Amyotrophic lateral sclerosis: mechanisms and therapeutics in the epigenomic era
Tóm tắt
Từ khóa
Tài liệu tham khảo
Robberecht, W. & Philips, T. The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14, 248–264 (2013).
Hardiman, O., van den Berg, L. H. & Kiernan, M. C. Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat. Rev. Neurol. 7, 639–649 (2011).
Kurian, K. M., Forbes, R. B., Colville, S. & Swingler, R. J. Cause of death and clinical grading criteria in a cohort of amyotrophic lateral sclerosis cases undergoing autopsy from the Scottish Motor Neurone Disease Register. J. Neurol. Neurosurg. Psychiatry 80, 84–87 (2009).
Al-Chalabi, A. & Hardiman, O. The epidemiology of ALS: a conspiracy of genes, environment and time. Nat. Rev. Neurol. 9, 617–628 (2013).
Traxinger, K., Kelly, C., Johnson, B. A., Lyles, R. H. & Glass, J. D. Prognosis and epidemiology of amyotrophic lateral sclerosis: Analysis of a clinic population, 1997–2011. Neurology 3, 313–320 (2013).
Blackhall, L. J. Amyotrophic lateral sclerosis and palliative care: where we are, and the road ahead. Muscle Nerve 45, 311–318 (2012).
Chiò, A. et al. Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J. Neurol. Neurosurg. Psychiatry 82, 740–746 (2011).
Vinsant, S. et al. Characterization of early pathogenesis in the SOD1G93A mouse model of ALS: part I, background and methods. Brain Behav. 3, 335–350 (2013).
Simon, N. G. et al. Quantifying disease progression in amyotrophic lateral sclerosis. Ann. Neurol. 76, 643–657 (2014).
Ling, S. C., Polymenidou, M. & Cleveland, D. W. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 79, 416–438 (2013).
Murphy, J. M. et al. Continuum of frontal lobe impairment in amyotrophic lateral sclerosis. Arch. Neurol. 64, 530–534 (2007).
Ringholz, G. M. et al. Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology 65, 586–590 (2005).
Dion, P. A., Daoud, H. & Rouleau, G. A. Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Nat. Rev. Genet. 10, 769–782 (2009).
Diekstra, F. P. et al. C9orf72 and UNC13A are shared risk loci for amyotrophic lateral sclerosis and frontotemporal dementia: a genome-wide meta-analysis. Ann. Neurol. 76, 120–133 (2014).
Matus, S., Medinas, D. B. & Hetz, C. Common ground: stem cell approaches find shared pathways underlying ALS. Cell Stem Cell 14, 697–699 (2014).
Renton, A. E., Chio, A. & Traynor, B. J. State of play in amyotrophic lateral sclerosis genetics. Nat. Neurosci. 17, 17–23 (2014).
Vucic, S., Rothstein, J. D. & Kiernan, M. C. Advances in treating amyotrophic lateral sclerosis: insights from pathophysiological studies. Trends Neurosci. (2014).
Ahmed, A. & Wicklund, M. P. Amyotrophic lateral sclerosis: what role does environment play? Neurol. Clin. 29, 689–711 (2011).
Al-Chalabi, A. et al. Genetic and epigenetic studies of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Frontotemporal Degener. 14 (Suppl. 1), 44–52 (2013).
Figueroa-Romero, C. et al. Identification of epigenetically altered genes in sporadic amyotrophic lateral sclerosis. PLoS ONE 7, e52672 (2012).
Kanekura, K., Suzuki, H., Aiso, S. & Matsuoka, M. ER stress and unfolded protein response in amyotrophic lateral sclerosis. Mol. Neurobiol. 39, 81–89 (2009).
Moloney, E. B., de Winter, F. & Verhaagen, J. ALS as a distal axonopathy: molecular mechanisms affecting neuromuscular junction stability in the presymptomatic stages of the disease. Front. Neurosci. 8, 252 (2014).
Strong, M. J. et al. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol. Cell. Neurosci. 35, 320–327 (2007).
He, C. Z. & Hays, A. P. Expression of peripherin in ubiquinated inclusions of amyotrophic lateral sclerosis. J. Neurol. Sci. 217, 47–54 (2004).
Corbo, M. & Hays, A. P. Peripherin and neurofilament protein coexist in spinal spheroids of motor neuron disease. J. Neuropathol. Exp. Neurol. 51, 531–537 (1992).
