Modeling motor neuron disease: The matter of time

Trends in Neurosciences

Volumn 37, Issue 11, 2014, Pages 642-652

  Arbab, Mandana ^a,b   Baars, Susanne ^a   Geijsen, Niels ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; CELL AGING; CELL TYPE; EMBRYONIC STEM CELL; HUMAN; IN VITRO STUDY; MODEL; MOTOR NEURON DISEASE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; ONSET AGE; PHENOTYPE; PLURIPOTENT STEM CELL; REVIEW; SIGNAL TRANSDUCTION; SPINAL MUSCULAR ATROPHY; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DISEASE MODEL; MOTONEURON; NEURODEGENERATIVE DISEASES; PHYSIOLOGY; STEM CELL; TIME;

ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; HUMANS; MOTOR NEURONS; NEURODEGENERATIVE DISEASES; STEM CELLS; TIME FACTORS;

EID: 84910077290     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2014.07.008     Document Type: Review

References (137)

1. Bellin M., et al. Induced pluripotent stem cells: the new patient?. Nat. Rev. Mol. Cell Biol. 2012, 13:713-726.
2. Dimos J.T., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
3. Bilican B., et al. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5803-5808.
4. Park I.H., et al. Disease-specific induced pluripotent stem (iPS) cells. Cell 2008, 134:877-886.
5. Ebert A., et al. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2008, 457:277-280.
6. Corti S., et al. Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy. Sci. Transl. Med. 2012, 4:165ra162.
7. Sareen D., et al. Inhibition of apoptosis blocks human motor neuron cell death in a stem cell model of spinal muscular atrophy. PLoS ONE 2012, 7:e39113.
8. Young R.A. Control of embryonic stem cell state. Cell 2012, 144:940-954.
9. Thomson J.A., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
10. Gurdon J.B. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 1962, 10:622-640.
11. Wilmut I., et al. Viable offspring derived from fetal and adult mammalian cells. Nature 1999, 385:810-814.
12. Tada M., et al. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr. Biol. 2001, 11:1553-1558.
13. Hochedlinger K., Jaenisch R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 2002, 415:1035-1038.
14. Cowan C.A., et al. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 2005, 309:1369-1373.
15. Takahashi K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
16. Stadtfeld M., Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev. 2010, 24:2239-2263.
17. Mikkelsen T.S., et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 2009, 454:49-55.
18. Guenther M.G., et al. Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 2011, 7:249-257.
19. Wernig M., et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007, 448:318-324.
20. Wichterle H., et al. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
21. Ying Q-L., et al. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 2003, 21:183-186.
22. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
23. Li X-J., et al. Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 2005, 23:215-221.
24. Chambers S., Fasano C. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 2009, 27:275-280.
25. Amoroso M.W., et al. Accelerated high-yield generation of limb-innervating motor neurons from human stem cells. J. Neurosci. 2013, 33:574-586.
26. Karumbayaram S., et al. Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 2009, 27:806-811.
27. Takazawa T., et al. Maturation of spinal motor neurons derived from human embryonic stem cells. PLoS ONE 2012, 7:e40154.
28. Hester M.E., et al. Rapid and efficient generation of functional motor neurons from human pluripotent stem cells using gene delivered transcription factor codes. Mol. Ther. 2011, 19:1905-1912.
29. Tsuchida T., et al. Topographic organization embryonic motor neurons defined by expression of LIM homeobox genes. Cell 1994, 79:957-970.
30. William C.M. Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins. Development 2003, 130:1523-1536.
31. Dasen J.S., et al. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 2005, 123:477-491.
32. Dalla Torre di Sanguinetto S.A., et al. Transcriptional mechanisms controlling motor neuron diversity and connectivity. Curr. Opin. Neurobiol. 2008, 18:36-43.
