Application of human induced pluripotent stem cells for modeling and treating neurodegenerative diseases

New Biotechnology

Volumn 32, Issue 1, 2015, Pages 212-228

  Payne, Natalie L ^a   Sylvain, Aude ^a   O'Brien, Carmel ^b,c   Herszfeld, Daniella ^a   Sun, Guizhi ^a   Bernard, Claude C A ^a  

^a Monash University   (Australia)

^b CSIRO   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DIAGNOSIS; NEURONS; REPAIR; STEM CELLS;

ALZHEIMER'S DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; DISEASE PHENOTYPES; DOPAMINERGIC NEURONS; HUMAN-INDUCED PLURIPOTENT STEM CELLS; MULTIPLE SCLEROSIS; PARKINSON'S DISEASE; REGENERATIVE MEDICINE;

NEURODEGENERATIVE DISEASES;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN CELL; CAENORHABDITIS ELEGANS; CELL RENEWAL; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; HUMAN; IN VITRO STUDY; MOTONEURON; MULTIPLE SCLEROSIS; NONHUMAN; NUCLEAR REPROGRAMMING; OLIGODENDROGLIA; PARKINSON DISEASE; PHENOTYPE; PLURIPOTENT STEM CELL; PRIMATE; STEM CELL TRANSPLANTATION; ZEBRA FISH; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; NEURODEGENERATIVE DISEASES; PATHOLOGY;

CELL DIFFERENTIATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; STEM CELL TRANSPLANTATION;

EID: 84912117942     PISSN: 18716784     EISSN: 18764347     Source Type: Journal    
DOI: 10.1016/j.nbt.2014.05.001     Document Type: Article

References (185)

1. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-666.
2. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
3. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
4. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
5. Park I.H., Arora N., Huo H., Maherali N., Ahfeldt T., Shimamura A., et al. Disease-specific induced pluripotent stem cells. Cell 2008, 134:877-886.
6. Kola I., Landis J. Can the pharmaceutical industry reduce attrition rates. Nat Rev Drug Discov 2004, 3:711-715.
7. Stadtfeld M., Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev 2010, 24:2239-2263.
8. Wang S., Bates J., Li X., Schanz S., Chandler-Militello D., Levine C., et al. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013, 12:252-264.
9. Franklin R.J., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008, 9:839-855.
10. Goldman S.A., Nedergaard M., Windrem M.S. Glial progenitor cell-based treatment and modeling of neurological disease. Science 2012, 338:491-495.
11. O'Brien C., Laslett A.L. Suspended in culture - human pluripotent cells for scalable technologies. Stem Cell Res 2012, 9:167-170.
12. Serra M., Brito C., Correia C., Alves P.M. Process engineering of human pluripotent stem cells for clinical application. Trends Biotechnol 2012, 30:350-359.
13. Fluri D.A., Tonge P.D., Song H., Baptista R.P., Shakiba N., Shukla S., et al. Derivation, expansion and differentiation of induced pluripotent stem cells in continuous suspension cultures. Nat Methods 2012, 9:509-516.
14. Shafa M., Day B., Yamashita A., Meng G., Liu S., Krawetz R., et al. Derivation of iPSCs in stirred suspension bioreactors. Nat Methods 2012, 9:465-466.
15. Gore A., Li Z., Fung H.-L., Young J.E., Agarwal S., Antosiewicz-Bourget J., et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011, 471:63-67.
16. Hussein S.M., Batada N.N., Vuoristo S., Ching R.W., Autio R., Narva E., et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011, 471:58-62.
17. Laurent L.C., Ulitsky I., Slavin I., Tran H., Schork A., Morey R., et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 2011, 8:106-118.
18. Martins-Taylor K., Xu R.-H. Concise review: genomic stability of human induced pluripotent stem cells. Stem Cells 2012, 30:22-27.
19. Abyzov A., Mariani J., Palejev D., Zhang Y., Haney M.S., Tomasini L., et al. Somatic copy number mosaicism in human skin revealed by induced pluripotent stem cells. Nature 2012, 492:438-442.