Ishtiaq, M., Campos-Melo, D., Volkening, K. & Strong, M. J. Analysis of novel NEFL mRNA targeting microRNAs in amyotrophic lateral sclerosis. PLoS ONE 9, e85653 (2014).
Voigt, A. et al. TDP-43-mediated neuron loss in vivo requires RNA-binding activity. PLoS ONE 5, e12247 (2010).
Narayanan, R. K. et al. Identification of RNA bound to the TDP-43 ribonucleoprotein complex in the adult mouse brain. Amyotroph. Lateral Scler. Frontotemporal Degener. 14, 252–260 (2013).
Meyerowitz, J. et al. C-Jun N-terminal kinase controls TDP-43 accumulation in stress granules induced by oxidative stress. Mol. Neurodegener. 6, 57 (2011).
Freibaum, B. D., Chitta, R. K., High, A. A. & Taylor, J. P. Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J. Proteome Res. 9, 1104–1120 (2010).
Neumann, M. et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130–133 (2006).
Yamazaki, T. et al. FUS-SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Rep. 2, 799–806 (2012).
Marangi, G. & Traynor, B. J. Genetic causes of amyotrophic lateral sclerosis: New genetic analysis methodologies entailing new opportunities and challenges. Brain Res. 1607, 75–93 (2015).
Boillee, S. et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312, 1389–1392 (2006).
Niikura, T., Kita, Y. & Abe, Y. SUMO3 modification accelerates the aggregation of ALS-linked SOD1 mutants. PLoS ONE 9, e101080 (2014).
Su, X. W., Broach, J. R., Connor, J. R., Gerhard, G. S. & Simmons, Z. Genetic heterogeneity of amyotrophic lateral sclerosis: implications for clinical practice and research. Muscle Nerve 49, 786–803 (2014).
Okado-Matsumoto, A. & Fridovich, I. Amyotrophic lateral sclerosis: a proposed mechanism. Proc. Natl Acad. Sci. USA 99, 9010–9014 (2002).
Turner, B. J., Ackerley, S., Davies, K. E. & Talbot, K. Dismutase-competent SOD1 mutant accumulation in myelinating Schwann cells is not detrimental to normal or transgenic ALS model mice. Hum. Mol. Genet. 19, 815–824 (2010).
Lobsiger, C. S. et al. Schwann cells expressing dismutase active mutant SOD1 unexpectedly slow disease progression in ALS mice. Proc. Natl Acad. Sci. USA 106, 4465–4470 (2009).
Liu, J. et al. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43, 5–17 (2004).
Polymenidou, M. & Cleveland, D. W. Prion-like spread of protein aggregates in neurodegeneration. J. Exp. Med. 209, 889–893 (2012).
Araki, T. et al. Misfolded SOD1 forms high-density molecular complexes with synaptic molecules in mutant SOD1-linked familial amyotrophic lateral sclerosis cases. J. Neurol. Sci. 314, 92–96 (2012).
Toivonen, J. M. et al. MicroRNA-206: a potential circulating biomarker candidate for amyotrophic lateral sclerosis. PLoS ONE 9, e89065 (2014).
Honda, D. et al. The ALS/FTLD-related RNA-binding proteins TDP-43 and FUS have common downstream RNA targets in cortical neurons. FEBS Open Bio 4, 1–10 (2013).
Buratti, E. et al. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J. Biol. Chem. 280, 37572–37584 (2005).
Johnson, B. S. et al. TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. J. Biol. Chem. 284, 20329–20339 (2009).
Kim, S. H., Shanware, N. P., Bowler, M. J. & Tibbetts, R. S. Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J. Biol. Chem. 285, 34097–34105 (2010).
Vance, C. et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208–1211 (2009).
Kwiatkowski, T. J. Jr et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205–1208 (2009).
Brown, J. A. et al. SOD1, ANG, TARDBP and FUS mutations in amyotrophic lateral sclerosis: a United States clinical testing lab experience. Amyotroph. Lateral Scler. 13, 217–222 (2012).
Lattante, S., Rouleau, G. A. & Kabashi, E. TARDBP and FUS mutations associated with amyotrophic lateral sclerosis: summary and update. Hum. Mutat. 34, 812–826 (2013).
