Anti-Aging Strategies Based on Cellular Reprogramming

Trends in Molecular Medicine

Volumn 22, Issue 8, 2016, Pages 725-738

  Ocampo, Alejandro ^a   Reddy, Pradeep ^a   Belmonte, Juan Carlos Izpisua ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

aging; epigenetics; rejuvenation; reprogramming

Indexed keywords

CELL AGING; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; DYSKERATOSIS CONGENITA; EPIGENETICS; GENE EXPRESSION; GENOMIC INSTABILITY; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NESTOR GUILLERMO PROGERIA SYNDROME; NONHUMAN; NUCLEAR REPROGRAMMING; PREMATURE AGING; PROGERIA; REVIEW; SENESCENCE; SOMATIC CELL; TELOMERE LENGTH; TELOMERE SHORTENING; WERNER SYNDROME; AGING; AGING, PREMATURE; ANIMAL; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PATHOLOGY; REGENERATIVE MEDICINE;

AGING; AGING, PREMATURE; ANIMALS; CELL AGING; CELLULAR REPROGRAMMING; EPIGENESIS, GENETIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; REGENERATIVE MEDICINE;

EID: 84978827225     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2016.06.005     Document Type: Review

References (93)

1. 1 Kirkwood, T.B.L., Understanding the odd science of aging. Cell 120 (2005), 437–447.
2. 2 López-Otín, C., et al. The hallmarks of aging. Cell 153 (2013), 1194–1217.
3. 3 Haigis, M.C., Sinclair, D.A., Mammalian sirtuins: biological insights and disease relevance. Annu. Rev. Pathol 5 (2010), 253–295.
4. 4 Kapahi, P., et al. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 14 (2004), 885–890.
5. 5 Kimura, K.D., daf-2, an insulin Receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277 (1997), 942–946.
6. 6 Conboy, I.M., et al. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433 (2005), 760–764.
7. 7 Conboy, M.J., et al. Heterochronic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging Cell 12 (2013), 525–530.
8. 8 Conboy, I.M., Notch-mediated restoration of regenerative potential to aged muscle. Science 302 (2003), 1575–1577.
9. 9 Carlson, M.E., et al. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454 (2008), 528–532.
10. 10 Brack, A.S., et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317 (2007), 807–810.
11. 11 Loffredo, F.S., et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 153 (2013), 828–839.
12. 12 Sinha, M., et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344 (2014), 649–652.
13. 13 Katsimpardi, L., et al. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 344 (2014), 630–634.
14. 14 Egerman, M.A., et al. GDF11 increases with age and inhibits skeletal muscle regeneration. Cell Metab. 22 (2015), 164–174.
15. 15 Hinken, A.C., et al. Lack of evidence for GDF11 as a rejuvenator of aged skeletal muscle satellite cells. Aging Cell 15 (2016), 582–584.
16. 16 Gurdon, J.B., Adult frogs derived from the nuclei of single somatic cells. Dev. Biol. 4 (1962), 256–273.
17. 17 Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
18. 18 Mahmoudi, S., Brunet, A., Aging and reprogramming: a two-way street. Curr. Opin. Cell Biol. 24 (2012), 744–756.
19. 19 Pollina, E.A., Brunet, A., Epigenetic regulation of aging stem cells. Oncogene 30 (2011), 3105–3126.
20. 20 Benayoun, B.A., et al. Epigenetic regulation of ageing: linking environmental inputs to genomic stability. Nat. Rev. Mol. Cell Biol. 16 (2015), 593–610.
21. 21 Fraga, M.F., Esteller, M., Epigenetics and aging: the targets and the marks. Trends Genet. 23 (2007), 413–418.
22. 22 Han, S., Brunet, A., Histone methylation makes its mark on longevity. Trends Cell Biol. 22 (2012), 42–49.
23. 23 Horvath, S., DNA methylation age of human tissues and cell types. Genome Biol., 14, 2013, R115.
24. 24 Shumaker, D.K., et al. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. U.S.A. 103 (2006), 8703–8708.
25. 25 Liu, G-H., et al. Recapitulation of premature ageing with iPSCs from Hutchinson–Gilford progeria syndrome. Nature 472 (2011), 221–225.
26. 26 Greer, E.L., et al. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466 (2010), 383–387.
27. 27 Guarente, L., Sirtuins, aging, and metabolism. Cold Spring Harb. Symp. Quant. Biol. 76 (2011), 81–90.