20. Quinlan A.R., Boland M.J., Leibowitz M.L., Shumilina S., Pehrson S.M., Baldwin K.K., et al. Genome sequencing of mouse induced pluripotent stem cells reveals retroelement stability and infrequent DNA rearrangement during reprogramming. Cell Stem Cell 2011, 9:366-373.
21. Kim K., Zhao R., Doi A., Ng K., Unternaehrer J., Cahan P., et al. Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat Biotechnol 2011, 29:1117-1119.
22. Ohi Y., Qin H., Hong C., Blouin L., Polo J.M., Guo T., et al. Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol 2011, 13:541-549.
23. Lister R., Pelizzola M., Kida Y.S., Hawkins R.D., Nery J.R., Hon G., et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011, 471:68-73.
24. Doi A., Park I.H., Wen B., Murakami P., Aryee M.J., Irizarry R., et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 2009, 41:1350-1353.
25. Mekhoubad S., Bock C., de Boer A.S., Kiskinis E., Meissner A., Eggan K. Erosion of dosage compensation impacts human iPSC disease modeling. Cell Stem Cell 2012, 10:595-609.
26. O'Brien C., Lambshead J., Chy H., Zhou Q., Wang Y.-C., Laslett A.L. Analysis and purification techniques for human pluripotent stem cells. Human stem cell manual: a laboratory guide 2012, 223-248. Elsevier, Amsterdam. S.E. Petersen, J.F. Loring (Eds.).
27. Tan H.L., Fong W.J., Lee E.H., Yap M., Choo A. mAb 84, a cytotoxic antibody that kills undifferentiated human embryonic stem cells via oncosis. Stem Cells 2009, 27:1792-1801.
28. Bieberich E., Silva J., Wang G.H., Krishnamurthy K., Condie B.G. Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 2004, 167:723-734.
29. Smith A.J., Nelson N.G., Oommen S., Hartjes K.A., Folmes C.D. Apoptotic susceptibility to DNA damage of pluripotent stem cells facilitates pharmacologic purging of teratoma risk. Stem Cells Transl Med 2012, 1:709-718.
30. Andrews P.W., Banting G., Damjanov I., Arnaud D., Avner P. Three monoclonal antibodies defining distinct differentiation antigens associated with different high molecular weight polypeptides on the surface of human embryonal carcinoma cells. Hybridoma 1984, 3:347-361.
31. Kannagi R., Levery S.B., Ishigami F., Hakomori S., Shevinsky L.H., Knowles B.B., et al. New globoseries glycosphingolipids in human teratocarcinoma reactive with the monoclonal antibody directed to a developmentally regulated antigen, stage-specific embryonic antigen 3. J Biol Chem 1983, 258:8934-8942.
32. Kannagi R., Cochran N.A., Ishigami F., Hakomori S., Andrews P.W., Knowles B.B., et al. Stage-specific embryonic antigens (SSEA-3 and SSEA-4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J 1983, 2:2355-2361.
33. Pera M.F., Blasco-Lafita M.J., Cooper S., Mason M., Mills J., Monaghan P. Analysis of cell-differentiation lineage in human teratomas using new monoclonal antibodies to cytostructural antigens of embryonal carcinoma cells. Differentiation 1988, 39:139-149.
34. Pera M.F., Filipczyk A.A., Hawes S.M., Laslett A.L. Isolation, characterization, and differentiation of human embryonic stem cells. Methods Enzymol 2003, 365:429-446.
35. Tang C., Lee A.S., Volkmer J.-P., Sahoo D., Nag D., Mosley A.R., et al. An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat Biotechnol 2011, 29:829-834.
36. Choo A.B., Tan H.L., Ang S.N., Fong W.J., Chin A., Lo J., et al. Selection against undifferentiated human embryonic stem cells by a cytotoxic antibody recognizing podocalyxin-like protein-1. Stem Cells 2008, 26:1454-1463.
37. Son Y.S., Park J.H., Kang Y.K., Park J.S., Choi H.S., Lim J.Y., et al. Heat shock 70-kDa protein 8 isoform 1 is expressed on the surface of human embryonic stem cells and downregulated upon differentiation. Stem Cells 2005, 23:1502-1513.
38. Laslett A.L., Filipczyk A.A., Pera M.F. Characterization and culture of human embryonic stem cells. Trends Cardiovasc Med 2003, 13:295-301.