33. Rekling J.C., et al. Synaptic control of motoneuronal excitability. Physiol. Rev. 2000, 80:767-852.
34. Lee H., et al. Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 2007, 25:1931-1939.
35. Friese A., et al. Gamma and alpha motor neurons distinguished by expression of transcription factor Err3. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13588-13593.
36. Shneider N.A., et al. Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival. Neural Dev. 2009, 4:42.
37. Frey D., et al. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 2000, 20:2534-2542.
38. Chakkalakal J.V., et al. Retrograde influence of muscle fibers on their innervation revealed by a novel marker for slow motoneurons. Development 2010, 137:3489-3499.
39. Egawa N., et al. Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci. Transl. Med. 2012, 4:145ra104.
40. Hu B-Y., et al. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4335-4340.
41. Saxena S., Caroni P. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 2007, 83:174-191.
42. Pun S., et al. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat. Neurosci. 2006, 9:408-419.
43. Burkhardt M.F., et al. A cellular model for sporadic ALS using patient-derived induced pluripotent stem cells. Mol. Cell. Neurosci. 2013, 56:355-364.
44. Patterson M., et al. Defining the nature of human pluripotent stem cell progeny. Cell Res. 2012, 22:178-193.
45. + T cells. Cell Stem Cell 2013, 12:31-36.
46. Nishimura T., et al. Generation of rejuvenated antigen-specific T cells by reprogramming to pluripotency and redifferentiation. Cell Stem Cell 2013, 12:114-126.
47. Abranches E., et al. Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo. PLoS ONE 2009, 4:e6286.
48. Kehat I., et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 2001, 108:363-364.
49. Laflamme M.A., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 2007, 25:1015-1024.
50. Spence J.R., et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011, 470:105-109.
51. Knickmeyer R., et al. A structural MRI study of human brain development from birth to 2 years. J. Neurosci. 2008, 28:12176-12182.
52. Kaplan A., et al. Neuronal matrix metalloproteinase-9 is a determinant of selective neurodegeneration. Neuron 2014, 81:333-348.
53. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013, 14:R115.
54. Batista L.F., et al. Telomere shortening and loss of self-renewal in dyskeratosis congenita induced pluripotent stem cells. Nature 2011, 474:399-402.
55. Nguyen H., et al. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 2011, 8:267-280.
56. Nishitoh H., et al. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 2008, 22:1451-1464.
57. García M.L., et al. Mitochondria, motor neurons and aging. J. Neurol. Sci. 2013, 330:18-26.
58. Sim F.J., et al. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J. Neurosci. 2002, 22:2451-2459.
59. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005, 58:495-505.
60. Estévez A.G., et al. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 1999, 286:2498-2500.
61. Wiedau-Pazos M., et al. Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science 1996, 271:515-518.
62. Manfredi G., Xu Z. Mitochondrial dysfunction and its role in motor neuron degeneration in ALS. Mitochondrion 2005, 5:77-87.
63. Qian W., et al. PP2A regulates tau phosphorylation directly and also indirectly via activating GSK-3β. J. Alzheimers Dis. 2010, 19:1221-1229.
64. Conboy M.J., et al. Heterochronic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging Cell 2013, 12:525-530.
65. Conboy I.M., et al. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433:760-764.
66. Carlson M., et al. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 2009, 8:676-689.
67. Loffredo F.S., et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell 2013, 153:828-839.
68. Sinha M., et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014, 344:649-652.
69. Katsimpardi L., et al. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 2014, 344:630-634.
70. Elabd C., et al. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat. Commun. 2014, 5:1-11.