28. 28 Krishnan, V., et al. Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc. Nat.l Acad. Sci. 108 (2011), 12325–12330.
29. 29 Peleg, S., et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328 (2010), 753–756.
30. 30 Blasco, M.A., The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8 (2007), 299–309.
31. 31 Issa, J-P., Aging and epigenetic drift: a vicious cycle. J. Clin. Invest. 124 (2014), 24–29.
32. 32 Lapasset, L., et al. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes. Dev. 25 (2011), 2248–2253.
33. 33 Yagi, T., et al. Establishment of induced pluripotent stem cells from centenarians for neurodegenerative disease research. PLoS ONE, 7, 2012, e41572.
34. 34 Marion, R.M., et al. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4 (2009), 141–154.
35. 35 Prigione, A., et al. Mitochondrial-associated cell death mechanisms are reset to an embryonic-like state in aged donor-derived iPS Cells harboring chromosomal aberrations. PLoS ONE, 6, 2011, e27352.
36. 36 Suhr, S.T., et al. Mitochondrial rejuvenation after induced pluripotency. PLoS ONE, 5, 2010, e14095.
37. 37 Suhr, S.T., et al. Telomere dynamics in human cells reprogrammed to pluripotency. PLoS ONE, 4, 2009, e8124.
38. 38 Zhang, J., et al. A human iPSC model of Hutchinson Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8 (2011), 31–45.
39. 39 Zhang, W., et al. A Werner syndrome stem cell model unveils heterochromatin alterations as a driver of human aging. Science 348 (2015), 1160–1163.
40. 40 Shimamoto, A., et al. Reprogramming suppresses premature senescence phenotypes of werner syndrome cells and maintains chromosomal stability over long-term culture. PLoS ONE, 9, 2014, e112900.
41. 41 Cheung, H-H., et al. Telomerase protects Werner syndrome lineage-specific stem cells from premature aging. Stem Cell Reports 2 (2014), 534–546.
42. 42 Agarwal, S., et al. Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients. Nature 464 (2010), 292–296.
43. 43 Batista, L.F.Z., et al. Telomere shortening and loss of self-renewal in dyskeratosis congenita induced pluripotent stem cells. Nature 474 (2011), 399–402.
44. 44 Soria-Valles, C., et al. NF-κB activation impairs somatic cell reprogramming in ageing. Nat. Cell Biol. 17 (2015), 1004–1013.
45. 45 Wakayama, S., et al. Successful serial recloning in the mouse over multiple generations. Cell Stem Cell 12 (2013), 293–297.
46. 46 Rando, T.A., Chang, H.Y., Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148 (2012), 46–57.
47. 47 Buganim, Y., et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150 (2012), 1209–1222.
48. 48 Polo, J.M., et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151 (2012), 1617–1632.
49. 49 Hansson, J., et al. Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency. Cell Rep. 2 (2012), 1579–1592.
50. 50 Kurian, L., et al. Conversion of human fibroblasts to angioblast-like progenitor cells. Nat. Meth. 10 (2013), 77–83.
51. 51 Mertens, J., et al. Directly reprogrammed himan neurons retain aging-associated transcriptomic signatures and reveal age-related nucleocytoplasmic defects. Cell Stem Cell 17 (2015), 705–718.
52. 52 Trounson, A., McDonald, C., Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell 17 (2015), 11–22.
53. 53 Liu, L., Rando, T.A., Manifestations and mechanisms of stem cell aging. J. Cell Biol. 193 (2011), 257–266.
54. 54 Oh, J., et al. Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat. Med. 20 (2014), 870–880.
55. 55 Abad, M., et al. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502 (2013), 340–345.
56. 56 Ohnishi, K., et al. Premature termination of reprogramming in vivo leads to cancer development through altered epigenetic regulation. Cell 156 (2014), 663–677.
57. 57 Hochedlinger, K., et al. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121 (2005), 465–477.
58. 58 Hou, P., et al. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341 (2013), 651–654.
59. 59 Eriksson, M., et al. Recurrent de novo point mutations in lamin A cause Hutchinson–Gilford progeria syndrome. Nature 423 (2003), 293–298.
