Stem cell-based models and therapies for neurodegenerative diseases

Critical Reviews in Biomedical Engineering

Volumn 37, Issue 4-5, 2009, Pages 321-353

  Iyer, Shilpa ^a   Alsayegh, Khaled ^b   Abraham, Sheena ^c   Rao, Raj R ^b,c  

^a UNIVERSITY OF VIRGINIA   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c Virginia Commonwealth University   (United States)

Author keywords

Cellular differentiation; Gene therapy; Mitochondria; Neural progenitors; Pluripotent stem cells

Indexed keywords

BIOCHEMISTRY; CELL CULTURE; CELLS; CYTOLOGY; CYTOTOXICITY; DISEASE CONTROL; FUNCTIONAL POLYMERS; GENE THERAPY; GENES; MITOCHONDRIA; NEURONS; STEM CELLS;

CELLULAR DIFFERENTIATION; HEALTH-CARE SYSTEM; IMMORTALIZED CELLS; MITOCHONDRIAL DYSFUNCTION; NEURAL PROGENITORS; NEURODEGENERATIVE DISORDERS; NEURONAL DEVELOPMENT; PLURIPOTENT STEM CELLS;

NEURODEGENERATIVE DISEASES;

MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; TRANSCRIPTION FACTOR;

ALZHEIMER DISEASE; CELL PROLIFERATION; CELL TYPE; DEGENERATIVE DISEASE; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYONIC STEM CELL; GENE DELETION; GENE DUPLICATION; GENE THERAPY; GENOME; HUMAN; IMMOBILIZED CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PARKINSON DISEASE; PLURIPOTENT STEM CELL; POINT MUTATION; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION;

EID: 77952127826     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevBiomedEng.v37.i4-5.20     Document Type: Review

References (145)