39. Wang Y.-C., Nakagawa M., Garitaonandia I., Slavin I., Altun G., Lacharite R.M., et al. Specific lectin biomarkers for isolation of human pluripotent stem cells identified through array-based glycomic analysis. Cell Res 2011, 21:1551-1563.
40. Tateno H., Toyota M., Saito S., Onuma Y., Ito Y., Hiemori K., et al. Glycome diagnosis of human induced pluripotent stem cells using lectin microarray. J Biol Chem 2011, 286:20345-20353.
41. Fong C.Y., Peh G.S., Gauthaman K., Bongso A. Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS). Stem Cell Rev 2009, 5:72-80.
42. Laslett A.L., Grimmond S., Gardiner B., Stamp L., Lin A., Hawes S.M., et al. Transcriptional analysis of early lineage commitment in human embryonic stem cells. BMC Dev Biol 2007, 7:12.
43. Hough S.R., Laslett A.L., Grimmond S.B., Kolle G., Pera M.F. A continuum of cell states spans pluripotency and lineage commitment in human embryonic stem cells. PLoS ONE 2009, 4:e7708.
44. Kolle G., Ho M., Zhou Q., Chy H.S., Krishnan K., Cloonan N., et al. Identification of human embryonic stem cell surface markers by combined membrane-polysome translation state array analysis and immunotranscriptional profiling. Stem Cells 2009, 27:2446-2456.
45. Polanco J.C., Ho M.S.H., Wang B., Zhou Q., Wolvetang E., Mason E., et al. Identification of unsafe human induced pluripotent stem cell lines using a robust surrogate assay for pluripotency. Stem Cells 2013, 31:1498-1510.
46. Mackay-Sim A. Patient-derived stem cells: pathways to drug discovery for brain diseases. Front Cell Neurosci 2013, 7:29.
47. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Sudhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
48. Han D.W., Tapia N., Hermann A., Hemmer K., Hoing S., Arauzo-Bravo M.J., et al. Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 2012, 10:465-472.
49. Thier M., Worsdorfer P., Lakes Y.B., Gorris R., Herms S., Opitz T., et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012, 10:473-479.
50. Yuan S.H., Martin J., Elia J., Flippin J., Paramban R.I., Hefferan M.P., et al. Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 2011, 6:e17540.
51. Israel M.A., Yuan S.H., Bardy C., Reyna S.M., Mu Y., Herrera C., et al. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 2012, 482:216-220.
52. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
53. Lancaster M.A., Renner M., Martin C.A., Wenzel D., Bicknell L.S., Hurles M., et al. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501:373-379.
54. Soldner F., Laganiere J., Cheng A.W., Hockemeyer D., Gao Q., Alagappan R., et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 2011, 146:318-331.
55. Liu G.H., Qu J., Suzuki K., Nivet E., Li M., Montserrat N., et al. Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 2012, 491:603-607.
56. Regal L., Vanopdenbosch L., Tilkin P., Van den Bosch L., Thijs V., Sciot R., et al. The G93C mutation in superoxide dismutase 1: clinicopathologic phenotype and prognosis. Arch Neurol 2006, 63:262-267.
57. Cookson M.R., van der Brug M. Cell systems and the toxic mechanism(s) of alpha-synuclein. Exp Neurol 2008, 209:5-11.
58. Giudice A., Trounson A. Genetic modification of human embryonic stem cells for derivation of target cells. Cell Stem Cell 2008, 2:422-433.
59. Saxena S., Caroni P. Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 2011, 71:35-48.
60. Miller R.G., Mitchell J.D., Lyon M., Moore D.H. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev 2007, CD001447.
61. Andersen P.M., Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: what do we really know. Nat Rev Neurol 2011, 7:603-615.
62. Rosen D.R. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 364:2.
63. Bendotti C., Marino M., Cheroni C., Fontana E., Crippa V., Poletti A., et al. Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response. Prog Neurobiol 2012, 97:101-126.
64. Chen S., Zhang X., Song L., Le W. Autophagy dysregulation in amyotrophic lateral sclerosis. Brain Pathol 2012, 22:110-116.
65. Kabashi E., Valdmanis P.N., Dion P., Spiegelman D., McConkey B.J., Vande Velde C., et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 2008, 40:572-574.
66. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
67. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
68. Vance C., Rogelj B., Hortobagyi T., De Vos K.J., Nishimura A.L., Sreedharan J., et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
69. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
70. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
71. Tsao W., Jeong Y.H., Lin S., Ling J., Price D.L., Chiang P.M., et al. Rodent models of TDP-43: recent advances. Brain Res 2012, 1462:26-39.
72. Lanson N.A., Pandey U.B. FUS-related proteinopathies: lessons from animal models. Brain Res 2012, 1462:44-60.
73. Teng Y.D., Benn S.C., Kalkanis S.N., Shefner J.M., Onario R.C., Cheng B., et al. Multimodal actions of neural stem cells in a mouse model of ALS: a meta-analysis. Sci Transl Med 2012, 4. 165ra164.
74. Wyatt T.J., Rossi S.L., Siegenthaler M.M., Frame J., Robles R., Nistor G., et al. Human motor neuron progenitor transplantation leads to endogenous neuronal sparing in 3 models of motor neuron loss. Stem Cells Int 2011, 2011:207230.
75. Popescu I.R., Nicaise C., Liu S., Bisch G., Knippenberg S., Daubie V., et al. Neural progenitors derived from human induced pluripotent stem cells survive and differentiate upon transplantation into a rat model of amyotrophic lateral sclerosis. Stem Cells Transl Med 2013, 2:167-174.
76. Nizzardo M., Simone C., Rizzo F., Ruggieri M., Salani S., Riboldi G., et al. Minimally invasive transplantation of iPSC-derived ALDHhiSSCloVLA4+ neural stem cells effectively improves the phenotype of an amyotrophic lateral sclerosis model. Hum Mol Genet 2014, 23:342-354.
77. Xu L., Yan J., Chen D., Welsh A.M., Hazel T., Johe K., et al. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 2006, 82:865-875.
78. Cizkova D., Kakinohana O., Kucharova K., Marsala S., Johe K., Hazel T., et al. Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 2007, 147:546-560.
79. Xu L., Ryugo D.K., Pongstaporn T., Johe K., Koliatsos V.E. Human neural stem cell grafts in the spinal cord of SOD1 transgenic rats: differentiation and structural integration into the segmental motor circuitry. J Comp Neurol 2009, 514:297-309.
80. Glass J.D., Boulis N.M., Johe K., Rutkove S.B., Federici T., Polak M., et al. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells 2012, 30:1144-1151.
81. Riley J., Federici T., Park J., Suzuki M., Franz C.K., Tork C., et al. Cervical spinal cord therapeutics delivery: preclinical safety validation of a stabilized microinjection platform. Neurosurgery 2009, 65:754-761.
82. O'Connor D.M., Boulis N.M. Cellular and molecular approaches to motor neuron therapy in amyotrophic lateral sclerosis and spinal muscular atrophy. Neurosci Lett 2012, 527:78-84.
83. Di Giorgio F.P., Carrasco M.A., Siao M.C., Maniatis T., Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 2007, 10:608-614.
84. Nagai M., Re D.B., Nagata T., Chalazonitis A., Jessell T.M., Wichterle H., et al. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 2007, 10:615-622.
85. 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.
86. Di Giorgio F.P., Boulting G.L., Bobrowicz S., Eggan K.C. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 2008, 3:637-648.
87. Haidet-Phillips A.M., Hester M.E., Miranda C.J., Meyer K., Braun L., Frakes A., et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 2011, 29:824-828.
88. Mitne-Neto M., Machado-Costa M., Marchetto M.C., Bengtson M.H., Joazeiro C.A., Tsuda H., et al. Downregulation of VAPB expression in motor neurons derived from induced pluripotent stem cells of ALS8 patients. Hum Mol Genet 2011, 20:3642-3652.
89. Egawa N., Kitaoka S., Tsukita K., Naitoh M., Takahashi K., Yamamoto T., et al. Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci Transl Med 2012, 4. 145ra104.
90. Bilican B., Serio A., Barmada S.J., Nishimura A.L., Sullivan G.J., Carrasco M., et al. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci USA 2012, 109:5803-5808.
91. Serio A., Bilican B., Barmada S.J., Ando D.M., Zhao C., Siller R., et al. Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proc Natl Acad Sci USA 2013, 110:4697-4702.
