IPSC technology to study human aging and aging-related disorders

Current Opinion in Cell Biology

Volumn 24, Issue 6, 2012, Pages 765-774

  Liu, Guang Hui ^a,b   Ding, Zhichao ^a   Izpisua Belmonte, Juan Carlos ^b,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c CENTER OF REGENERATIVE MEDICINE IN BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; BETA GALACTOSIDE; DYSKERIN; INTERLEUKIN 8; KI 67 ANTIGEN; KRUPPEL LIKE FACTOR 4; LAMIN; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PARKIN; PHOSPHATIDYLINOSITOL 3 KINASE; PRESENILIN 1; PROTEIN P16; REACTIVE OXYGEN METABOLITE; RNA; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

AGING; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CAENORHABDITIS ELEGANS; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DEGENERATIVE DISEASE; DNA DAMAGE; DNA REPAIR; DYSKERATOSIS CONGENITA; EX VIVO STUDY; EXON; FIBROBLAST; GENE MUTATION; GENE OVEREXPRESSION; GERIATRIC DISORDER; HUMAN; IN VIVO STUDY; MACROMOLECULE; MAMMAL; MOLECULAR BIOLOGY; NERVE CELL; NEUROFILAMENT; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PLURIPOTENT STEM CELL; PREMATURE AGING; PRIORITY JOURNAL; PROGERIA; PROTEIN EXPRESSION; REVIEW; SKIN BIOPSY; TELOMERE; TELOMERE HOMEOSTASIS; WERNER SYNDROME;

AGING; ANIMALS; BIOTECHNOLOGY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; PROGERIA; STEM CELL RESEARCH; TELOMERE;

ANIMALIA;

EID: 84871936169     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2012.08.014     Document Type: Review

References (82)