1. Rossant J. Lineage development and polar asymmetries in the periimplantation mouse blastocyst. Semin Cell Dev Biol. 2004 Oct;15(5): 573-581
2. Du ZW, Zhang SC. Neural differentiation from embryonic stem cells: which way? Stem Cells Dev. 2004 Aug;13(4):372-381
3. Harland R. Neural induction. Curr Opin Genet Dev. 2000 Aug;10(4): 357-362
4. Graham A, Francis-West P, Brickell P, Lumsden A. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature. 1994 Dec 15;372(6507):684-686
5. Shimamura K, Rubenstein JL. Inductive interactions direct early regionalization of the mouse forebrain. Development. 1997 Jul;124(14):2709-2718
6. Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci. 2007 Oct;8(10):755-765
7. Takemoto T, Uchikawa M, Kamachi Y, Kondoh H. Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development. 2006 Jan;133(2):297-306.
8. Pevny L, Placzek M. SOX genes and neural progenitor identity. Curr Opin Neurobiol. 2005 Feb;15(1):7-13.
9. Zhao S, Nichols J, Smith AG, Li M. SoxB transcription factors specify neuroectodermal lineage choice in ES cells. Mol Cell Neurosci. 2004 Nov;27(3):332-342
10. Mitalipova M, Calhoun J, Shin S, Wininger D, Schulz T, Noggle S, Venable A, Lyons I, Robins A, Stice S. Human embryonic stem cell lines derived from discarded embryos. Stem Cells. 2003;21(5):521-526
11. Reubinoff BE, Pera MF, Fong C-Y, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotech. 2000;18(4):399-404.
12. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998 Nov 6;282(5391):1145-1147
13. Dhara SK, Stice SL. Neural differentiation of human embryonic stem cells. J Cell Biochem. 2008 Oct 15;105(3):633-640
14. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 2008 Jan 15;22(2):152-165
15. Elkabetz Y, Studer L. Human ESC-derived neural rosettes and neural stem cell progression. Cold Spring Harb Symp Quant Biol. 2008;73: 377-387
16. Dhara SK, Hasneen K, Machacek DW, Boyd NL, Rao RR, Stice SL. Human neural progenitor cells derived from embryonic stem cells in feeder-free cultures. Differentiation. 2008 May;76(5):454-464
17. Shin S, Mitalipova M, Noggle S, Tibbitts D, Venable A, Rao R, Stice SL. Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions. Stem Cells. 2006 Jan;24(1):125-138
18. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol. 2001 Dec;19(12):1129-1133
19. Perrier AL, Tabar V, Barberi T, Rubio ME, Bruses J, Topf N, Harrison NL, Studer L. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12543-12548
20. Yan Y, Yang D, Zarnowska ED, Du Z, Werbel B, Valliere C, Pearce RA, Thomson JA, Zhang SC. Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells. 2005 Jun-Jul;23(6):781-790
21. Zhang SC. Neural subtype specification from embryonic stem cells. Brain Pathol. 2006 Apr;16(2):132-142
22. Crimi M, Rigolio R. The mitochondrial genome, a growing interest inside an organelle. Int J Nanomedicine. 2008;3(1):51-57
23. Parker GC, Acsadi G, Brenner CA. Mitochondria: determinants of stem cell fate? Stem Cells Dev. 2009 Jul-Aug;18(6):803-806
24. Sekine S, Miura M, Chihara T. Organelles in developing neurons: Essential regulators of neuronal morphogenesis and function. Int J Dev Biol. 2009;53(1):19-27
25. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004 Mar 4;41(5):683-686
26. Gage FH. Mammalian neural stem cells. Science. 2000 Feb 25;287(5457): 1433-1438
27. Ma DK, Bonaguidi MA, Ming GL, Song H. Adult neural stem cells in the mammalian central nervous system. Cell Res. 2009 Jun;19(6): 672-682
28. Ma DK, Ming GL, Song H. Glial influences on neural stem cell development: Cellular niches for adult neurogenesis. Curr Opin Neurobiol. 2005 Oct;15(5):514-520
29. Morrison RS, Kornblum HI, Leslie FM, Bradshaw RA. Trophic stimulation of cultured neurons from neonatal rat brain by epidermal growth factor. Science. 1987 Oct 2;238(4823):72-75
30. Nurcombe V, Ford MD, Wildschut JA, Bartlett PF. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science. 1993 Apr 2;260(5104):103-106
31. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992 Mar 27;255(5052):1707-1710
32. Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 1996 Apr 10;175(1):1-13.
33. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron. 1994 Nov;13(5):1071-1082
34. Palmer TD, Ray J, Gage FH. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci. 1995 Oct;6(5):474-486
35. Palmer TD, Takahashi J, Gage FH. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci. 1997;8(6):389-404.
36. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci. 1996 Dec 1;16(23):7599-7609
37. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci. 1996 Sep;19(9):387-393
38. Bonaguidi MA, Peng CY, McGuire T, Falciglia G, Gobeske KT, Czeisler C, Kessler JA. Noggin expands neural stem cells in the adult hippocampus. J Neurosci. 2008 Sep 10;28(37):9194-9204
39. Dromard C, Bartolami S, Deleyrolle L, Takebayashi H, Ripoll C, Simonneau L, Prome S, Puech S, Tran VB, Duperray C, Valmier J, Privat A, Hugnot JP. NG2 and Olig2 expression provides evidence for phenotypic deregulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells. 2007 Feb;25(2):340-353
40. Brazel CY, Limke TL, Osborne JK, Miura T, Cai J, Pevny L, Rao MS. Sox2 expression defines a heterogeneous population of neurosphereforming cells in the adult murine brain. Aging Cell. 2005 Aug;4(4): 197-207.
41. Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells. 2008 Apr;26(4):988-996
42. Davis AA, Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature. 1994 Nov 17;372(6503):263-266
43. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J. Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11879-11883
44. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells. Nature. 2002 May 2;417(6884):39-44.
45. Song HJ, Stevens CF, Gage FH. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci. 2002 May;5(5):438-445
46. Suhonen JO, Peterson DA, Ray J, Gage FH. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature. 1996 Oct 17;383(6601):624-627
47. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005 Sep;3(9):e283.
48. Martin GR, Evans MJ. Differentiation of clonal lines of teratocarcinoma cells: Formation of embryoid bodies in vitro. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1441-1445
49. Schuldiner M, Yanuka O, Itskovitz-Eldor J, Melton DA, Benvenisty N. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11307-11312
50. Carpenter MK, Inokuma MS, Denham J, Mujtaba T, Chiu CP, Rao MS. Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol. 2001 Dec;172(2):383-397 (Pubitemid 34075087)
51. Hong S, Kang UJ, Isacson O, Kim KS. Neural precursors derived from human embryonic stem cells maintain long-term proliferation without losing the potential to differentiate into all three neural lineages, including dopaminergic neurons. J Neurochem. 2008 Jan;104(2): 316-324
52. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci. 2005 May 11;25(19):4694-4705
53. Schulz TC, Palmarini GM, Noggle SA, Weiler DA, Mitalipova MM, Condie BG. Directed neuronal differentiation of human embryonic stem cells. BMC Neurosci. 2003 Oct 22;4:27.
54. Vazin T, Chen J, Lee CT, Amable R, Freed WJ. Assessment of stromalderived inducing activity in the generation of dopaminergic neurons from human embryonic stem cells. Stem Cells. 2008 Jun;26(6):1517-1525
55. Baharvand H, Mehrjardi NZ, Hatami M, Kiani S, Rao M, Haghighi MM. Neural differentiation from human embryonic stem cells in a defined adherent culture condition. Int J Dev Biol. 2007;51(5):371-378
56. Erceg S, Lainez S, Ronaghi M, Stojkovic P, Perez-Arago MA, Moreno- Manzano V, Moreno-Palanques R, Planells-Cases R, Stojkovic M. Differentiation of human embryonic stem cells to regional specific neural precursors in chemically defined medium conditions. PLoS One. 2008;3(5):e2122.
57. Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R. Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci U S A. 2003 Oct 28;100(22): 12741-12746 (Pubitemid 37339969)
58. Reubinoff BE, Itsykson P, Turetsky T, Pera MF, Reinhartz E, Itzik A, Ben-Hur T. Neural progenitors from human embryonic stem cells. Nat Biotech. 2001;19(12):1134-1140
59. Schuldiner M, Eiges R, Eden A, Yanuka O, Itskovitz-Eldor J, Goldstein RS, Benvenisty N. Induced neuronal differentiation of human embryonic stem cells. Brain Res. 2001 Sep 21;913(2):201-205 (Pubitemid 32817068)
60. Gerrard L, Rodgers L, Cui W. Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells. 2005 Oct;23(9):1234-1241
61. Itsykson P, Ilouz N, Turetsky T, Goldstein RS, Pera MF, Fishbein I, Segal M, Reubinoff BE. Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol Cell Neurosci. 2005 Sep;30(1):24-36.
62. Pera MF, Andrade J, Houssami S, Reubinoff B, Trounson A, Stanley EG, Ward-van Oostwaard D, Mummery C. Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J Cell Sci. 2004 Mar 1;117(Pt 7):1269-1280
63. Tabert MH, Liu X, Doty RL, Serby M, Zamora D, Pelton GH, Marder K, Albers MW, Stern Y, Devanand DP. A 10-item smell identification scale related to risk for Alzheimers disease. Ann Neurol. 2005 Jul;58(1): 155-160
64. Gasser T. Molecular pathogenesis of Parkinson disease: insights from genetic studies. Expert Rev Mol Med. 2009;11:e22.
65. Gasser T. Genomic and proteomic biomarkers for Parkinson disease. Neurology. 2009 Feb 17;72(7 Suppl):S27-31.
66. Davie CA. A review of Parkinsons disease. Br Med Bull. 2008;86:109-127
67. Zeviani M. Mitochondrial disorders. Suppl Clin Neurophysiol. 2004;57:304-312
68. Wallace DC. Mitochondrial diseases in man and mouse. Science. 1999 Mar 5;283(5407):1482-1488
69. Bosbach S, Kornblum C, Schroder R, Wagner M. Executive and visuospatial deficits in patients with chronic progressive external ophthalmoplegia and Kearns-Sayre syndrome. Brain. 2003 May;126(Pt 5): 1231-1240
70. Goto Y, Nonaka I, Horai S. A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature. 1990 Dec 13;348(6302):651-653
71. Shoffner JM, Lott MT, Lezza AM, Seibel P, Ballinger SW, Wallace DC. Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation. Cell. 1990 Jun 15;61(6):931-937
72. Huoponen K, Vilkki J, Aula P, Nikoskelainen EK, Savontaus ML. A new mtDNA mutation associated with Leber hereditary optic neuroretinopathy. Am J Hum Genet. 1991 Jun;48(6):1147-1153
73. Wallace DC, Singh G, Lott MT, Hodge JA, Schurr TG, Lezza AM, Elsas LJ, 2nd, Nikoskelainen EK. Mitochondrial DNA mutation associated with Lebers hereditary optic neuropathy. Science. 1988 Dec 9;242(4884):1427-1430
74. Kirby DM, McFarland R, Ohtake A, Dunning C, Ryan MT, Wilson C, Ketteridge D, Turnbull DM, Thorburn DR, Taylor RW. Mutations of the mitochondrial ND1 gene as a cause of MELAS. J Med Genet. 2004 Oct;41(10):784-789
75. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A. 2003 Apr 1;100(7): 4078-4083
76. Liu J, Lillo C, Jonsson PA, Vande Velde C, Ward CM, Miller TM, Subramaniam JR, Rothstein JD, Marklund S, Andersen PM, Brannstrom T, Gredal O, Wong PC, Williams DS, Cleveland DW. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron. 2004 Jul 8;43(1):5-17.
77. Pasinelli P, Belford ME, Lennon N, Bacskai BJ, Hyman BT, Trotti D, Brown RH, Jr. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron. 2004 Jul 8;43(1):19-30.
78. Chang KT, Min KT. Drosophila melanogaster homolog of Down syndrome critical region 1 is critical for mitochondrial function. Nat Neurosci. 2005 Nov;8(11):1577-1585
79. Schapira AH. Mitochondrial disease. Lancet. 2006 Jul 1;368(9529):70-82.
80. Jacobs LJ, de Coo IF, Nijland JG, Galjaard RJ, Los FJ, Schoonderwoerd K, Niermeijer MF, Geraedts JP, Scholte HR, Smeets HJ. Transmission and prenatal diagnosis of the T9176C mitochondrial DNA mutation. Mol Hum Reprod. 2005 Mar;11(3):223-228
81. Holt IJ, Harding AE, Morgan-Hughes JA. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature. 1988 Feb 25;331(6158):717-719