92. Burkhardt M.F., Martinez F.J., Wright S., Ramos C., Volfson D., Mason M., et al. A cellular model for sporadic ALS using patient-derived induced pluripotent stem cells. Mol Cell Neurosci 2013, 56:355-364.
93. Almeida S., Gascon E., Tran H., Chou H.J., Gendron T.F., et al. Modeling key pathological features of frontotemporal dementia with C9ORF72 repeat expansion in iPSC-derived human neurons. Acta Neuropathol 2013, 126:385-399.
94. Sareen D., O'Rourke J.G., Meera P., Muhammad A.K., Grant S., et al. Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci Transl Med 2013, 5. 208ra149.
95. Donnelly C.J., Zhang P.W., Pham J.T., Heusler A.R., Mistry N.A., et al. RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013, 80:415-428.
96. Teuling E., Ahmed S., Haasdijk E., Demmers J., Steinmetz M.O., Akhmanova A., et al. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci 2007, 27:9801-9815.
97. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
98. Kabashi E., Lin L., Tradewell M.L., Dion P.A., Bercier V., Bourgouin P., et al. Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 2010, 19:671-683.
99. Farg M.A., Sundaramoorthy V., Sultana J.M., Yang S., Atkinson R.A., Levina V., et al. C9ORF72, implicated in amytrophic lateral sclerosis and frontotemporal dementia, regulates endosomal trafficking. Hum Mol Genet 2014, [Epub February 27]. 10.1093/hmg/ddu068.
100. Marques O., Outeiro T.F. Alpha-synuclein: from secretion to dysfunction and death. Cell Death Dis 2012, 3:e350.
101. Samii A., Nutt J.G., Ransom B.R. Parkinson's disease. Lancet 2004, 363:1783-1793.
102. Lesage S., Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet 2009, 18:R48-R59.
103. Biedler J.L., Roffler-Tarlov S., Schachner M., Freedman L.S. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 1978, 38:3751-3757.
104. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 1976, 73:2424-2428.
105. Brundin P., Strecker R.E., Lindvall O., Isacson O., Nilsson O.G., Barbin G., et al. Intracerebral grafting of dopamine neurons. Experimental basis for clinical trials in patients with Parkinson's disease. Ann N Y Acad Sci 1987, 495:473-496.
106. Carlsson T., Carta M., Winkler C., Bjorklund A., Kirik D. Serotonin neuron transplants exacerbate L-DOPA-induced dyskinesias in a rat model of Parkinson's disease. J Neurosci 2007, 27:8011-8022.
107. Breysse N., Carlsson T., Winkler C., Bjorklund A., Kirik D. The functional impact of the intrastriatal dopamine neuron grafts in parkinsonian rats is reduced with advancing disease. J Neurosci 2007, 27:5849-5856.
108. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotech 2009, 27:275-280.
109. Badger J.L., Cordero-Llana O., Hartfield E.M., Wade-Martins R. Parkinson's disease in a dish - using stem cells as a molecular tool. Neuropharmacology 2014, 76:A:88-A:96.
110. Takagi Y., Takahashi J., Saiki H., Morizane A., Hayashi T., Kishi Y., et al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 2005, 115:102-109.
111. Kim J.H., Auerbach J.M., Rodriguez-Gomez J.A., Velasco I., Gavin D., Lumelsky N., et al. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 2002, 418:50-56.
112. Kriks S., Shim J.W., Piao J., Ganat Y.M., Wakeman D.R., Xie Z., et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011, 480:547-551.
113. Wernig M., Zhao J.P., Pruszak J., Hedlund E., Fu D., Soldner F., et al. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci USA 2008, 105:5856-5861.
114. Rhee Y.H., Ko J.Y., Chang M.Y., Yi S.H., Kim D., Kim C.H., et al. Protein-based human iPS cells efficiently generate functional dopamine neurons and can treat a rat model of Parkinson disease. J Clin Invest 2011, 121:2326-2335.
115. Hargus G., Cooper O., Deleidi M., Levy A., Lee K., Marlow E., 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 USA 2010, 107:15921-15926.
116. Emborg M.E., Liu Y., Xi J., Zhang X., Yin Y., Lu J., et al. Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep 2013, 3:646-650.