1. Lutz W., Sanderson W., Scherbov S. The coming acceleration of global population ageing. Nature 2008, 451:716-719.
2. Alwan A., Maclean D.R., Riley L.M., d'Espaignet E.T., Mathers C.D., Stevens G.A., Bettcher D. Monitoring and surveillance of chronic non-communicable diseases: progress and capacity in high-burden countries. Lancet 2010, 376:1861-1868.
3. Jin K. Modern Biological Theories of Aging. Aging Dis 2010, 1:72-74.
4. Partridge L., Thornton J., Bates G. The new science of ageing. Philos Trans R Soc Lond B Biol Sci 2011, 366:6-8.
5. Jang Y.C., Remmen V.H. The mitochondrial theory of aging: insight from transgenic and knockout mouse models. Exp Gerontol 2009, 44:256-260.
6. Murga M., Bunting S., Montana M.F., Soria R., Mulero F., Canamero M., Lee Y., McKinnon P.J., Nussenzweig A., Fernandez-Capetillo O. A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nat Genet 2009, 41:891-898.
7. Hinkal G.W., Gatza C.E., Parikh N., Donehower L.A. Altered senescence, apoptosis, and DNA damage response in a mutant p53 model of accelerated aging. Mech Ageing Dev 2009, 130:262-271.
8. Yang S.H., Meta M., Qiao X., Frost D., Bauch J., Coffinier C., Majumdar S., Bergo M.O., Young S.G., Fong L.G. A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest 2006, 116:2115-2121.
9. Glazko G.V., Koonin E.V., Rogozin I.B. Molecular dating: ape bones agree with chicken entrails. Trends Genet 2005, 21:89-92.
10. Itahana K., Campisi J., Dimri G. Mechanisms of cellular senescence in human and mouse cells. Biogerontology 2004, 5:1-10.
11. Jucker M. The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med 2010, 16:1210-1214.
12. Cristofalo V.J., Allen R.G., Pignolo R.J., Martin B.G., Beck J.C. Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation. PNAS 1998, 95:10614-10619.
13. Frippiat C., Dewelle J., Remacle J., Toussaint O. Signal transduction in H2O2-induced senescence-like phenotype in human diploid fibroblasts. Free Radic Biol Med 2002, 33:1334-1346.
14. Hornsby P.J. Cellular aging and cancer. Crit Rev Oncol Hematol 2011, 79:189-195.
15. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995, 92:9363-9367.
16. Narita M., Nunez S., Heard E., Lin A.W., Hearn S.A., Spector D.L., Hannon G.J., Lowe S.W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 113:703-716.
17. Janzen V., Forkert R., Fleming H.E., Saito Y., Waring M.T., Dombkowski D.M., Cheng T., DePinho R.A., Sharpless N.E., Scadden D.T. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
18. Acosta J.C., O'Loghlen A., Banito A., Guijarro M.V., Augert A., Raguz S., Fumagalli M., Da Costa M., Brown C., Popov N., et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008, 133:1006-1018.
19. Martin G.M. Genetic syndromes in man with potential relevance to the pathobiology of aging. Birth Defects Orig Artic Ser 1978, 14:5-39.
20. Ramirez C.L., Cadinanos J., Varela I., Freije J.M., Lopez-Otin C. Human progeroid syndromes, aging and cancer: new genetic and epigenetic insights into old questions. Cell Mol Life Sci 2007, 64:155-170.
21. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
22. Tiscornia G., Vivas E.L., Belmonte J.C. Diseases in a dish: modeling human genetic disorders using induced pluripotent cells. Nat Med 2011, 17:1570-1576.
23. Rowntree R.K., McNeish J.D. Induced pluripotent stem cells: opportunities as research and development tools in 21st century drug discovery. Regen Med 2010, 5:557-568.
24. Eriksson M., Brown W.T., Gordon L.B., Glynn M.W., Singer J., Scott L., Erdos M.R., Robbins C.M., Moses T.Y., Berglund P., et al. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003, 423:293-298.
25. Scaffidi P., Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006, 312:1059-1063.
26. McClintock D., Ratner D., Lokuge M., Owens D.M., Gordon L.B., Collins F.S., Djabali K. The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS ONE 2007, 2:e1269.
27. Scaffidi P., Misteli T. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol 2008, 10:452-459.
28. Liu G.-H., Barkho B.Z., Ruiz S., Diep D., Qu J., Yang S.-L., Panopoulos A.D., Suzuki K., Kurian L., Walsh C., et al. Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 2011, 472:221-225.
29. Zhang J., Lian Q., Zhu G., Zhou F., Sui L., Tan C., Mutalif R.A., Navasankari R., Zhang Y., Tse H.F., et al. A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 2011, 8:31-45.
30. Ho J.C., Zhou T., Lai W.H., Huang Y., Chan Y.C., Li X., Wong N.L., Li Y., Au K.W., Guo D., et al. Generation of induced pluripotent stem cell lines from 3 distinct laminopathies bearing heterogeneous mutations in lamin A/C. Aging (Albany, NY) 2011, 3:380-390.
31. Constantinescu D., Gray H.L., Sammak P.J., Schatten G.P., Csoka A.B. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 2006, 24:177-185.