60. 60 Muchir, A., et al. Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery–Dreifuss muscular dystrophy. J Clin Invest 117 (2007), 1282–1293.
61. 61 Goldman, R.D., et al. Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson–Gilford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 8963–8968.
62. 62 Hennekam, R.C.M., Hutchinson–Gilford progeria syndrome: review of the phenotype. Am. J. Med. Genet. 140 (2006), 2603–2624.
63. 63 Varela, I., et al. Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature 437 (2005), 564–568.
64. 64 Osorio, F.G., et al. Splicing-directed therapy in a new mouse model of human accelerated aging. Sci. Transl. Med., 3, 2011, 106ra107.
65. 65 Yu, C.E., et al. Positional cloning of the Werner's syndrome gene. Science 272 (1996), 258–262.
66. 66 Kudlow, B.A., et al. Werner and Hutchinson–Gilford progeria syndromes: mechanistic basis of human progeroid diseases. Nat. Rev. Mol. Cell Biol. 8 (2007), 394–404.
67. 67 Martínez, P., Blasco, M.A., Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins. Nat. Rev. Cancer 11 (2011), 161–176.
68. 68 Stanley, S.E., Armanios, M., The short and long telomere syndromes: paired paradigms for molecular medicine. Curr. Opin. Genet. Dev. 33 (2015), 1–9.
69. 69 Cabanillas, R., et al. Néstor–Guillermo progeria syndrome: a novel premature aging condition with early onset and chronic development caused by BANF1 mutations. Am. J. Med. Genet. 155 (2011), 2617–2625.
70. 70 Puente, X.S., et al. Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. 88 (2011), 650–656.
71. 71 Takahashi, K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131 (2007), 861–872.
72. 72 Park, I.H., et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451 (2008), 141–146.
73. 73 Sommer, C.A., et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27 (2009), 543–549.
74. 74 Yu, J., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318 (2007), 1917–1920.
75. 75 Carey, B.W., et al. Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 157–162.
76. 76 Hockemeyer, D., et al. A drug-inducible system for direct reprogramming of human somatic cells to pluripotency. Cell Stem Cell 3 (2008), 346–353.
77. 77 Maherali, N., et al. A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 3 (2008), 340–345.
78. 78 Stadtfeld, M., et al. Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2 (2008), 230–240.
79. 79 Soldner, F., et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136 (2009), 964–977.
80. 80 Somers, A., et al. Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells 28 (2010), 1728–1740.
81. 81 Kaji, K., et al. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458 (2009), 771–775.
82. 82 Woltjen, K., et al. PiggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458 (2009), 766–770.
83. 83 Stadtfeld, M., et al. Induced pluripotent stem cells generated without viral integration. Science 322 (2008), 945–949.
84. 84 Zhou, W., Freed, C.R., Adenoviral gene Delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells 27 (2009), 2667–2674.
85. 85 Okita, K., et al. Generation of mouse induced pluripotent stem cells without viral vectors. Science 322 (2008), 949–953.
86. 86 Yu, J., et al. Human induced pluripotent Stem cells free of vector and transgene sequences. Science 324 (2009), 797–801.
87. 87 Jia, F., et al. A nonviral minicircle vector for deriving human iPS cells. Nat. Meth. 7 (2010), 197–199.
88. 88 Fusaki, N., et al. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc. Jpn. Acad., Ser. B 85 (2009), 348–362.
89. 89 Kim, D., et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4 (2009), 472–476.
90. 90 Zhou, H., et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4 (2009), 381–384.
91. 91 Warren, L., et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7 (2010), 618–630.
92. 92 Miyoshi, N., et al. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8 (2011), 633–638.
93. 93 Anokye-Danso, F., et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8 (2011), 376–388.