Neural stem cells in aging and disease

Journal of Cellular and Molecular Medicine

Volumn 6, Issue 4, 2002, Pages 475-496

  Limke, Tobi ^a   Rao, Mahendra S ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Aging; Alzheimer's; Neural stem cell; Parkinson's; Stroke

Indexed keywords

AGING; ANIMAL; BRAIN; BRAIN DISEASE; CELL DIFFERENTIATION; CELL DIVISION; CELL SURVIVAL; CYTOLOGY; HUMAN; NERVE CELL; PATHOLOGY; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

AGING; ANIMALS; BRAIN; BRAIN DISEASES; CELL DIFFERENTIATION; CELL DIVISION; CELL SURVIVAL; HUMANS; NEURONS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 0037686253     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2002.tb00451.x     Document Type: Review

References (136)

1. Kemper T., Neuroanatomical and neuropathological changes during aging and in dementia. In: Albert M., Knoepfel J., eds., Clinical Neurology of Aging, Oxford University Press, New York, 1994, pp. 3-67
2. Cowell P.E., Turetsky B.I., Gur R.C., Grossman R.I., Shtasel D.L., Gur R.E., Sex differences in aging of the human frontal and temporal lobes, J. Neurosci., 14: 4748-4755, 1994
3. Raz N., Gunning F.M., Head D., Dupuis J.H., McQuain J., Briggs S.D., Loken W.J., Thornton A.E., Acker J.D., Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter, Cereb. Cortex., 7: 268-282, 1997
4. Raz N., Torres I.J., Acker J.D., Age, gender, and hemispheric differences in human striatum: a quantitative review and new data from in vivo MRI morphometry, Neurobiol. Learn. Mem., 63: 133-142, 1995
5. Doraiswamy P.M., Na C., Husain M.M., Figiel G.S., McDonald W.M., Ellinwood E.H., Jr., Boyko O.B., Krishnan K.R., Morphometric changes of the human midbrain with normal aging: MR and stereologic findings, AJNR Am. J. Neuroradiol., 13: 383-386, 1992
6. Weis S., Kimbacher M., Wenger E., Neuhold A., Morphometric analysis of the corpus callosum using MR: correlation of measurements with aging in healthy individuals, AJNR Am. J. Neuroradiol., 14: 637-645, 1993
7. Trollor J.N., Valenzuela M.J., Brain ageing in the new millennium, Aust N Z J Psychiatry, 35: 788-805, 2001
8. Morrison J.H., Hof P.R., Life and death of neurons in the aging brain, Science, 278: 412-9, 1997
9. Bertoni-Freddari C., Fattoretti P., Paoloni R., Caselli U., Galeazzi L., Meier-Ruge W., Synaptic structural dynamics and aging, Gerontology, 42: 170-180, 1996
10. Mattson M.P., Pedersen W.A., Duan W., Culmsee C., Camandola S., Cellular and molecular mechanisms underlying perturbed energy metabolism and neuronal degeneration in Alzheimer's and Parkinson's diseases, Ann. N. Y. Acad. Sci., 893: 154-175, 1999
11. Sastre J., Pallardo F.V., Vina J., Mitochondrial oxidative stress plays a key role in aging and apoptosis, IUBMB Life, 49: 427-435, 2000
12. Schapira A.H., Oxidative stress and mitochondrial dysfunction in neurodegeneration, Curr. Opin. Neurol., 9: 260-264, 1996
13. Keller J.N., Mattson M.P., Roles of lipid peroxidation in modulation of cellular signaling pathways, cell dysfunction, and death in the nervous system, Rev. Neurosci., 9: 105-116, 1998
14. Reuter-Lorenz P., New visions of the aging mind and brain, Trends Cogn. Sci., 6: 394, 2002
15. Mattson M.P., Brain evolution and lifespan regulation: conservation of signal transduction pathways that regulate energy metabolism, Mech. Ageing Dev., 123: 947-953, 2002
16. Bartke A., Brown-Borg H.M., Bode A.M., Carlson J., Hunter W.S., Bronson R.T., Does growth hormone prevent or accelerate aging?, Exp. Gerontol., 33: 675-687, 1998
17. Flurkey K., Papaconstantinou J., Miller R.A., Harrison D.E., Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production, Proc. Natl. Acad. Sci. U S A, 98: 6736-6741, 2001
18. Honda Y., Honda S., The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans, Faseb J., 13: 1385-1393, 1999
19. Lin K., Hsin H., Libina N., Kenyon C., Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling, Nat. Genet., 28: 139-145, 2001
20. Wolkow C.A., Kimura K.D., Lee M.S., Ruvkun G., Regulation of C. elegans life-span by insulinlike signaling in the nervous system, Science, 290: 147-150, 2000