82. Lightowlers RN, Chinnery PF, Turnbull DM, Howell N. Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet. 1997 Nov;13(11):450-455
83. Papa S, Petruzzella V, Scacco S, Vergari R, Panelli D, Tamborra R, Corsi P, Picciariello M, Lambo R, Bertini E, Santorelli FM. Respiratory complex I in brain development and genetic disease. Neurochem Res. 2004 Mar;29(3):547-560
84. Kirby DM, Rennie KJ, Smulders-Srinivasan TK, Acin-Perez R, Whittington M, Enriquez JA, Trevelyan AJ, Turnbull DM, Lightowlers RN. Transmitochondrial embryonic stem cells containing pathogenic mtDNA mutations are compromised in neuronal differentiation. Cell Prolif. 2009 Aug;42(4):413-424
85. Atamna H, Frey WH, 2nd. Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimers disease. Mitochondrion. 2007 Sep;7(5):297-310.
86. Kraytsberg Y, Kudryavtseva E, McKee AC, Geula C, Kowall NW, Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat Genet. 2006 May;38(5):518-520
87. Bender A, Krishnan KJ, Morris CM, Taylor GA, Reeve AK, Perry RH, Jaros E, Hersheson JS, Betts J, Klopstock T, Taylor RW, Turnbull DM. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat Genet. 2006 May;38(5):515-517
88. Parker WD, Jr., Parks JK, Swerdlow RH. Complex I deficiency in Parkinsons disease frontal cortex. Brain Res. 2008 Jan 16;1189:215-218
89. Hattingen E, Magerkurth J, Pilatus U, Mozer A, Seifried C, Steinmetz H, Zanella F, Hilker R. Phosphorus and proton magnetic resonance spectroscopy demonstrates mitochondrial dysfunction in early and advanced Parkinsons disease. Brain. 2009 Dec;132(Pt 12):3285-3297
90. Parker WD, Jr., Parks J, Filley CM, Kleinschmidt-DeMasters BK. Electron transport chain defects in Alzheimers disease brain. Neurology. 1994 Jun;44(6):1090-1096
91. Ghosh SS, Swerdlow RH, Miller SW, Sheeman B, Parker WD, Jr., Davis RE. Use of cytoplasmic hybrid cell lines for elucidating the role of mitochondrial dysfunction in Alzheimers disease and Parkinsons disease. Ann N Y Acad Sci. 1999;893:176-191
92. Swerdlow RH, Parks JK, Miller SW, Tuttle JB, Trimmer PA, Sheehan JP, Bennett JP, Jr., Davis RE, Parker WD, Jr. Origin and functional consequences of the complex I defect in Parkinsons disease. Ann Neurol. 1996 Oct;40(4):663-671
93. Borland MK, Mohanakumar KP, Rubinstein JD, Keeney PM, Xie J, Capaldi R, Dunham LD, Trimmer PA, Bennett JP, Jr. Relationships among molecular genetic and respiratory properties of Parkinsons disease cybrid cells show similarities to Parkinsons brain tissues. Biochim Biophys Acta. 2009 Jan;1792(1):68-74.
94. Khan SM, Cassarino DS, Abramova NN, Keeney PM, Borland MK, Trimmer PA, Krebs CT, Bennett JC, Parks JK, Swerdlow RH, Parker WD, Jr., Bennett JP, Jr. Alzheimers disease cybrids replicate betaamyloid abnormalities through cell death pathways. Ann Neurol. 2000 Aug;48(2):148-155
95. Trimmer PA, Bennett JP, Jr. The cybrid model of sporadic Parkinsons disease. Exp Neurol. 2009 Aug;218(2):320-325
96. Trimmer PA, Swerdlow RH, Parks JK, Keeney P, Bennett JP, Jr., Miller SW, Davis RE, Parker WD, Jr. Abnormal mitochondrial morphology in sporadic Parkinsons and Alzheimers disease cybrid cell lines. Exp Neurol. 2000 Mar;162(1):37-50.
97. Abraham S, Eroshenko N, Rao RR. Role of bioinspired polymers in determination of pluripotent stem cell fate. Regen Med. 2009 Jul;4(4): 561-578
98. Huttner WB, Kosodo Y. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr Opin Cell Biol. 2005 Dec;17(6):648-657
99. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2008 Jan;26(1):101-106
100. 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 Nov 30;131(5):861-872
101. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006 Aug 25;126(4):663-676
102. Yamanaka S. [Molecular mechanisms underlying pluripotency of embryonic stem cells]. Seikagaku. 2006 Jan;78(1):27-33.
103. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin, II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007 Dec 21;318(5858):1917-1920
104. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008 Aug 29;321(5893):1218-1221
105. Ebert AD, Yu J, Rose FF, Jr., Mattis VB, Lorson CL, Thomson JA, Svendsen CN. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature. 2009 Jan 15;457(7227):277-280
106. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, Le Paslier D, Frézal J, Cohen D, Weissenbach J, Munnich A, Melki J. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995 Jan 13;80(1):155-165
107. Crawford TO, Pardo CA. The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis. 1996 Apr;3(2):97-110.
108. Lefebvre S, Burlet P, Liu Q, Bertrandy S, Clermont O, Munnich A, Dreyfuss G, Melki J. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet. 1997 Jul;16(3):265-269
109. Schmid A, DiDonato CJ. Animal models of spinal muscular atrophy. J Child Neurol. 2007 Aug;22(8):1004-1012
110. Wilson PG, Cherry JJ, Schwamberger S, Adams AM, Zhou J, Shin S, Stice SL. An SMA project report: neural cell-based assays derived from human embryonic stem cells. Stem Cells Dev. 2007 Dec;16(6): 1027-1041
111. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ. Disease-specific induced pluripotent stem cells. Cell. 2008 Sep 5;134(5):877-886
112. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, Isacson O, Jaenisch R. Parkinsons disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell. 2009 Mar 6;136(5):964-977
113. Wernig M, Zhao JP, Pruszak J, Hedlund E, Fu D, Soldner F, Broccoli V, Constantine-Paton M, Isacson O, Jaenisch R. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinsons disease. Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5856-5861
114. Mendez I, Sanchez-Pernaute R, Cooper O, Vinuela A, Ferrari D, Bjorklund L, Dagher A, Isacson O. Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinsons disease. Brain. 2005 Jul;128(Pt 7): 1498-1510
115. Kordower JH, Freeman TB, Snow BJ, Vingerhoets FJ, Mufson EJ, Sanberg PR, Hauser RA, Smith DA, Nauert GM, Perl DP, Olanow CW. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinsons disease. N Engl J Med. 1995 Apr 27;332(17):1118-1124
116. Piccini P, Brooks DJ, Bjorklund A, Gunn RN, Grasby PM, Rimoldi O, Brundin P, Hagell P, Rehncrona S, Widner H, Lindvall O. Dopamine release from nigral transplants visualized in vivo in a Parkinsons patient. Nat Neurosci. 1999 Dec;2(12):1137-1140
117. Freed CR, Greene PE, Breeze RE, Tsai WY, DuMouchel W, Kao R, Dillon S, Winfield H, Culver S, Trojanowski JQ, Eidelberg D, Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinsons disease. N Engl J Med. 2001 Mar 8;344(10):710-719
118. Lindvall O, Bjorklund A. Cell therapy in Parkinsons disease. NeuroRx. 2004 Oct;1(4):382-393
119. Schulz TC, Noggle SA, Palmarini GM, Weiler DA, Lyons IG, Pensa KA, Meedeniya AC, Davidson BP, Lambert NA, Condie BG. Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells. 2004;22(7):1218-1238
120. Roy NS, Cleren C, Singh SK, Yang L, Beal MF, Goldman SA. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med. 2006 Nov;12(11):1259-1268
121. Bjorklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2344-2349
122. Cho MS, Lee YE, Kim JY, Chung S, Cho YH, Kim DS, Kang SM, Lee H, Kim MH, Kim JH, Leem JW, Oh SK, Choi YM, Hwang DY, Chang JW, Kim DW. Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3392-3397
123. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest. 2005 Jan;115(1):102-109
124. Yang D, Zhang ZJ, Oldenburg M, Ayala M, Zhang SC. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells. 2008 Jan;26(1):55-63.
125. Chiba S, Lee YM, Zhou W, Freed CR. Noggin enhances dopamine neuron production from human embryonic stem cells and improves behavioral outcome after transplantation into Parkinsonian rats. Stem Cells. 2008 Nov;26(11):2810-2820
126. Srivastava AS, Malhotra R, Sharp J, Berggren T. Potentials of ES cell therapy in neurodegenerative diseases. Curr Pharm Des. 2008;14(36):3873-3879