32. Liu G.H., Suzuki K., Qu J., Sancho-Martinez I., Yi F., Li M., Kumar S., Nivet E., Kim J., Soligalla R.D., et al. Targeted gene correction of laminopathy-associated LMNA mutations in patient-specific iPSCs. Cell Stem Cell 2011, 8:688-694.
33. Misteli T. HGPS-derived iPSCs for the ages. Cell Stem Cell 2011, 8:4-6.
34. Cao K., Blair C.D., Faddah D.A., Kieckhaefer J.E., Olive M., Erdos M.R., Nabel E.G., Collins F.S. Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest 2011, 121:2833-2844.
35. Harley C.B., Futcher A.B., Greider C.W. Telomeres shorten during ageing of human fibroblasts. Nature 1990, 345:458-460.
36. de Lange T. Telomeres and senescence: ending the debate. Science 1998, 279:334-335.
37. Blasco M.A. Telomere length, stem cells and aging. Nat Chem Biol 2007, 3:640-649.
38. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
39. Marion R.M., Strati K., Li H., Tejera A., Schoeftner S., Ortega S., Serrano M., Blasco M.A. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 2009, 4:141-154.
40. Martinez P., Blasco M.A. Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins. Nat Rev Cancer 2011, 11:161-176.
41. Agarwal S., Loh Y.H., McLoughlin E.M., Huang J., Park I.H., Miller J.D., Huo H., Okuka M., Dos Reis R.M., Loewer S., et al. Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients. Nature 2010, 464:292-296.
42. Batista L.F., Pech M.F., Zhong F.L., Nguyen H.N., Xie K.T., Zaug A.J., Crary S.M., Choi J., Sebastiano V., Cherry A., et al. Telomere shortening and loss of self-renewal in dyskeratosis congenita induced pluripotent stem cells. Nature 2011, 474:399-402.
43. Wang F., Yin Y., Ye X., Liu K., Zhu H., Wang L., Chiourea M., Okuka M., Ji G., Dan J., et al. Molecular insights into the heterogeneity of telomere reprogramming in induced pluripotent stem cells. Cell Res 2011, 22:757-768.
44. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
45. Lesage S., Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet 2009, 18:R48-R59.
46. Kume T., Kawato Y., Osakada F., Izumi Y., Katsuki H., Nakagawa T., Kaneko S., Niidome T., Takada-Takatori Y., Akaike A. Dibutyryl cyclic AMP induces differentiation of human neuroblastoma SH-SY5Y cells into a noradrenergic phenotype. Neurosci Lett 2008, 443:199-203.
47. Park I.H., Arora N., Huo H., Maherali N., Ahfeldt T., Shimamura A., Lensch M.W., Cowan C., Hochedlinger K., Daley G.Q. Disease-specific induced pluripotent stem cells. Cell 2008, 134:877-886.
48. Soldner F., Hockemeyer D., Beard C., Gao Q., Bell G.W., Cook E.G., Hargus G., Blak A., Cooper O., Mitalipova M., et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009, 136:964-977.
49. Cooper O., Hargus G., Deleidi M., Blak A., Osborn T., Marlow E., Lee K., Levy A., Perez-Torres E., Yow A., et al. Differentiation of human ES and Parkinson's disease iPS cells into ventral midbrain dopaminergic neurons requires a high activity form of SHH, FGF8a and specific regionalization by retinoic acid. Mol Cell Neurosci 2010, 45:258-266.
50. Hargus G., Cooper O., Deleidi M., Levy A., Lee K., Marlow E., Yow A., Soldner F., Hockemeyer D., Hallett P.J., et al. Differentiated Parkinson patient-derived induced pluripotent stem cells grow in the adult rodent brain and reduce motor asymmetry in Parkinsonian rats. Proc Natl Acad Sci U S A 2010, 107:15921-15926.
51. Nguyen H.N., Byers B., Cord B., Shcheglovitov A., Byrne J., Gujar P., Kee K., Schule B., Dolmetsch R.E., Langston W., et al. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 2011, 8:267-280.
52. Seibler P., Graziotto J., Jeong H., Simunovic F., Klein C., Krainc D. Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J Neurosci 2011, 31:5970-5976.
53. Soldner F., Laganiere J., Cheng A.W., Hockemeyer D., Gao Q., Alagappan R., Khurana V., Golbe L.I., Myers R.H., Lindquist S., et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 2011, 146:318-331.
54. Devine M.J., Ryten M., Vodicka P., Thomson A.J., Burdon T., Houlden H., Cavaleri F., Nagano M., Drummond N.J., Taanman J.W., et al. Parkinson's disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat Commun 2011, 2:440.
55. Yagi T., Ito D., Okada Y., Akamatsu W., Nihei Y., Yoshizaki T., Yamanaka S., Okano H., Suzuki N. Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum Mol Genet 2011, 20:4530-4539.
56. Byers B., Cord B., Nguyen H.N., Schule B., Fenno L., Lee P.C., Deisseroth K., Langston J.W., Pera R.R., Palmer T.D. SNCA triplication Parkinson's patient's iPSC-derived DA neurons accumulate alpha-synuclein and are susceptible to oxidative stress. PLoS ONE 2011, 6:e26159.
57. Erceg SaS M., Bhattacharya S.S. Derivation of dopaminergic neurons from human embryonic stem cells and IPS cells in animal-free conditions ready to use in a treatment of Parkinson's disease. Mov Disord 2011, S335.
58. Jiang H., Ren Y., Yuen E.Y., Zhong P., Ghaedi M., Hu Z., Azabdaftari G., Nakaso K., Yan Z., Feng J. Parkin controls dopamine utilization in human midbrain dopaminergic neurons derived from induced pluripotent stem cells. Nat Commun 2012, 3:668.