21. Kalyani A.J., Mujtaba T., Rao M.S., Expression of EGF receptor and FGF receptor isoforms during neuroepithelial stem cell differentiation, J. Neurobiol., 38: 207-224, 1999
22. Quinn S.M., Walters W.M., Vescovi A.L., Whittemore S.R., Lineage restriction of neuroepithelial precursor cells from fetal human spinal cord, J. Neurosci. Res., 57: 590-602, 1999
23. Ling Z.D., Potter E.D., Lipton J.W., Carvey P.M., Differentiation of mesencephalic progenitor cells into dopaminergic neurons by cytokines, Exp. Neurol., 149: 411-423, 1998
24. Roy N.S., Benraiss A., Wang S., Fraser R.A., Goodman R., Couldwell W.T., Nedergaard M., Kawaguchi A., Okano H., Goldman S.A., Promoter-targeted selection and isolation of neural progenitor cells from the adult human ventricular zone, J. Neurosci. Res., 59: 321-331, 2000
25. Roy N.S., Wang S., Jiang L., Kang J., Benraiss A., Harrison-Restelli C., Fraser R.A., Couldwell W.T., Kawaguchi A., Okano H., Nedergaard M., Goldman S.A., In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus, Nat. Med., 6: 271-277, 2000
26. Song H.J., Stevens C.F., Gage F.H., Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons, Nat. Neurosci., 5: 438-445, 2002
27. Li R., Thode S., Zhou J., Richard N., Pardinas J., Rao M.S., Sah D.W., Motoneuron differentiation of immortalized human spinal cord cell lines, J. Neurosci. Res., 59: 342-352, 2000
28. Sato K., Hayashi T., Sasaki C., Iwai M., Li F., Manabe Y., Seki T., Abe K., Temporal and spatial differences of PSA-NCAM expression between young-adult and aged rats in normal and ischemic brains, Brain Res., 922: 135-139, 2001
29. Scolding N.J., Rayner P.J., Compston D.A., Identification of A2B5-positive putative oligodendrocyte progenitor cells and A2B5-positive astrocytes in adult human white matter, Neuroscience, 89: 1-4, 1999
30. Prabhakar S., D'Souza S., Antel J.P., McLaurin J., Schipper H.M., Wang E., Phenotypic and cell cycle properties of human oligodendrocytes in vitro, Brain Res., 672: 159-169, 1995
31. Rao M.S., Mayer-Proschel M., Glial-restricted precursors are derived from multipotent neuroepithelial stem cells, Dev. Biol., 188: 48-63, 1997
32. Mi H., Barres B.A., Purification and characterization of astrocyte precursor cells in the developing rat optic nerve, J. Neurosci., 19: 1049-1061, 1999
33. Seidman K.J., Teng A.L., Rosenkopf R., Spilotro P., Weyhenmeyer J.A., Isolation, cloning and characterization of a putative type-1 astrocyte cell line, Brain Res., 753: 18-26, 1997
34. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., Steindler D.A., Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain, Proc. Natl. Acad. Sci. U S A, 97: 13883-13888, 2000
35. Kondo T., Raff M., Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells, Science, 289: 1754-1757, 2000
36. Sommer L., Rao M., Neural stem cells and regulation of cell number, Prog. Neurobiol., 66: 1-18, 2002
37. McMahon J.A., Takada S., Zimmerman L.B., Fan C.M., Harland R.M., McMahon A.P., Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite, Genes Dev., 12: 1438-1452, 1998
38. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A., Noggin antagonizes BMP signaling to create a niche for adult neurogenesis, Neuron, 28: 713-726, 2000
39. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., Gage F.H., Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS, J. Neurosci., 19: 8487-8497, 1999
40. Whittemore S.R., Morassutti D.J., Walters W.M., Liu R.H., Magnuson D.S., Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations, Exp. Cell Res., 252: 75-95, 1999
41. Pincus D.W., Keyoung H.M., Harrison-Restelli C., Goodman R.R., Fraser R.A., Edgar M., Sakakibara S., Okano H., Nedergaard M., Goldman S.A., Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells, Ann. Neurol., 43: 576-585, 1998
42. Shetty A.K., Turner D.A., In vitro survival and differentiation of neurons derived from epidermal growth factor-responsive postnatal hippocampal stem cells: inducing effects of brain-derived neurotrophic factor, J. Neurobiol., 35: 395-425, 1998
43. Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., Rogers D., Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides, Nature, 336: 688-690, 1988
44. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M., Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells, Nature, 336: 684-687, 1988
45. Conover J.C., Ip N.Y., Poueymirou W.T., Bates B., Goldfarb M.P., DeChiara T.M., Yancopoulos G.D., Ciliary neurotrophic factor maintains the pluripotentiality of embryonic stem cells, Development, 119: 559-565, 1993
46. Yoshida K., Chambers I., Nichols J., Smith A., Saito M., Yasukawa K., Shoyab M., Taga T., Kishimoto T., Maintenance of the pluripotential phenotype of embryonic stem cells through direct activation of gp130 signalling pathways, Mech. Dev., 45: 163-171, 1994
47. Hughes S.M., Lillien L.E., Raff M.C., Rohrer H., Sendtner M., Ciliary neurotrophic factor induces type-2 astrocyte differentiation in culture, Nature, 335: 70-73, 1988
48. Johe K.K., Hazel T.G., Muller T., Dugich-Djordjevic M.M., McKay R.D., Single factors direct the differentiation of stem cells from the fetal and adult central nervous system, Genes Dev., 10: 3129-3140, 1996
49. Koblar S.A., Turnley A.M., Classon B.J., Reid K.L., Ware C.B., Cheema S.S., Murphy M., Bartlett P.F., Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor, Proc. Natl. Acad. Sci. U S A, 95: 3178-3181, 1998
50. Mayer M., Bhakoo K., Noble M., Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro, Development, 120: 143-153, 1994
51. Gard A.L., Williams W.C., 2nd, Burrell M.R., Oligodendroblasts distinguished from O-2A glial progenitors by surface phenotype (04+GalC-) and response to cytokines using signal transducer LIFR beta, Dev. Biol., 167: 596-608, 1995
52. Marmur R., Kessler J.A., Zhu G., Gokhan S., Mehler M.F., Differentiation of oligodendroglial progenitors derived from cortical multipotent cells requires extrinsic signals including activation of gp130/LIFbeta receptors, J. Neurosci., 18: 9800-9811, 1998
53. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., Ray J., Multipotent progenitor cells in the adult dentate gyrus, J. Neurobiol., 36: 249-266, 1998
54. Garcia-Verdugo J.M., Doetsch F., Wichterle H., Lim D.A., Alvarez-Buylla A., Architecture and cell types of the adult subventricular zone: in search of the stem cells, J. Neurobiol., 36: 234-248, 1998
55. Lemaire V., Koehl M., Le Moal M., Abrous D.N., Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus, Proc. Natl. Acad. Sci. U S A, 97: 11032-11037, 2000
56. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C.W., Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain, Brain Res., 726: 49-56, 1996
57. Kempermann G., van Praag H., Gage F.H., Activity-dependent regulation of neuronal plasticity and self repair, Prog. Brain Res., 127: 35-48, 2000
58. van Praag H., Kempermann G., Gage F.H., Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus, Nat. Neurosci., 2: 266-270, 1999
59. Kempermann G., Gage F.H., Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal, Hippocampus, 9: 321-332, 1999
60. Young D., Lawlor P.A., Leone P., Dragunow M., During M.J., Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective, Nat. Med., 5: 448-453, 1999
61. Liu J., Solway K., Messing R.O., Sharp F.R., Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils, J. Neurosci., 18: 7768-7778, 1998
62. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H., Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus, J. Neurosci., 17: 3727-3738, 1997
63. Kuhn H.G., Dickinson-Anson H., Gage F.H., Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation, J. Neurosci., 16: 2027-2033, 1996
64. Montaron M.F., Petry K.G., Rodriguez J.J., Marinelli M., Aurousseau C., Rougon G., Le Moal M., Abrous D.N., Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus, Eur. J. Neurosci., 11: 1479-1485, 1999
65. Haughey N.J., Liu D., Nath A., Borchard A.C., Mattson M.P., Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease, Neuromolecular Med., 1: 125-135, 2002