117. Sundberg M., Bogetofte H., Lawson T., Jansson J., Smith G., Astradsson A., et al. Improved cell therapy protocols for Parkinson's disease based on differentiation efficiency and safety of hESC-, hiPSC-, and non-human primate iPSC-derived dopaminergic neurons. Stem Cells 2013, 31:1548-1562.
118. Soldner F., Hockemeyer D., Beard C., Gao Q., Bell G.W., Cook E.G., et al. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009, 136:964-977.
119. Cooper O., Hargus G., Deleidi M., Blak A., Osborn T., Marlow E., 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.
120. Byers B., Cord B., Nguyen H.N., Schule B., Fenno L., Lee P.C., et al. SNCA triplication Parkinson's patient's iPSC-derived DA neurons accumulate alpha-synuclein and are susceptible to oxidative stress. PLoS One 2011, 6:e26159.
121. Devine M.J., Ryten M., Vodicka P., Thomson A.J., Burdon T., Houlden H., et al. Parkinson's disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat Commun 2011, 2:440.
122. Ryan S.D., Dolatabadi N., Chan S.F., Zhang X., Akhtar M.W., et al. Isogenic human iPSC Parkinson's model shows nitrosative stress-induced dysfunction in MEF2-PGC1α transcription. Cell 2013, 155:1351-1364.
123. 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.
124. Nguyen H.N., Byers B., Cord B., Shcheglovitov A., Byrne J., Gujar P., et al. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 2011, 8:267-280.
125. Sanchez-Danes A., Richaud-Patin Y., Carballo-Carbajal I., Jimenez-Delgado S., Caig C., Mora S., 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.
126. Sanders L.H., Laganière J., Cooper O., Mak S.K., Vu B.J., Huang Y.A., et al. LRRK2 mutations cause mitochondrial DNA damage in iPSC-derived neural cells from Parkinson's disease patients: reversal by gene correction. Neurobiol Dis 2014, 62:381-386.
127. Jiang H., Ren Y., Yuen E.Y., Zhong P., Ghaedi M., Hu Z., et al. Parkin controls dopamine utilization in human midbrain dopaminergic neurons derived from induced pluripotent stem cells. Nat Commun 2012, 3:668.
128. Imaizumi Y., Okada Y., Akamatsu W., Koike M., Kuzumaki N., Hayakawa H., et al. Mitochondrial dysfunction associated with increased oxidative stress and alpha-synuclein accumulation in PARK2 iPSC-derived neurons and postmortem brain tissue. Mol Brain 2012, 5:35.
129. Paisan-Ruiz C., Lang A.E., Kawarai T., Sato C., Salehi-Rad S., Fisman G.K., et al. LRRK2 gene in Parkinson disease: mutation analysis and case control association study. Neurology 2005, 65:696-700.
130. Kachergus J., Mata I.F., Hulihan M., Taylor J.P., Lincoln S., Aasly J., et al. Identification of a novel LRRK2 mutation linked to autosomal dominant parkinsonism: evidence of a common founder across European populations. Am J Hum Genet 2005, 76:672-680.
131. Cookson M.R. alpha-synuclein and neuronal cell death. Mol Neurodegener 2009, 4:9.
132. Reinhardt P., Schmid B., Burbulla L.F., Schondorf D.C., Wagner L., Glatza M., et al. Genetic correction of a LRRK2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-dependent changes in gene expression. Cell Stem Cell 2013, 12:354-367.
133. Goldstein L.S. Axonal transport and neurodegenerative disease: can we see the elephant?. Prog Neurobiol 2012, 99:186-190.
134. Herrmann N., Chau S.A., Kircanski I., Lanctot K.L. Current and emerging drug treatment options for Alzheimer's disease: a systematic review. Drugs 2011, 71:2031-2065.
135. St George-Hyslop P.H. Genetic factors in the genesis of Alzheimer's disease. Ann N Y Acad Sci 2000, 924:1-7.
136. Brunholz S., Sisodia S., Lorenzo A., Deyts C., Kins S., Morfini G. Axonal transport of APP and the spatial regulation of APP cleavage and function in neuronal cells. Exp Brain Res 2012, 217:353-364.
137. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
138. Wolfe M.S. When loss is gain: reduced presenilin proteolytic function leads to increased Abeta42/Abeta40. Talking point on the role of presenilin mutations in Alzheimer disease. EMBO Rep 2007, 8:136-140.
139. Wicklund L., Leao R.N., Stromberg A.M., Mousavi M., Hovatta O., Nordberg A., et al. Beta-amyloid 1-42 oligomers impair function of human embryonic stem cell-derived forebrain cholinergic neurons. PLoS One 2010, 5:e15600.
140. Sun B., Halabisky B., Zhou Y., Palop J.J., Yu G., Mucke L., et al. Imbalance between GABAergic and glutamatergic transmission impairs adult neurogenesis in an animal model of Alzheimer's disease. Cell Stem Cell 2009, 5:624-633.
141. Khandekar N., Lie K.H., Sachdev P.S., Sidhu K.S. Amyloid precursor proteins, neural differentiation of pluripotent stem cells and its relevance to Alzheimer's disease. Stem Cells Dev 2012, 21:997-1006.
142. Avramopoulos D. Genetics of Alzheimer's disease: recent advances. Genome Med 2009, 1:34.
143. Bettens K., Sleegers K., Van Broeckhoven C. Genetic insights in Alzheimer's disease. Lancet Neurol 2013, 12:92-104.
144. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., et al. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991, 30:572-580.
145. Blurton-Jones M., Kitazawa M., Martinez-Coria H., Castello N.A., Muller F.J., Loring J.F., et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci USA 2009, 106:13594-13599.
146. Hampton D.W., Webber D.J., Bilican B., Goedert M., Spillantini M.G., Chandran S. Cell-mediated neuroprotection in a mouse model of human tauopathy. J Neurosci 2010, 30:9973-9983.
147. Chen W.W., Blurton-Jones M. Concise review: can stem cells be used to treat or model Alzheimer's disease. Stem Cells 2012, 30:2612-2618.
148. Fan X., Sun D., Tang X., Cai Y., Yin Z.Q., Xu H. Stem-cell challenges in the treatment of Alzheimer's disease: a long way from bench to bedside. Med Res Rev 2014, [Epub February 5]. 10.1002/med.21309.
149. Yagi T., Ito D., Okada Y., Akamatsu W., Nihei Y., Yoshizaki T., et al. Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum Mol Genet 2011, 20:453-459.
150. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
151. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., et al. Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 2003, 100:10417-10422.
152. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
153. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008, 14:837-842.
154. Noguchi A., Matsumura S., Dezawa M., Tada M., Yanazawa M., Ito A., et al. Isolation and characterization of patient-derived, toxic, high mass amyloid beta-protein (Abeta) assembly from Alzheimer disease brains. J Biol Chem 2009, 284:32895-32905.
155. Kondo T., Asai M., Tsukita K., Kutoku Y., Ohsawa Y., Sunada Y., et al. Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular Aβ and differential drug responsiveness. Cell Stem Cell 2013, 12:487-496.
156. Yahata N., Asai M., Kitaoka S., Takahashi K., Asaka I., Hioki H., 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.
157. Xu X., Lei Y., Luo J., Wang J., Zhang S., Yang X.J., et al. Prevention of beta-amyloid induced toxicity in human iPS cell-derived neurons by inhibition of Cyclin-dependent kinases and associated cell cycle events. Stem Cell Res 2013, 10:213-227.
158. Ontaneda D., Hyland M., Cohen J.A. Multiple sclerosis: new insights in pathogenesis and novel therapeutics. Annu Rev Med 2012, 63:389-404.
159. Giovannoni G., Southam E., Waubant E. Systematic review of disease-modifying therapies to assess unmet needs in multiple sclerosis: tolerability and adherence. Mult Scler 2012, 18:932-946.
160. Sawcer S., Hellenthal G., Pirinen M., Spencer C.C., Patsopoulos N.A., Moutsianas L., et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011, 476:214-219.
161. Baranzini S.E., Nickles D. Genetics of multiple sclerosis: swimming in an ocean of data. Curr Opin Neurol 2012, 25:239-245.
162. Gourraud P.A., Harbo H.F., Hauser S.L., Baranzini S.E. The genetics of multiple sclerosis: an up-to-date review. Immunol Rev 2012, 248:87-103.
