stroke 2011; 42(12): 3542-50.
67. Madonna R, Willerson JT, Geng YJ. Myocardin a enhances telomerase activities in adipose tissue mesenchymal cells and embryonic stem cells undergoing cardiovascular myogenic differentiation. Stem Cells 2008; 26(1): 202-11.
68. Madonna R, Wu D, Wassler M, De Caterina R, Willerson JT, Geng YJ. Myocardin-A enhances expression of promyogenic genes without depressing telomerase activity in adipose tissue-derived mesenchymal stem cells. Int J Cardiol 2012; 167(6): 2912-21.
69. Madonna R, Geng YJ, Bolli R, et al. Co-Activation of Nuclear Factor-kappaB and Myocardin/Serum Response Factor Conveys the Hypertrophy Signal of High Insulin Levels in Cardiac Myoblasts. J Biol Chem 2014; 289(28): 19585-98.
70. Ueyama T, Kasahara H, Ishiwata T, Nie Q, Izumo S. Myocardin expression is regulated by Nkx2.5, and its function is required for cardiomyogenesis. Mol Cell Biol 2003; 23(24): 9222-32.
71. Wang Z, Wang DZ, Pipes GC, Olson EN. Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci USA 2003; 100(12): 7129-34.
72. Cao XL, Hu XM, Hu JQ, Zheng WX. Myocardin-related transcription factor-A promoting neuronal survival against apoptosis induced by hypoxia/ischemia. Brain Res 2011; 1385: 263-74.
73. Huang J, Min Lu M, Cheng L, et al. Myocardin is required for cardiomyocyte survival and maintenance of heart function. Proc Natl Acad Sci USA 2009; 106(44): 18734-9.
74. Miranville A, Heeschen C, Sengenes C, Curat CA, Busse R, Bouloumie A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 2004; 110(3): 349- 55.
75. Fraser JK, Schreiber R, Strem B, et al. Plasticity of human adipose stem cells toward endothelial cells and cardiomyocytes. Nat Clin Pract Cardiovasc Med 2006; 3 Suppl 1: S33-37.
76. Gaustad KG, Boquest AC, Anderson BE, Gerdes AM, Collas P. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes. Biochem Biophys Res Commun 2004; 314(2): 420-7.
77. Traktuev DO, Merfeld-Clauss S, Li J, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008; 102(1): 77-85.
78. Madonna R, De Caterina R, Willerson JT, Geng YJ. Biologic function and clinical potential of telomerase and associated proteins in cardiovascular tissue repair and regeneration. Eur Heart J 2011; 32(10): 1190-6.
79. Cho HC, Marban E. Biological therapies for cardiac arrhythmias: can genes and cells replace drugs and devices? Circ Res 2010; 106: 674-85.
80. Gansbacher B, Report of a second serious adverse event in a clinical trial of gene therapy for X-linked severe combined immune deficiency (X-SCID). Position of the European Society of Gene Therapy (ESGT). J Gene Med 2003; 5: 261-2.
81. Sluijter JP, van Mil A, van Vliet P, et al. MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells. Arterioscler Thromb Vasc Biol 2010; 30(4): 859-68.
82. Hosoda T, Zheng H, Cabral-da-Silva M, et al. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 2011; 123(12): 1287-96.
83. Rando TA, Wyss-Coray T. Stem cells as vehicles for youthful regeneration of aged tissues. J Gerontol A Biol Sci Med Sci 2014; 69 Suppl 1: S39-42.
84. Siddiqi S, Sussman MA. Cell and gene therapy for severe heart failure patients: the time and place for Pim-1 kinase. Expert Rev Cardiovasc Ther 2013; 11(8): 949-57.
85. Feyen D, Gaetani R, Liu J, et al. Increasing short-term cardiomyocyte progenitor cell (CMPC) survival by necrostatin-1 did not further preserve cardiac function. Cardiovasc Res 2013; 99(1): 83-91.
86. Gaetani R, Doevendans PA, Metz CH, et al. Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. Biomaterials 2012; 33(6): 1782-90.
87. Gaetani R, Rizzitelli G, Chimenti I, et al. Cardiospheres and tissue engineering for myocardial regeneration: potential for clinical application. J Cell Mol Med 2010; 14(5): 1071-7.
88. Patra C, Boccaccini A, Engel F. Vascularisation for cardiac tissue engineering: the extracellular matrix. Thromb Haemost 2014; 113(1).