66. Morgan C.D., Nordin S., Murphy C., Odor identification as an early marker for Alzheimer's disease: impact of lexical functioning and detection sensitivity, J. Clin. Exp. Neuropsychol., 17: 793-803, 1995
67. Devanand D.P., Michaels-Marston K.S., Liu X., Pelton G.H., Padilla M., Marder K., Bell K., Stern Y., Mayeux R., Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up, Am. J. Psychiatry, 157: 1399-1405, 2000
68. Esiri M.M., Wilcock G.K., The olfactory bulbs in Alzheimer's disease, J. Neurol. Neurosurg. Psychiatry, 47: 56-60, 1984
69. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T., Nakafuku M., Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors, Cell, 110: 429-441, 2002
70. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O., Neuronal replacement from endogenous precursors in the adult brain after stroke, Nat. Med., 8: 963-970, 2002
71. Lie D.C., Dziewczapolski G., Willhoite A.R., Kaspar B.K., Shults C.W., Gage F.H., The adult substantia nigra contains progenitor cells with neurogenic potential, J. Neurosci., 22: 6639-6649, 2002
72. Flax J.D., Aurora S., Yang C., Simonin C., Wills A.M., Billinghurst L.L., Jendoubi M., Sidman R.L., Wolfe J.H., Kim S.U., Snyder E.Y., Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes, Nat. Biotechnol., 16: 1033-1039, 1998
73. Terada N., Hamazaki T., Oka M., Hoki M., Mastalerz D.M., Nakano Y., Meyer E.M., Morel L., Petersen B.E., Scott E.W., Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion, Nature, 416: 542-545, 2002
74. Ying Q.L., Nichols J., Evans E.P., Smith A.G., Changing potency by spontaneous fusion, Nature, 416: 545-548, 2002
75. Studer L., Tabar V., McKay R.D., Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats, Nat. Neurosci., 1: 290-295, 1998
76. Kim J.H., Auerbach J.M., Rodriguez-Gomez J.A., Velasco I., Gavin D., Lumelsky N., Lee S.H., Nguyen J., Sanchez-Pernaute R., Bankiewicz K., McKay R., Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease, Nature, 418: 50-56, 2002
77. Widner H., The Lund transplant program for Parkinson's disease and patients with MPTP-induced parkinsonism. In: Freeman T.B., Widner H., eds., Cell transplantation for neurological disorders: toward reconstruction of the human central nervous system., Humana Press, Totowa, 1998, pp. 1-17
78. Hauser R.A., Fetal nigral transplantation in Parkinson's disease: the USF pilot program (12 to 24 month evaluation). In: Freeman T.B., Widner H., eds., Cell transplantation for neurological disorders: toward reconstruction of the human central nervous system., Humana Press, Totowa, 1998, pp. 19-30
79. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., Fahn S., Transplantation of embryonic dopamine neurons for severe Parkinson's disease, N. Engl. J. Med., 344: 710-719, 2001
80. Aboody K.S., Brown A., Rainov N.G., Bower K.A., Liu S., Yang W., Small J.E., Herrlinger U., Ourednik V., Black P.M., Breakefield X.O., Snyder E.Y., From the cover: neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas, Proc. Natl. Acad. Sci. U S A, 97: 12846-12851, 2000
81. Park K.I., Teng Y.D., Snyder E.Y., The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue, Nat. Biotechnol, 20: 1111-1117, 2002
82. Fukunaga A., Uchida K., Hara K., Kuroshima Y., Kawase T., Differentiation and angiogenesis of central nervous system stem cells implanted with mesenchyme into ischemic rat brain, Cell Transplant., 8: 435-441, 1999
83. Li L., Liu F., Salmonsen R.A., Turner T.K., Litofsky N.S., Di Cristofano A., Pandolfi P.P., Jones S.N., Recht L.D., Ross A.H., PTEN in neural precursor cells: regulation of migration, apoptosis, and proliferation, Mol. Cell Neurosci., 20: 21-9, 2002
84. Shihabuddin L.S., Palmer T.D., Gage F.H., The search for neural progenitor cells: prospects for the therapy of neurodegenerative disease, Mol. Med. Today, 5: 474-480, 1999
85. Svendsen C.N., Caldwell M.A., Ostenfeld T., Human neural stem cells: isolation, expansion and transplantation, Brain Pathol., 9: 499-513, 1999
86. Gould E., Gross C.G., Neurogenesis in adult mammals: some progress and problems, J. Neurosci., 22: 619-623, 2002
87. Temple S., Stem cell plasticity - building the brain of our dreams, Nat. Rev. Neurosci., 2: 513-520, 2001
88. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H., Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain, J. Neurosci., 17: 5820-5829, 1997
89. Raballo R., Rhee J., Lyn-Cook R., Leckman J.F., Schwartz M.L., Vaccarino F.M., Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex, J. Neurosci., 20: 5012-5023, 2000
90. Vaccarino F.M., Schwartz M.L., Raballo R., Rhee J., Lyn-Cook R., Fibroblast growth factor signaling regulates growth and morphogenesis at multiple steps during brain development, Curr. Top. Dev. Biol., 46: 179-200, 1999
91. Gritti A., Frolichsthal-Schoeller P., Galli R., Parati E.A., Cova L., Pagano S.F., Bjornson C.R., Vescovi A.L., Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain, J. Neurosci., 19: 3287-3297, 1999
92. Tropepe V., Sibilia M., Ciruna B.C., Rossant J., Wagner E.F., van der Kooy D., Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon, Dev. Biol., 208: 166-188, 1999
93. Lee J.C., Mayer-Proschel M., Rao M.S., Gliogenesis in the central nervous system, Glia, 30: 105-121, 2000
94. Briscoe J., Ericson J., The specification of neuronal identity by graded Sonic Hedgehog signalling, Semin. Cell Dev. Biol., 10: 353-362, 1999
95. Zhu G., Mehler M.F., Zhao J., Yu Yung S., Kessler J.A., Sonic hedgehog and BMP2 exert opposing actions on proliferation and differentiation of embryonic neural progenitor cells, Dev. Biol., 215: 118-129, 1999
96. Sieber-Blum M., Growth factor synergism and antagonism in early neural crest development, Biochem Cell Biol., 76: 1039-1050, 1998
97. Andsberg G., Kokaia Z., Bjorklund A., Lindvall O., Martinez-Serrano A., Amelioration of ischaemia-induced neuronal death in the rat striatum by NGF-secreting neural stem cells, Eur. J. Neurosci., 10: 2026-2036, 1998
98. Martinez-Serrano A., Bjorklund A., Ex vivo nerve growth factor gene transfer to the basal forebrain in presymptomatic middle-aged rats prevents the development of cholinergic neuron atrophy and cognitive impairment during aging, Proc. Natl. Acad. Sci. U S A, 95: 1858-1863, 1998
99. Pencea V., Bingaman K.D., Freedman L.J., Luskin M.B., Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain, Exp. Neurol., 172: 1-16, 2001
100. Akerud P., Canals J.M., Snyder E.Y., Arenas E., Neuroprotection through delivery of glial cell line-derived neurotrophic factor by neural stem cells in a mouse model of Parkinson's disease, J. Neurosci., 21: 8108-8118, 2001
101. Hayflick L., Human cells and aging, Sci. Am., 218: 32-37, 1968
102. Kruger G.M., Morrison S.J., Brain repair by endogenous progenitors, Cell, 110: 399-402, 2002
103. Harley C.B., Futcher A.B., Greider C.W., Telomeres shorten during ageing of human fibroblasts, Nature, 345: 458-460, 1990
104. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E., Extension of lifespan by introduction of telomerase into normal human cells, Science, 279: 349-352, 1998
105. Allsopp R.C., Weissman I.L., Replicative senescence of hematopoietic stem cells during serial transplantation: does telomere shortening play a role?, Oncogene, 21: 3270-3273, 2002
106. Greenberg R.A., Allsopp R.C., Chin L., Morin G.B., DePinho R.A., Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation, Oncogene, 16: 1723-1730, 1998
107. Martin-Rivera L., Herrera E., Albar J.P., Blasco M.A., Expression of mouse telomerase catalytic subunit in embryos and adult tissues, Proc. Natl. Acad. Sci. U S A, 95: 10471-10476, 1998
108. Prowse K.R., Greider C.W., Developmental and tissue-specific regulation of mouse telomerase and telomere length, Proc. Natl. Acad. Sci. U S A, 92: 4818-4822, 1995
109. Blasco M.A., Funk W., Villeponteau B., Greider C.W., Functional characterization and developmental regulation of mouse telomerase RNA, Science, 269: 1267-1270, 1995
110. Haik S., Gauthier L.R., Granotier C., Peyrin J.M., Lages C.S., Dormont D., Boussin F.D., Fibroblast growth factor 2 up regulates telomerase activity in neural precursor cells, Oncogene, 19: 2957-2966, 2000
111. Vaziri H., Dragowska W., Allsopp R.C., Thomas T.E., Harley C.B., Lansdorp P.M., Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age, Proc. Natl. Acad. Sci. U S A, 91: 9857-9860, 1994