71. Conboy I.M., et al. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302:1575-1577.
72. Brack A.S., et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317:807-810.
73. Villeda S.a., et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
74. Ruckh J., et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 2012, 10:96-103.
75. Edgar J.M., Nave K-A. The role of CNS glia in preserving axon function. Curr. Opin. Neurobiol. 2009, 19:498-504.
76. Tikka T.M., et al. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 2002, 125:722-731.
77. Nagaraja T.N., et al. Neurofilament phosphorylation is enhanced in cultured chick spinal cord neurons exposed to cerebrospinal fluid from amyotrophic lateral sclerosis patients. Acta Neuropathol. 1994, 88:349-352.
78. Couratier P., et al. Cell culture evidence for neuronal degeneration in amyotrophic lateral sclerosis being linked to glutamate AMPA/kainate receptors. Lancet 1993, 341:265-268.
79. Wolfgram F., Myers L. Amyotrophic lateral sclerosis: effect of serum on anterior horn cells in tissue culture. Science 1973, 179:579-580.
80. Scaffidi P., Misteli T. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat. Cell Biol. 2008, 10:452-459.
81. Decker M.L., et al. Telomere length in Hutchinson-Gilford progeria syndrome. Mech. Ageing Dev. 2009, 130:377-383.
82. Kudlow B.A., et al. Suppression of proliferative defects associated with processing-defective lamin A mutants by hTERT or inactivation of p53. Mol. Cell. Biol. 2008, 19:5238-5248.
83. Liu B., et al. Genomic instability in laminopathy-based premature aging. Nat. Med. 2005, 11:780-785.
84. d'Adda di Fagagna F., et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
85. Liu G., et al. Recapitulation of premature aging with iPSCs from Hutchinson- Gilford progeria syndrome. Nature 2011, 472:221-225.
86. Zhang J., et al. A human iPSC model of Hutchinson-Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 2011, 8:31-45.
87. Nissan X., et al. Unique preservation of neural cells in Hutchinson-Gilford progeria syndrome is due to the expression of the neural-specific miR-9 microRNA. Cell Rep. 2012, 2:1-9.
88. Miller J.D., et al. Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 2013, 13:691-705.
89. Merideth M.A., et al. Phenotype and course of Hutchinson-Gilford progeria syndrome. N. Engl. J. Med. 2008, 358:592-604.
90. Wheless J.W., Kim H.L. Adolescent seizures and epilepsy syndromes. Epilepsia 2002, 43(Suppl. 3):33-52.
91. Markham J.A. Sex steroids and schizophrenia. Rev. Endocr. Metab. Disord. 2012, 13:187-207.
92. Pilch J., et al. Topical review: Friedreich's ataxia. J. Child Neurol. 2002, 17:315-319.
93. Tella S.H., Gallagher J.C. Prevention and treatment of postmenopausal osteoporosis. J. Steroid Biochem. Mol. Biol. 2014, 142:155-170.
94. Key T., et al. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J. Natl. Cancer Inst. 2002, 94:606-616.
95. Son E.Y., et al. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 2011, 9:205-218.
96. Park H-W., et al. Directed induction of functional motor neuron-like cells from genetically engineered human mesenchymal stem cells. PLoS ONE 2012, 7:e35244.
97. Chiò A., et al. Epidemiology of ALS in Italy: a 10-year prospective population-based study. Neurology 2009, 72:725-731.
98. Kanning K.C., et al. Motor neuron diversity in development and disease. Annu. Rev. Neurosci. 2010, 33:409-440.
99. van Es M.A., et al. Large-scale SOD1 mutation screening provides evidence for genetic heterogeneity in amyotrophic lateral sclerosis. J. Neurol. 2010, 81:562-566.
100. Chiò A., et al. Clinical characteristics of patients with familial amyotrophic lateral sclerosis carrying the pathogenic GGGGCC hexanucleotide repeat expansion of C9ORF72. Brain 2012, 135:784-793.
101. Li T., et al. Comparison of sporadic and familial disease amongst 580 cases of motor neuron disease. J. Neurol. Neurosurg. Psychiatry 1988, 51:778-784.
102. Majounie E., et al. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 2012, 11:323-330.
103. Rosen D.R., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
104. Howland D., et al. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1604-1609.