127. Borlongan CV, Tajima Y, Trojanowski JQ, Lee VM, Sanberg PR. Cerebral ischemia and CNS transplantation: differential effects of grafted fetal rat striatal cells and human neurons derived from a clonal cell line. Neuroreport. 1998 Nov 16;9(16):3703-3709
128. Muir JK, Raghupathi R, Saatman KE, Wilson CA, Lee VM, Trojanowski JQ, Philips MF, McIntosh TK. Terminally differentiated human neurons survive and integrate following transplantation into the traumatically injured rat brain. J Neurotrauma. 1999 May;16(5):403-414
129. Buhnemann C, Scholz A, Bernreuther C, Malik CY, Braun H, Schachner M, Reymann KG, Dihne M. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain. 2006 Dec;129(Pt 12):3238-3248
130. Li XJ, Du ZW, Zarnowska ED, Pankratz M, Hansen LO, Pearce RA, Zhang SC. Specification of motoneurons from human embryonic stem cells. Nat Biotechnol. 2005 Feb;23(2):215-221
131. Shin S, Dalton S, Stice SL. Human motor neuron differentiation from human embryonic stem cells. Stem Cells Dev. 2005 Jun;14(3):266-269 (Pubitemid 40885250)
132. Singh Roy N, Nakano T, Xuing L, Kang J, Nedergaard M, Goldman SA. Enhancer-specified GFP-based FACS purification of human spinal motor neurons from embryonic stem cells. Exp Neurol. 2005 Dec;196(2):224-234
133. Garbuzova-Davis S, Willing AE, Milliken M, Saporta S, Zigova T, Cahill DW, Sanberg PR. Positive effect of transplantation of hNT neurons (NTera 2/D1 cell-line) in a model of familial amyotrophic lateral sclerosis. Exp Neurol. 2002 Apr;174(2):169-180
134. Kendall AL, Rayment FD, Torres EM, Baker HF, Ridley RM, Dunnett SB. Functional integration of striatal allografts in a primate model of Huntingtons disease. Nat Med. 1998 Jun;4(6):727-729
135. Liu S, Qu Y, Stewart TJ, Howard MJ, Chakrabortty S, Holekamp TF, McDonald JW. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci U S A. 2000 May 23;97(11):6126-6131
136. Kang SM, Cho MS, Seo H, Yoon CJ, Oh SK, Choi YM, Kim DW. Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells. 2007 Feb;25(2):419-424
137. Brustle O, Jones KN, Learish RD, Karram K, Choudhary K, Wiestler OD, Duncan ID, McKay RD. Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science. 1999 Jul 30;285(5428):754-756
138. Glaser T, Perez-Bouza A, Klein K, Brustle O. Generation of purified oligodendrocyte progenitors from embryonic stem cells. Faseb J. 2005 Jan;19(1):112-114
139. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia. 2005 Feb;49(3): 385-396
140. Burt RK, Loh Y, Cohen B, Stefoski D, Balabanov R, Katsamakis G, Oyama Y, Russell EJ, Stern J, Muraro P, Rose J, Testori A, Bucha J, Jovanovic B, Milanetti F, Storek J, Voltarelli JC, Burns WH. Autologous non-myeloablative haemopoietic stem cell transplantation in relapsingremitting multiple sclerosis: A phase I/II study. Lancet Neurol. 2009 Mar;8(3):244-253
141. Iyer S, Thomas RR, Portell FR, Dunham LD, Quigley CK, Bennett JP, Jr. Recombinant mitochondrial transcription factor A with N-terminal mitochondrial transduction domain increases respiration and mitochondrial gene expression. Mitochondrion. 2009 Jun;9(3):196-203.
142. Khan SM, Bennett JP, Jr. Development of mitochondrial gene replacement therapy. J Bioenerg Biomembr. 2004 Aug;36(4):387-393
143. Khan SM, Smigrodzki RM, Swerdlow RH. Cell and animal models of mtDNA biology: Progress and prospects. Am J Physiol Cell Physiol. 2007 Feb;292(2):C658-69.
144. Keeney PM, Quigley CK, Dunham LD, Papageorge CM, Iyer S, Thomas RR, Schwarz KM, Trimmer PA, Khan SM, Portell FR, Bergquist KE, Bennett JP, Jr. Mitochondrial gene therapy augments mitochondrial physiology in a Parkinsons disease cell model. Hum Gene Ther. 2009 Aug;20(8):897-907.
145. Mitalipova MM, Rao RR, Hoyer DM, Johnson JA, Meisner LF, Jones KL, Dalton S, Stice SL. Preserving the genetic integrity of human embryonic stem cells. Nat Biotechnol. 2005 Jan;23(1):19-20. (Pubitemid 41724618)