Groen, E. J. et al. ALS-associated mutations in FUS disrupt the axonal distribution and function of SMN. Hum. Mol. Genet. 22, 3690–3704 (2013).
Paez-Colasante, X. et al. Improvement of neuromuscular synaptic phenotypes without enhanced survival and motor function in severe spinal muscular atrophy mice selectively rescued in motor neurons. PLoS ONE 8, e75866 (2013).
Droppelmann, C. A., Campos-Melo, D., Ishtiaq, M., Volkening, K. & Strong, M. J. RNA metabolism in ALS: when normal processes become pathological. Amyotroph. Lateral Scler. Frontotemporal Degener. 15, 321–336 (2014).
Dewey, C. M. et al. TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol. Cell. Bio. 31, 1098–1108 (2011).
Liu-Yesucevitz, L. et al. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS ONE 5, e13250 (2010).
Volkening, K., Leystra-Lantz, C., Yang, W., Jaffee, H. & Strong, M. J. Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS). Brain Res. 1305, 168–182 (2009).
Renton, A. E. et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72, 257–68 (2011).
DeJesus-Hernandez, M. et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72, 245–256 (2011).
Wicks, P. et al. SOD1 and cognitive dysfunction in familial amyotrophic lateral sclerosis. J. Neurol. 256, 234–241 (2009).
Borroni, B. et al. Mutation within TARDBP leads to frontotemporal dementia without motor neuron disease. Hum. Mut. 30, E974–E983 (2009).
Broustal, O. et al. FUS mutations in frontotemporal lobar degeneration with amyotrophic lateral sclerosis. J. Alzheimer Dis. 22, 765–769 (2010).
Xi, Z. et al. Hypermethylation of the CpG island near the G4C2 repeat in ALS with a C9orf72 expansion. Am. J. Hum. Genet. 92, 981–989 (2013).
Sareen, D. et al. Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci. Transl. Med. 5, 208ra149 (2013).
Ash, P. E. et al. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 77, 639–646 (2013).
Zhang, Y. J. et al. Aggregation-prone c9FTD/ALS poly(GA) RAN-translated proteins cause neurotoxicity by inducing ER stress. Acta Neuropathol. 128, 505–524 (2014).
Donnelly, C. J. et al. RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 80, 415–428 (2013).
Kwon, I. et al. Poly-dipeptides encoded by the C9orf72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science 345, 1139–1145 (2014).
Morris, H. R., Waite, A. J., Williams, N. M., Neal, J. W. & Blake, D. J. Recent advances in the genetics of the ALS-FTLD complex. Curr. Neurol. Neurosci. Rep. 12, 243–250 (2012).
Johnson, J. O. et al. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat. Neurosci. 17, 664–666 (2014).
Takanashi, K. & Yamaguchi, A. Aggregation of ALS-linked FUS mutant sequesters RNA binding proteins and impairs RNA granules formation. Biochem. Biophys. Res. Commun. 452, 600–607 (2014).
D'Ambrogio, A. et al. Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. Nucleic Acids Res. 37, 4116–4126 (2009).
Kim, H. J. et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495, 467–473 (2013).
Hirano, M. et al. Senataxin mutations and amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 12, 223–227 (2011).
Bannwarth, S. et al. Reply: Mutations in the CHCHD10 gene are a common cause of familial amyotrophic lateral sclerosis. Brain 137, e312 (2014).
Muller, K. et al. Two novel mutations in conserved codons indicate that CHCHD10 is a gene associated with motor neuron disease. Brain 137, e309 (2014).
Baker, M. et al. Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442, 916–919 (2006).
Gellera, C. et al. Identification of new ANG gene mutations in a large cohort of Italian patients with amyotrophic lateral sclerosis. Neurogenetics 9, 33–40 (2008).
Giordana, M. T. et al. Dementia and cognitive impairment in amyotrophic lateral sclerosis: a review. Neurol. Sci. 32, 9–16 (2011).
Wu, C. H. et al. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488, 499–503 (2012).
Johnson, J. O. et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68, 857–864 (2010).
Al-Chalabi, A. et al. An estimate of amyotrophic lateral sclerosis heritability using twin data. J. Neurol. Neurosurg. Psychiatry 81, 1324–1326 (2010).
Al-Chalabi, A. et al. Analysis of amyotrophic lateral sclerosis as a multistep process: a population-based modelling study. Lancet Neurol. 13, 1108–1113 (2014).