105. Sreedharan J., et al. TDP-43 Mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1671.
106. Kabashi E., et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:572-574.
107. Vance C., et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
108. Kwiatkowski T.J., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
109. Elden A., et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS Andrew. Nature 2010, 466:1069-1075.
110. Ross O.A., et al. Ataxin-2 repeat-length variation and neurodegeneration. Hum. Mol. Genet. 2011, 20:3207-3212.
111. Farg M.A., et al. Ataxin-2 interacts with FUS and intermediate-length polyglutamine expansions enhance FUS-related pathology in amyotrophic lateral sclerosis. Hum. Mol. Genet. 2013, 22:717-728.
112. Hart M., Gitler A. ALS-associated ataxin 2 polyQ expansions enhance stress- induced caspase 3 activation and increase TDP-43 pathological modifications. J. Neurosci. 2012, 32:9133-9142.
113. Nihei Y., et al. Roles of ataxin-2 in pathological cascades mediated by TAR DNA-binding protein 43 (TDP-43) and Fused in Sarcoma (FUS). J. Biol. Chem. 2012, 287:41310-41323.
114. Kim S.H., et al. Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J. Biol. Chem. 2010, 285:34097-34105.
115. Andersen P.M., Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: what do we really know?. Nat. Rev. Neurol. 2011, 7:603-615.
116. Prudencio M., et al. Variation in aggregation propensities among ALS-associated variants of SOD1: correlation to human disease. Hum. Mol. Genet. 2009, 18:3217-3226.
117. Keller B.A., et al. Co-aggregation of RNA binding proteins in ALS spinal motor neurons: evidence of a common pathogenic mechanism. Acta Neuropathol. 2012, 124:733-747.
118. Bruijn L.I., et al. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 1998, 281:1851-1854.
119. Neumann M., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
120. Blokhuis A.M., et al. Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 2013, 125:777-794.
121. Arnold E.S., et al. ALS-linked TDP-43 mutations produce aberrant RNA splicing and adult-onset motor neuron disease without aggregation or loss of nuclear TDP-43. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E736-E745.
122. Tummala H., et al. Inhibition of chaperone activity is a shared property of several Cu, Zn-superoxide dismutase mutants that cause amyotrophic lateral sclerosis. J. Biol. Chem. 2005, 280:17725-17731.
123. Kabashi E., et al. Focal dysfunction of the proteasome: a pathogenic factor in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 2004, 89:1325-1335.
124. Puttaparthi K., Elliott J.L. Non-neuronal induction of immunoproteasome subunits in an ALS model: possible mediation by cytokines. Exp. Neurol. 2005, 196:441-451.
125. Paushkin S., et al. The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 2002, 14:305-312.
126. Zhang Z., et al. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 2008, 133:585-600.
127. Gabanella F., et al. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS ONE 2007, 2:e921.
128. Schrank B., Götz R. Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:9920-9925.
129. Wirth B., et al. Mildly affected patients with spinal muscular atrophy are partially protected by an increased SMN2 copy number. Hum. Genet. 2006, 119:422-428.
130. Talbot K., Davies K.E. Spinal muscular atrophy. Semin. Neurol. 2001, 21:189-197.
131. Murray L.M., et al. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum. Mol. Genet. 2008, 17:949-962.
132. Lefebvre S., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995, 80:155-165.
133. McGovern V.L., et al. Embryonic motor axon development in the severe SMA mouse. Hum. Mol. Genet. 2008, 17:2900-2909.
134. Pellizzoni L. Chaperoning ribonucleoprotein biogenesis in health and disease. EMBO Rep. 2007, 8:340-345.
135. Pearn J. Classification of spinal muscular atrophies. Lancet 1980, 1:919-922.
136. -/- mice and results in a mouse with spinal muscular atrophy. Hum. Mol. Genet. 2000, 9:333-339.
137. Kugelberg E., Welander L. Heredofamilial juvenile muscular atrophy simulating muscular dystrophy. AMA Arch. Neurol. Psychiatry 1956, 75:500-509.