163. Stys P.K., Zamponi G.W., van Minnen J., Geurts J.J. Will the real multiple sclerosis please stand up?. Nat Rev Neurosci 2012, 13:507-514.
164. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., et al. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 2003, 422:688-694.
165. Pluchino S., Zanotti L., Rossi B., Brambilla E., Ottoboni L., Salani G., et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005, 436:266-271.
166. Einstein O., Karussis D., Grigoriadis N., Mizrachi-Kol R., Reinhartz E., Abramsky O., et al. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 2003, 24:1074-1082.
167. Einstein O., Grigoriadis N., Mizrachi-Kol R., Reinhartz E., Polyzoidou E., Lavon I., et al. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp Neurol 2006, 198:275-284.
168. Einstein O., Fainstein N., Vaknin I., Mizrachi-Kol R., Reihartz E., Grigoriadis N., et al. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 2007, 61:209-218.
169. Aharonowiz M., Einstein O., Fainstein N., Lassmann H., Reubinoff B., Ben-Hur T. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS One 2008, 3:e3145.
170. Ben-Hur T., van Heeswijk R.B., Einstein O., Aharonowiz M., Xue R., Frost E.E., et al. Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn Reson Med 2007, 57:164-171.
171. Payne N.L., Sun G., Herszfeld D., Tat-Goh P.A., Verma P.J., Parkington H.C., et al. Comparative study on the therapeutic potential of neurally differentiated stem cells in a mouse model of multiple sclerosis. PLoS One 2012, 7:e35093.
172. Giannakopoulou A., Grigoriadis N., Polyzoidou E., Lourbopoulos A., Michaloudi E., Papadopoulos G.C. Time-dependent fate of transplanted neural precursor cells in experimental autoimmune encephalomyelitis mice. Exp Neurol 2011, 230:16-26.
173. Muja N., Cohen M.E., Zhang J., Kim H., Gilad A.A., Walczak P., et al. Neural precursors exhibit distinctly different patterns of cell migration upon transplantation during either the acute or chronic phase of EAE: a serial MR imaging study. Magn Reson Med 2011, 65:1738-1749.
174. Kim H., Walczak P., Kerr C., Galpoththawela C., Gilad A.A., Muja N., et al. Immunomodulation by transplanted human embryonic stem cell-derived oligodendroglial progenitors in experimental autoimmune encephalomyelitis. Stem Cells 2012, 30:2820-2829.
175. Laterza C., Merlini A., De Feo D., Ruffini F., Menon R., Onorati M., et al. iPSC-derived neural precursors exert a neuroprotective role in immune-mediated demyelination via the secretion of LIF. Nat Commun 2013, 4:2597.
176. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006, 129:3165-3172.
177. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 2005, 25:4694-4705.
178. Izrael M., Zhang P., Kaufman R., Shinder V., Ella R., Amit M., et al. Human oligodendrocytes derived from embryonic stem cells: Effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Mol Cell Neurosci 2007, 34:310-323.
179. Windrem M.S., Nunes M.C., Rashbaum W.K., Schwartz T.H., Goodman R.A., McKhann G., et al. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 2004, 10:93-97.
180. Windrem M.S., Schanz S.J., Guo M., Tian G.F., Washco V., Stanwood N., et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008, 2:553-565.
181. Yang N., Zuchero J.B., Ahlenius H., Marro S., Ng Y.H., Vierbuchen T., et al. Generation of oligodendroglial cells by direct lineage conversion. Nat Biotechnol 2013, 31:434-439.
182. Najm F.J., Lager A.M., Zaremba A., Wyatt K., Caprariello A.V., Factor D.C., et al. Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat Biotechnol 2013, 31:426-433.
183. Song B., Sun G., Herszfeld D., Sylvain A., Campanale N.V., Hirst C.E., et al. Neural differentiation of patient specific iPS cells as a novel approach to study the pathophysiology of multiple sclerosis. Stem Cell Res 2012, 8:259-273.
184. Matigian N., Abrahamsen G., Sutharsan R., Cook A.L., Vitale A.M., Nouwens A., et al. Disease-specific, neurosphere-derived cells as models for brain disorders. Dis Model Mech 2010, 3:785-798.
185. 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. 124ra29.