59. Sanchez-Danes A., Richaud-Patin Y., Carballo-Carbajal I., Jimenez-Delgado S., Caig C., Mora S., Di Guglielmo C., Ezquerra M., Patel B., Giralt A., et al. Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol Med 2012, 4:380-395.
60. Do C.B., Tung J.Y., Dorfman E., Kiefer A.K., Drabant E.M., Francke U., Mountain J.L., Goldman S.M., Tanner C.M., Langston J.W., et al. Web-based genome-wide association study identifies two novel loci and a substantial genetic component for Parkinson's disease. PLoS Genet 2011, 7:e1002141.
61. Rissman R.A., Mobley W.C. Implications for treatment: GABAA receptors in aging, Down syndrome and Alzheimer's disease. J Neurochem 2011, 117:613-622.
62. Israel M.A., Goldstein L.S. Capturing Alzheimer's disease genomes with induced pluripotent stem cells: prospects and challenges. Genome Med 2011, 3:49.
63. Choi S.H., Tanzi R.E. iPSCs to the rescue in Alzheimer's research. Cell Stem Cell 2012, 10:235-236.
64. Koch P., Tamboli I.Y., Mertens J., Wunderlich P., Ladewig J., Stüber K., Esselmann H., Wiltfang J., Brüstle O., Walter J. Presenilin-1 L166P mutant human pluripotent stem cell-derived neurons exhibit partial loss of γ-secretase activity in endogenous amyloid-β generation. Am J Pathol 2012, 180:2404-2416.
65. Israel M.A., Yuan S.H., Bardy C., Reyna S.M., Mu Y., Herrera C., Hefferan M.P., Van Gorp S., Nazor K.L., Boscolo F.S., et al. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 2012, 482:216-220.
66. Yahata N., Asai M., Kitaoka S., Takahashi K., Asaka I., Hioki H., Kaneko T., Maruyama K., Saido T.C., Nakahata T., et al. Anti-Abeta drug screening platform using human iPS cell-derived neurons for the treatment of Alzheimer's disease. PLoS ONE 2011, 6:e25788.
67. Shi Y., Kirwan P., Smith J., Maclean G., Orkin S.H., Livesey F.J. A human stem cell model of early Alzheimer's disease pathology in down syndrome. Sci Transl Med 2012, 4:124ra129.
68. Kato S. Amyotrophic lateral sclerosis models and human neuropathology: similarities and differences. Acta Neuropathol 2008, 115:97-114.
69. Traub R., Mitsumoto H., Rowland L.P. Research advances in amyotrophic lateral sclerosis, 2009 to 2010. Curr Neurol Neurosci Rep 2011, 11:67-77.
70. Marchetto M.C., Muotri A.R., Mu Y., Smith A.M., Cezar G.G., Gage F.H. Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008, 3:649-657.
71. Bilican B., Serio A., Barmada S.J., Nishimura A.L., Sullivan G.J., Carrasco M., Phatnani H.P., Puddifoot C.A., Story D., Fletcher J., et al. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci 2012, 109:5803-5808.
72. Lapasset L., Milhavet O., Prieur A., Besnard E., Babled A., Ait-Hamou N., Leschik J., Pellestor F., Ramirez J.M., De Vos J., et al. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev 2011, 25:2248-2253.
73. Ohmine S., Squillace K.A., Hartjes K.A., Deeds M.C., Armstrong A.S., Thatava T., Sakuma T., Terzic A., Kudva Y., Ikeda Y. Reprogrammed keratinocytes from elderly type 2 diabetes patients suppress senescence genes to acquire induced pluripotency. Aging (Albany, NY) 2012, 4:60-73.
74. Barrero M.J., Izpisua Belmonte J.C. iPS cells forgive but do not forget. Nat Cell Biol 2011, 13:523-525.
75. Müller L.U.W., Milsom M.D., Harris C.E., Vyas R., Brumme K.M., Parmar K., Moreau L.A., Schambach A., Park I.-H., London W.B., et al. Overcoming reprogramming resistance of fanconi anemia cells. Blood 2012, 119:5449-5457.
76. McCracken K.W., Howell J.C., Wells J.M., Spence J.R. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat Protoc 2011, 6:1920-1928.
77. Spence J.R., Mayhew C.N., Rankin S.A., Kuhar M.F., Vallance J.E., Tolle K., Hoskins E.E., Kalinichenko V.V., Wells S.I., Zorn A.M., et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011, 470:105-109.
78. Marolt D., Campos I.M., Bhumiratana S., Koren A., Petridis P., Zhang G., Spitalnik P.F., Grayson W.L., Vunjak-Novakovic G. Engineering bone tissue from human embryonic stem cells. Proc Natl Acad Sci U S A 2012, 109:8705-8709.
79. Phillips M.J., Wallace K.A., Dickerson S.J., Miller M.J., Verhoeven A., Martin J.M., Wright L., Shen W., Capowski E.E., Percin E.F., et al. Blood-derived Human iPS cells generate optic vesicle-like structures with the capacity to form retinal laminae and develop synapses. Invest Ophthalmol Vis Sci 2012, 53:2007-2019.
80. Kobayashi T., Yamaguchi T., Hamanaka S., Kato-Itoh M., Yamazaki Y., Ibata M., Sato H., Lee Y.S., Usui J., Knisely A.S., et al. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell 2010, 142:787-799.
81. Isotani A., Hatayama H., Kaseda K., Ikawa M., Okabe M. Formation of a thymus from rat ES cells in xenogeneic nude mouse<-->rat ES chimeras. Genes Cells 2011, 16:397-405.
82. Zhang W., Ding Z., Liu G.H. Evolution of iPSC disease models. Protein Cell 2012, 3:1-4.