Conradi, S., Ronnevi, L. O., Nise, G. & Vesterberg, O. Abnormal distribution of lead in amyotrophic lateral sclerosis—reestimation of lead in the cerebrospinal fluid. J. Neurol. Sci. 48, 413–418 (1980).
Conradi, S., Ronnevi, L. O. & Vesterberg, O. Lead concentration in skeletal muscle in amyotrophic lateral sclerosis patients and control subjects. J. Neurol. Neurosurg. Psychiatry 41, 1001–1004 (1978).
Conradi, S., Ronnevi, L. O. & Vesterberg, O. Increased plasma levels of lead in patients with amyotrophic lateral sclerosis compared with control subjects as determined by flameless atomic absorption spectrophotometry. J. Neurol. Neurosurg. Psychiatry 41, 389–393 (1978).
Fang, F. et al. Association between blood lead and the risk of amyotrophic lateral sclerosis. Am. J. Epidemiol. 171, 1126–1133 (2010).
Petkau, A., Sawatzky, A., Hillier, C. R. & Hoogstraten, J. Lead content of neuromuscular tissue in amyotrophic lateral sclerosis: case report and other considerations. Br. J. Ind. Med. 31, 275–287 (1974).
Wang, M. D., Gomes, J., Cashman, N. R., Little, J. & Krewski, D. A meta-analysis of observational studies of the association between chronic occupational exposure to lead and amyotrophic lateral sclerosis. J. Occup. Environ. Med. 56, 1235–1242 (2014).
Callaghan, B., Feldman, D., Gruis, K. & Feldman, E. The association of exposure to lead, mercury, and selenium and the development of amyotrophic lateral sclerosis and the epigenetic implications. Neurodegener. Dis. 8, 1–8 (2011).
Perl, D. P., Gajdusek, D. C., Garruto, R. M., Yanagihara, R. T. & Gibbs, C. J. Intraneuronal aluminum accumulation in amyotrophic lateral sclerosis and Parkinsonism-dementia of Guam. Science 217, 1053–1055 (1982).
Kihira, T., Yoshida, S., Yase, Y., Ono, S. & Kondo, T. Chronic low-Ca/Mg high-Al diet induces neuronal loss. Neuropathology 22, 171–179 (2002).
Giagheddu, M. et al. Epidemiologic study of amyotrophic lateral sclerosis in Sardinia, Italy. Acta Neurol. Scand. 68, 394–404 (1983).
Chio, A., Meineri, P., Tribolo, A. & Schiffer, D. Risk factors in motor neuron disease: a case-control study. Neuroepidemiology 10, 174–184 (1991).
Granieri, E. et al. Motor neuron disease in the province of Ferrara, Italy, in 1964–1982 Neurology 38, 1604–1608 (1988).
Yu, Y. et al. Environmental risk factors and amyotrophic lateral sclerosis (ALS): a case-control study of ALS in Michigan. PLoS ONE 9, e101186 (2014).
Desplats, P. et al. Combined exposure to Maneb and Paraquat alters transcriptional regulation of neurogenesis-related genes in mice models of Parkinson's disease. Mol. Neurodegener. 7, 49 (2012).
Kong, M. et al. 5′-Aza-dC sensitizes paraquat toxic effects on PC12 cell. Neurosci. Lett. 524, 35–39 (2012).
Nelson, L. M., McGuire, V., Longstreth, W. T. Jr & Matkin, C. Population-based case–control study of amyotrophic lateral sclerosis in western Washington State. I. Cigarette smoking and alcohol consumption. Am. J. Epidemiol. 151, 156–163 (2000).
Wang, H. et al. Smoking and risk of amyotrophic lateral sclerosis: a pooled analysis of 5 prospective cohorts. Arch. Neurol. 68, 207–213 (2011).
de Jong, S. W. et al. Smoking, alcohol consumption, and the risk of amyotrophic lateral sclerosis: a population-based study. Am. J. Epidemiol. 176, 233–239 (2012).
Alonso, A., Logroscino, G. & Hernan, M. A. Smoking and the risk of amyotrophic lateral sclerosis: a systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatry 81, 1249–1252 (2010).
Alonso, A., Logroscino, G., Jick, S. S. & Hernan, M. A. Association of smoking with amyotrophic lateral sclerosis risk and survival in men and women: a prospective study. BMC Neurol. 10, 6 (2010).
