Aging of Stem and Progenitor Cells: Mechanisms, Impact on Therapeutic Potential, and Rejuvenation

Rejuvenation Research

Volumn 19, Issue 1, 2016, Pages 3-12

  Nurkovic, Jasmin ^a   Volarevic, Vladislav ^b   Lako, Majlinda ^c   Armstrong, Lyle ^c   Arsenijevic, Nebojsa ^b   Stojkovic, Miodrag ^b,d  

^a State University of Novi Pazar   (Serbia)

^b University of Kragujevac Medical Faculty   (Serbia)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d Spebo Medical ^*  (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ARF PROTEIN; CARBONYL DERIVATIVE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; LIPOFUSCIN; REACTIVE OXYGEN METABOLITE; TELOMERASE;

ARTICLE; CELL AGING; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; COLONY FORMING UNIT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; EMBRYONIC STEM CELL; ENZYME ACTIVITY; EPIGENETICS; GENE LOCUS; HUMAN; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MECHANICS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL AGING; TELOMERE SHORTENING; CYTOLOGY; REJUVENATION; STEM CELL TRANSPLANTATION;

CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; REJUVENATION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84958959610     PISSN: 15491684     EISSN: 15578577     Source Type: Journal    
DOI: 10.1089/rej.2015.1676     Document Type: Article

References (94)

1. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res 1961;25:585-621.
2. Medvedev ZA. An attempt at a rational classification of theories of ageing. Biol Rev Camb Philos Soc 1990;65: 375-398.
3. Kirkwood TB. Understanding the odd science of aging. Cell 2005;120:437-447.
4. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest 2004;113:160-168.
5. Blasco MA. Telomeres and human disease: Ageing, cancer and beyond. Nat Rev Genet 2005;6:611-622.
6. Campisi J. Senescent cells, tumor suppression, and organismal aging: Good citizens, bad neighbors. Cell 2005;120:513-522.
7. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci 2002;27:339-344.
8. Lansdorp PM. Telomeres and disease. EMBO J 2009;28: 2532-2540.
9. Tümpel S, Rudolph KL. The role of telomere shortening in somatic stem cells and tissue aging: Lessons from telomerase model systems. Ann NY Acad Sci 2012;1266:28-39.
10. O'Connor MS, Carlson ME, Conboy IM. Differentiation rather than aging of muscle stem cells abolishes their telomerase activity. Biotechnol Prog 2009;25:1130-1137.
11. Signer RA, Morrison SJ. Mechanisms that regulate stem cell aging and life span. Cell Stem Cell 2013;12:152-165.
12. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE, ScaddenDT. Stem cell ageingmodified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006;443:421-426.
13. Liu Y, Sanoff HK, Cho H, Burd CE, Torrice C, Ibrahim JG, Thomas NE, Sharpless NE. Expression of p16INK4a in peripheral blood T-cells is a biomarker of human aging. Aging Cell 2009;8:439-448.
14. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 2003; 5:741-747.
15. Hasty P, Campisi J, Hoeijmakers J, van Steeg H, Vijg J. Aging and genome maintenance: Lessons from the mouse? Science 2003;299:1355-1359.
16. Cousin W, Ho ML, Desai R, Tham A, Chen RY, Kung S, Elabd C, Conboy IM. Regenerative capacity of old muscle stem cells declines without significant accumulation of DNA damage. PLoS One 2013;8:e63528.
17. Beerman I, Seita J, Inlay MA, Weissman IL, Rossi DJ. Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 2014;15:37-50.
18. Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med 2009;361:1475-1485.
19. Feng Q, Lu SJ, Klimanskaya I, Gomes I, Kim D, Chung Y, Honig GR, Kim KS, Lanza R. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 2010;28:704-712.
20. Fraga MF, Esteller M. Epigenetics and aging: The targets and the marks. Trends Genet 2007;23:413-418.
21. Armstrong L, Al-Aama J, Stojkovic M, Lako M. Concise review: The epigenetic contribution to stem cell ageing: Can we rejuvenate our older cells? Stem Cells 2014;32:2291-2298.
22. Issa JP. Age-related epigenetic changes and the immune system. Clin Immunol 2003;109:103-108.
23. Oakes CC, Smiraglia DJ, Plass C, Trasler JM, Robaire B. Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc Natl Acad Sci USA. 2003;100:1775-1780.
24. Cadinanos J, Varela I, López-Otín C, Freije JM. From immature lamin to premature aging: Molecular pathways and therapeutic opportunities. Cell Cycle 2005;4:1732-1735.
25. Sasaki, T, Maier B, Bartke A, Scrable H. Progressive loss of SIRT1with cell cycle withdrawal.Aging Cell 2006;5:413-422.
26. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004;23:2369-2380.
27. Bosch-Presegué L, Vaquero A. The dual role of sirtuins in cancer. Genes Cancer 2011;2:648-662.
28. Yuan HF, Zhai C, Yan XL, Zhao DD, Wang JX, Zeng Q, Chen L, Nan X, He LJ, Li ST, Yue W, Pei XT. SIRT1 is required for long-term growth of human mesenchymal stem cells. J Mol Med 2012;90:389-400.
29. Chen H, Liu X, Chen H, Cao J, Zhang L, Hu X, Wang J. Role of SIRT1 and AMPK in mesenchymal stem cells differentiation. Ageing Res Rev 2014;13:55-64.
30. Harman D. Aging: A theory based on free radical and radiation chemistry. J. Gerontol. 1956;11:298-300.
31. Wallace DC. Mitochondrial diseases in man and mouse. Science 1999;283:1482-1488.
32. Brierley EJ, Johnson MA, Lightowlers RN, James OF, Turnbull DM. Role of mitochondrial DNA mutations in human aging: Implications for the central nervous system and muscle. Ann Neurol 1998;43:217-223.
33. CottrellDA, Ince PG, Blakely EL, JohnsonMA, Chinnery PF, Hanna M, Turnbull DM. Neuropathological and histochemical changes in a multiple mitochondrial DNA deletion disorder. J Neuropathol Exp Neurol 2000;59:621-627.
34. Barazzoni R, Short KR, Nair KS. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J Biol Chem 2000;275:3343-3347.
35. Taylor RW, Barron MJ, Borthwick GM, Gospel A, Chinnery PF, Samuels DC, Taylor GA, Plusa SM, Needham SJ, Greaves LC. Mitochondrial DNA mutations in human colonic crypt stem cells. J Clin Invest 2003;112:1351-1360.