112. Lindsey J., McGill N.I., Lindsey L.A., Green D.K., Cooke H.J., In vivo loss of telomeric repeats with age in humans, Mutat. Res., 256: 45-48, 1991
113. Wyllie F.S., Jones C.J., Skinner J.W., Haughton M.F., Wallis C., Wynford-Thomas D., Faragher R.G., Kipling D., Telomerase prevents the accelerated cell ageing of Werner syndrome fibroblasts, Nat. Genet., 24: 16-17, 2000
114. Faragher R.G., Kipling D., How might replicative senescence contribute to human ageing?, Bioessays, 20: 985-991, 1998
115. Campisi J., Cancer, aging and cellular senescence, In Vivo. 14: 183-188, 2000
116. Goldstein S., Replicative senescence: the human fibroblast comes of age, Science, 249: 1129-1133, 1990
117. Lee H.W., Blasco M.A., Gottlieb G.J., Horner J.W., 2nd, Greider C.W., DePinho R.A., Essential role of mouse telomerase in highly proliferative organs, Nature, 392: 569-574, 1998
118. Rudolph K.L., Chang S., Lee H.W., Blasco M., Gottlieb G.J., Greider C., DePinho R.A., Longevity, stress response, and cancer in aging telomerase-deficient mice, Cell, 96: 701-712, 1999
119. Oikawa S., Tada-Oikawa S., Kawanishi S., Site-specific DNA damage at the GGG sequence by UVA involves acceleration of telomere shortening, Biochemistry, 40: 4763-4768, 2001
120. Petersen S., Saretzki G., von Zglinicki T., Preferential accumulation of single-stranded regions in telomeres of human fibroblasts, Exp. Cell Res., 239: 152-160, 1998
121. Henle E.S., Han Z., Tang N., Rai P., Luo Y., Linn S., Sequence-specific DNA cleavage by Fe2+-mediated fenton reactions has possible biological implications, J. Biol. Chem., 274: 962-971, 1999
122. Sitte N., Merker K., Von Zglinicki T., Grune T., Davies K.J., Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: part I-effects of proliferative senescence, Faseb J., 14: 2495-2502, 2000
123. von Zglinicki T., Pilger R., Sitte N., Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts, Free Radic. Biol. Med., 28: 64-74, 2000
124. Samani N.J., Boultby R., Butler R., Thompson J.R., Goodall A.H., Telomere shortening in atherosclerosis, Lancet, 358: 472-473, 2001
125. von Zglinicki T., Oxidative stress shortens telomeres, Trends Biochem. Sci., 27: 339-344, 2002
126. Bryan T.M., Englezou A., Dalla-Pozza L., Dunham M.A., Reddel R.R., Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines, Nat. Med., 3: 1271-1274, 1997
127. Shay J.W., Gazdar A.F., Telomerase in the early detection of cancer, J. Clin. Pathol., 50: 106-109, 1997
128. Bryan T.M., Englezou A., Gupta J., Bacchetti S., Reddel R.R., Telomere elongation in immortal human cells without detectable telomerase activity, EMBO J., 14: 4240-4248, 1995
129. Gobbel G.T., Bellinzona M., Vogt A.R., Gupta N., Fike J.R., Chan P.H., Response of postmitotic neurons to X-irradiation: implications for the role of DNA damage in neuronal apoptosis, J. Neurosci., 18: 147-155, 1998
130. Yoshikawa K., Cell cycle regulators in neural stem cells and postmitotic neurons, Neurosci. Res., 37: 1-14, 2000
131. Edgar B., Diversification of cell cycle controls in developing embryos, Curr. Opin. Cell Biol., 7: 815-824, 1995
132. Callaghan D.A., Dong L., Callaghan S.M., Hou Y.X., Dagnino L., Slack R.S., Neural precursor cells differentiating in the absence of Rb exhibit delayed terminal mitosis and deregulated E2F 1 and 3 activity, Dev. Biol., 207: 257-270, 1999
133. Weinberg R.A., The retinoblastoma protein and cell cycle control, Cell, 81: 323-330, 1995
134. Lois A.F., Cooper L.T., Geng Y., Nobori T., Carson D., Expression of the p16 and p15 cyclin-dependent kinase inhibitors in lymphocyte activation and neuronal differentiation, Cancer Res., 55: 4010-4013, 1995
135. Park D.S., Morris E.J., Padmanabhan J., Shelanski M.L., Geller H.M., Greene L.A., Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents, J. Cell Biol., 143: 457-467, 1998
136. Arendt T., Alzheimer's disease as a loss of differentiation control in a subset of neurons that retain immature features in the adult brain, Neurobiol. Aging, 21: 783-796, 2000