Horner, R. D. et al. Occurrence of amyotrophic lateral sclerosis among Gulf War veterans. Neurology 61, 742–749 (2003).
Qureshi, I. A. & Mehler, M. F. Epigenetic mechanisms governing the process of neurodegeneration. Mol. Aspects Med. 34, 875–882 (2013).
Staszewski, O. & Prinz, M. Glial epigenetics in neuroinflammation and neurodegeneration. Cell Tissue Res. 356, 609–616 (2014).
Chestnut, B. A. et al. Epigenetic regulation of motor neuron cell death through DNA methylation. J. Neurosci. 31, 16619–16636 (2011).
Choy, M. K. et al. Genome-wide conserved consensus transcription factor binding motifs are hyper-methylated. BMC Genomics 11, 519 (2010).
Urdinguio, R. G., Sanchez-Mut, J. V. & Esteller, M. Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol. 8, 1056–1072 (2009).
Chen, P. Y., Feng, S., Joo, J. W., Jacobsen, S. E. & Pellegrini, M. A comparative analysis of DNA methylation across human embryonic stem cell lines. Genome Bio. 12, R62 (2011).
Gavin, D. P., Chase, K. A. & Sharma, R. P. Active DNA demethylation in post-mitotic neurons: a reason for optimism. Neuropharmacology 75, 233–245 (2013).
Laurent, L. et al. Dynamic changes in the human methylome during differentiation. Genome Res. 20, 320–331 (2010).
Feng, J., Fouse, S. & Fan, G. Epigenetic regulation of neural gene expression and neuronal function. Pediatric Res. 61, 58R–63R (2007).
Tremolizzo, L. et al. Whole-blood global DNA methylation is increased in amyotrophic lateral sclerosis independently of age of onset. Amyotroph. Lateral Scler. Frontotemporal Degener. 15, 98–105 (2013).
Morahan, J. M., Yu, B., Trent, R. J. & Pamphlett, R. A genome-wide analysis of brain DNA methylation identifies new candidate genes for sporadic amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 10, 418–429 (2009).
Tibshirani, M. et al. Cytoplasmic sequestration of FUS/TLS associated with ALS alters histone marks through loss of nuclear protein arginine methyltransferase 1. Hum. Mol. Genet. 24, 773–786 (2014).
Xi, Z. et al. Hypermethylation of the CpG-island near the C9orf72 G4C2-repeat expansion in FTLD patients. Hum. Mol. Genet. 23, 5630–5637 (2014).
Belzil, V. V. et al. Characterization of DNA hypermethylation in the cerebellum of c9FTD/ALS patients. Brain Res. 1584, 15–21 (2014).
Liu, E. Y. et al. C9orf72 hypermethylation protects against repeat expansion-associated pathology in ALS/FTD. Acta Neuropathol. 128, 525–541 (2014).
Dion, V., Lin, Y., Hubert, L. Jr, Waterland, R. A. & Wilson, J. H. Dnmt1 deficiency promotes CAG repeat expansion in the mouse germline. Hum. Mol. Genet. 17, 1306–1317 (2008).
Jowaed, A., Schmitt, I., Kaut, O. & Wullner, U. Methylation regulates alpha-synuclein expression and is decreased in Parkinson's disease patients' brains. J. Neurosci. 30, 6355–6359 (2010).
Fuso, A., Nicolia, V., Cavallaro, R. A. & Scarpa, S. DNA methylase and demethylase activities are modulated by one-carbon metabolism in Alzheimer's disease models. J. Nutr. Biochem. 22, 242–251 (2011).
Lagali, P. S. & Picketts, D. J. Matters of life and death: the role of chromatin remodeling proteins in retinal neuron survival. J. Ocular Bio. 4, 111–120 (2011).
Lazo-Gomez, R., Ramirez-Jarquin, U. N., Tovar, Y. R. & Tapia, R. Histone deacetylases and their role in motor neuron degeneration. Front. Cell. Neurosci. 7, 243 (2013).
Martin, C. & Zhang, Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Bio. 6, 838–849 (2005).
Bardai, F. H. & D'Mello, S. R. Selective toxicity by HDAC3 in neurons: regulation by Akt and GSK3beta. J. Neurosci. 31, 1746–1751 (2011).