36. Oh J, Lee YD, Wagers AJ. Stem cell aging: Mechanisms, regulators and therapeutic opportunities. Nat Med 2014;20:870-880.
37. Siddiqui S, Fang M, Ni B, Lu D, Martin B, Maudsley S. Central role of the EGF receptor in neurometabolic aging. Int J Endocrinol 2012;2012:739428.
38. Silva H, Carboy IM. Aging and stem cell renewal ( January 16, 2009). In: StemBook. Harvard Stem Cell Institute, The Stem Cell Research Community, StemBook. Available at www.stembook.org
39. Carlson ME, Suetta C, Conboy MJ, Aagaard P, Mackey A, Kjaer M, Conboy I. Molecular aging and rejuvenation of human muscle stem cells. EMBOMol Med 2009;1:381-391.
40. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, Mikels AJ, Agrawal S, Schaffer DV, Conboy IM. Relative roles of TGF-b1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 2009;8:676-689.
41. Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 2000;908:244-254.
42. de Magalhaes JP, Curado J, Church GM. Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 2009;25:875-881.
43. Coppé JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: The dark side of tumor suppression. Annu Rev Pathol 2010;5:99-118.
44. Conboy IM,Conboy MJ,WagersAJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005;433:760-764.
45. Wagner W, Bork S, Lepperdigner G, Joussen S, Ma N, Strunk D, Koch C. How to track cellular aging of mesenchimal stromal cells? Aging 2010;2:224-230.
46. Xie X, Hiona A, Lee AS, Cao F, Huang M, Li Z, Cherry A, Pei XT, Wu JC. Effects of long term culture on human embryonic stem cell aging. Stem Cells Dev 2011;20:127-138.
47. Lee BY, Han JA, Im JS,Morrone A, Johung K, Goodwin EC, Kleijer WJ, DiMaio D, Hwang ES. Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 2006;5:187-195.
48. Schallmoser K, Bartmann C, Rohde E, Bork S, Guelly C, ObenaufA. C, ReinischA,Horn P,HoAD, Strunk D,Wagner W. Replicative senescence-associated gene expression changes in mesenchymal stromal cells are similar under different culture conditions. Haematologica 2010;95:867-874.
49. Castilho RM, Squarize CH, Chodosh LA, Williams BO, Gutkind JS. mTOR mediates Wnt-induced epidermal stem cell exhaustion and aging. Cell Stem Cell 2009;5:279-289.
50. Scholz JL, Diaz A, Riley RL, Cancro MP, Frasca D. A comparative review of aging and B cell function in mice and humans. Curr Opin Immunol 2013;25:504-510.
51. Heinbokel T, Elkhal A, Liu G, Edtinger K, Tullius SG. Immunosenescence and organ transplantation. Transplant Rev (Orlando) 2013;27:65-75.
52. Katsimpardi L, Litterman NK, Schein PA, Miller CM, Loffredo FS, Wojtkiewicz GR, Chen JW, Lee RT, Wagers AJ, Rubin LL. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 2014;344:630-634.
53. Segers VF, Lee RT. Biomaterials to enhance stem cell function in the heart. Circ Res 2011;109:910-922.
54. Chinnadurai R, Copland IB, Patel SR, Galipeau J. IDOindependent suppression of T cell effector function by IFNc-licensed human mesenchymal stromal cells. J Immunol 2014;192:1491-1501.
55. Seeger FH, Zeiher AM, Dimmeler S. MicroRNAs in stem cell function and regenerative therapy of the heart. Arterioscler Thromb Vasc Biol 2013;33:1739-1746.
56. Yang C, Przyborski S, Cooke MJ, Zhang X, Stewart R, Anyfantis G, Atkinson SP, Saretzki G, Armstrong L, Lako M. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 2008;26:850-863.
57. Hwang ES. Senescence suppressors: Their practical importance in replicative lifespan extension in stem cells. Cell Mol Life Sci 2014;71:4207-4219.
58. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br J Haematol 2003;121:368-374.
59. Siegel G, Kluba T, Hermanutz-Klein U, Bieback K, Northoff H, Schäfer R. Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Med 2013;11:146.
60. Alt EU, Senst C, Murthy SN, Slakey DP, Dupin CL, Chaffin AE, Kadowitz PJ, Izadpanah R. Aging alters tissue resident mesenchymal stem cell properties. Stem Cell Res 2012;8:215-225.
61. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol 2006;7:1-7.
62. Yew T, Chiu F, Tsai C, Chen H, Lee W, Chen YJ, Chang MC, Hung SC. Knockdown of p21Cip1/Waf1 enhances proliferation, the expression of stemness markers, and osteogenic potential in human mesenchymal stem cells. Aging Cell 2011;10:1-13.
63. Rubin H. The disparity between human cell senescence in vitro and lifelong replication in vivo. Nat Biotechnol 2002;20:675-681.
64. Rubin H. Cell aging in vivo and in vitro. Mech Ageing Dev1997;98:1-35.
65. Cameron IL. Minimum number of cell doublings in an epithelial cell population during the lifespan of the mouse. J Gerontol 1972;27:157-161.
66. Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: Consequences for cell therapies. Mech Ageing Dev 2008;129:163-173.
67. Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003;33:919-926.
68. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004;22:675-682.
69. Geißler S, Textor M, Kühnisch J, Könnig D, Klein O, Ode A, Pfitzner T, Adjaye J, Kasper G, Duda GN. Functional comparison of chronological and in vitro aging: Differential role of the cytoskeleton and mitochondria in mesenchymal stromal cells. PLoS One 2012;7:e52700.
70. Carlson ME, Conboy IM. Loss of stem cell regenerative capacity within aged niches. Aging Cell 2007;6:371-382.
71. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Després S, Aigner L, Li G, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function.Nature 2011;477:90-94.
72. Baker N, Boyette LB, Tuan RS. Characterization of bone marrow-derived mesenchymal stem cells in aging. Bone 2015;70:37-47.
73. Huang K, Zhou DH, Huang SL, Liang SH. Age-related biological characteristics of human bone marrow mesenchymal stem cells from different age donors. J Exp Hematol 2005;13:1049-1053.
74. Mareschi K, Ferrero I, Rustichelli D, Aschero S, Gammaitoni L, Aglietta M, Madon E, Fagioli F. Expansion of mesenchymal stem cells isolated from paediatric and adult donor bone marrow. J Cell Biochem 2006;97:744-754.
75. Schipper BM, Marra KG, Zhang W, Donnenberg AD, Rubin JP. Regional anatomic and age effects on cell function of human adipose-derived stem cells. Ann Plast Surg 2008;60:538-544.
76. Nayan M, Paul A, Chen G, Chiu RC, Prakash S, Shum-Tim D. Superior therapeutic potential of young bone marrow mesenchymal stem cells by direct intramyocardial delivery in aged recipients with acute myocardial infarction: In vitro and in vivo investigation. J Tissue Eng 2011;2011:741213.
77. Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res 2008;102:1319-1330.
78. Scheubel RJ, Zorn H, Silber RE, Kuss O, Morawietz H, Holtz J, Simm A. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol 2003;42:2073-2080.
79. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 2014;12:8.
80. Volarevic V, Ljujic B, Stojkovic P, Lukic A, Arsenijevic N, Stojkovic M. Human stem cell research and regenerative medicine-present and future. Br Med Bull 2011;99:155-168.
81. Lapasset L, Milhavet O, Prieur A, Besnard E, Babled A, Aït-Hamou N, Leschik J, Pellestor F, Ramirez JM, De Vos J, Lehmann S, Lemaitre JM. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev 2011;25:2248-2253.
82. Armstrong L, Tilgner K, Saretzki G, Atkinson SP, Stojkovic M, Moreno R, Przyborski S, Lako M. Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells 2010;28:661-673.
83. Rohani L, Johnson AA, Arnold A, Stolzing A. The aging signature: A hallmark of induced pluripotent stem cells? Aging Cell 2014;13:2-7.
84. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA, Ramalho-Santos J, Van Houten B, Schatten G. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011;6:e20914.
85. Lako M, Armstrong L, Stojkovic M. Induced pluripotent stem cells: It looks simple but can looks deceive? Stem Cells 2010;28:845-850.
86. Neganova I, Vilella F, Atkinson SP, Lloret M, Passos JF, von Zglinicki T, O'Connor JE, Burks D, Jones R, Armstrong L, Lako M. An important role for CDK2 in G1 to S checkpoint activation and DNA damage response in human embryonic stem cells. Stem Cells 2011;29:651-659.
87. Cha J, Falanga V. Stem cells in cutaneous wound healing. Clin Dermatol 2007;25:73-78.
88. Liu L, Rando TA. Manifestations and mechanisms of stem cell aging. J Cell Biol 2011;193:257-266.
89. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM. Clearance of p16Ink4a-positive senescent cells delays ageingassociated disorders. Nature 2011;479:232-236.
90. Ibarretxe G, Alvarez A, Canãvate ML, Hilario E, Aurrekoetxea M, Unda F. Cell reprogramming, IPS limitations, and overcoming strategies in dental bioengineering. Stem Cells Int 2012;2012:365932.
91. Kim JS, ChoiHW, Choi S, Do JT. Reprogrammed pluripotent stem cells from somatic cells. Int J Stem Cells. 2011;4:1-8.
92. Weidner CI, Lin Q, Koch CM, Eisele L, Beier F, Ziegler P, Bauerschlag DO, Jöckel KH, Erbel R, Mühleisen TW, Zenke M, Brümmendorf TH, Wagner W. Aging of blood can be tracked by DNA methylation changes at just three CpG sites. Genome Biol 2014;15:R24.
93. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol 2014;14:R115.
94. Wahlestedt M, Pronk CJ, Bryder D. Concise review: Hematopoietic stem cell aging and the prospects for rejuvenation. Stem Cells Transl Med 2015;4:1-9.