Janssen, C. et al. Differential histone deacetylase mRNA expression patterns in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 69, 573–581 (2010).
Valle, C. et al. Tissue-specific deregulation of selected HDACs characterizes ALS progression in mouse models: pharmacological characterization of SIRT1 and SIRT2 pathways. Cell Death Dis. 5, e1296 (2014).
Teyssou, E. et al. Genetic analysis of SS18L1 in French amyotrophic lateral sclerosis. Neurobiol. Aging 35, 1213.e19–1213.e12 (2014).
Simpson, C. L. et al. Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum. Mol. Genet. 18, 472–481 (2009).
Kwak, S., Hideyama, T., Yamashita, T. & Aizawa, H. AMPA receptor-mediated neuronal death in sporadic ALS. Neuropathology 30, 182–188 (2010).
Hideyama, T. et al. Profound downregulation of the RNA editing enzyme ADAR2 in ALS spinal motor neurons. Neurobiol. Dis. 45, 1121–1128 (2012).
Kawahara, Y. et al. Glutamate receptors: RNA editing and death of motor neurons. Nature 427, 801 (2004).
Yamashita, T. & Kwak, S. The molecular link between inefficient GluA2 Q/R site-RNA editing and TDP-43 pathology in motor neurons of sporadic amyotrophic lateral sclerosis patients. Brain Res. 1584, 28–38 (2014).
Yamashita, T. et al. Rescue of amyotrophic lateral sclerosis phenotype in a mouse model by intravenous AAV9-ADAR2 delivery to motor neurons. EMBO Mol. Med. 5, 1710–1719 (2013).
Lagos-Quintana, M., Rauhut, R., Lendeckel, W. & Tuschl, T. Identification of novel genes coding for small expressed RNAs. Science 294, 853–858 (2001).
Lee, R. C. & Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862–864 (2001).
Selbach, M. et al. Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63 (2008).
Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).
Lau, N. C., Lim, L. P., Weinstein, E. G. & Bartel, D. P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858–862 (2001).
University of Manchester. miRBase [online] , (2014).
Ponomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M. & Weiner, H. L. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway. Nat. Med. 17, 64–70 (2011).
Engels, B. M. & Hutvagner, G. Principles and effects of microRNA-mediated post-transcriptional gene regulation. Oncogene 25, 6163–6169 (2006).
Lau, P. & de Strooper, B. Dysregulated microRNAs in neurodegenerative disorders. Semin. Cell Dev. Bio. 21, 768–773 (2010).
Mondanizadeh, M. et al. MicroRNA-124 regulates neuronal differentiation of mesenchymal stem cells by targeting Sp1 mRNA. J. Cell. Biochem. (2015).
Lagos-Quintana, M. et al. Identification of tissue-specific microRNAs from mouse. Curr. Bio. 12, 735–739 (2002).
Coolen, M., Katz, S. & Bally-Cuif, L. miR-9: a versatile regulator of neurogenesis. Front. Cell. Neurosci. 7, 220 (2013).
Winter, J., Jung, S., Keller, S., Gregory, R. I. & Diederichs, S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Bio. 11, 228–234 (2009).
Lee, Y., Jeon, K., Lee, J. T., Kim, S. & Kim, V. N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663–4670 (2002).
Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419 (2003).
Yi, R., Qin, Y., Macara, I. G. & Cullen, B. R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Devel. 17, 3011–3016 (2003).
Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834–838 (2001).
Pillai, R. S., Artus, C. G. & Filipowicz, W. Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 10, 1518–1525 (2004).
Zhang, R. et al. Evidence for systemic immune system alterations in sporadic amyotrophic lateral sclerosis (sALS). J. Neuroimmunol. 159, 215–224 (2005).
Koval, E. D. et al. Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum. Mol. Genet. 22, 4127–4135 (2013).
Miyoshi, K., Miyoshi, T. & Siomi, H. Many ways to generate microRNA-like small RNAs: non-canonical pathways for microRNA production. Mol. Genet. Genomics 284, 95–103 (2010).
Okamura, K., Hagen, J. W., Duan, H., Tyler, D. M. & Lai, E. C. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila Cell 130, 89–100 (2007).
Ruby, J. G., Jan, C. H. & Bartel, D. P. Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83–86 (2007).
Diederichs, S. & Haber, D. A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 131, 1097–1108 (2007).
Hansen, T. B. et al. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 30, 4414–4422 (2011).
Haramati, S. et al. miRNA malfunction causes spinal motor neuron disease. Proc. Natl Acad. Sci. USA 107, 13111–13116 (2010).
Tan, L. & Yu, J. T. Causes and consequences of microRNA dysregulation in neurodegenerative diseases. Mol. Neurobio. http://dx.doi.org/10.1007/s12035-014-8803-9 .
Kawahara, Y. & Mieda-Sato, A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl Acad. Sci. USA 109, 3347–3352 (2012).
Ruegger, S. & Grosshans, H. MicroRNA turnover: when, how, and why. Trends Biochem. Sci. 37, 436–446 (2012).
Freischmidt, A., Muller, K., Ludolph, A. C. & Weishaupt, J. H. Systemic dysregulation of TDP-43 binding microRNAs in amyotrophic lateral sclerosis. Acta Neuropathol. Commun. 1, 42 (2013).
De Felice, B. et al. miR-338-3p is over-expressed in blood, CFS, serum and spinal cord from sporadic amyotrophic lateral sclerosis patients. Neurogenetics 15, 243–253 (2014).
Morel, L. et al. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J. Biol. Chem. 288, 7105–7116 (2013).
Russell, A. P. et al. Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol. Dis. 49, 107–117 (2013).
Williams, A. H. et al. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326, 1549–1554 (2009).
Campos-Melo, D., Droppelmann, C. A., He, Z., Volkening, K. & Strong, M. J. Altered microRNA expression profile in amyotrophic lateral sclerosis: a role in the regulation of NFL mRNA levels. Mol. Brain 6, 26 (2013).
Butovsky, O. et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J. Clin. Invest. 122, 3063–3087 (2012).
Parisi, C. et al. Dysregulated microRNAs in amyotrophic lateral sclerosis microglia modulate genes linked to neuroinflammation. Cell Death Dis. 4, e959 (2013).
Jobe, E. M., McQuate, A. L. & Zhao, X. Crosstalk among epigenetic pathways regulates neurogenesis. Front. Neurosci. 6, 59 (2012).
Goodall, E. F., Heath, P. R., Bandmann, O., Kirby, J. & Shaw, P. J. Neuronal dark matter: the emerging role of microRNAs in neurodegeneration. Front. Cell. Neurosci. 7, 178 (2013).
Rossi, J. J. A novel nuclear miRNA mediated modulation of a non-coding antisense RNA and its cognate sense coding mRNA. EMBO J. 30, 4340–4341 (2011).
Bruneteau, G. et al. Muscle histone deacetylase 4 upregulation in amyotrophic lateral sclerosis: potential role in reinnervation ability and disease progression. Brain 136, 2359–2368 (2013).
Dini Modigliani, S., Morlando, M., Errichelli, L., Sabatelli, M. & Bozzoni, I. An ALS-associated mutation in the FUS 3′-UTR disrupts a microRNA-FUS regulatory circuitry. Nat. Commun. 5, 4335 (2014).
Kabashi, E. et al. FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS Genet. 7, e1002214 (2011).
Gascon, E. & Gao, F. B. The emerging roles of microRNAs in the pathogenesis of frontotemporal dementia-amyotrophic lateral sclerosis (FTD-ALS) spectrum disorders. J. Neurogenet. 28, 30–40 (2014).
Jiao, J., Herl, L. D., Farese, R. V. & Gao, F. B. MicroRNA-29b regulates the expression level of human progranulin, a secreted glycoprotein implicated in frontotemporal dementia. PLoS ONE 5, e10551 (2010).
Buratti, E. et al. Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 277, 2268–2281 (2010).
King, I. N. et al. The RNA-binding protein TDP-43 selectively disrupts microRNA-1/206 incorporation into the RNA-induced silencing complex. J. Biol. Chem. 289, 14263–14271 (2014).
Bensimon, G., Lacomblez, L. & Meininger, V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N. Engl. J. Med. 330, 585–591 (1994).
Miller, T. M. et al. An antisense oligonucleotide against SOD1 delivered intrathecally for patients with SOD1 familial amyotrophic lateral sclerosis: a phase 1, randomised, first-in-man study. Lancet Neurol. 12, 435–442 (2013).
Lagier-Tourenne, C. et al. Targeted degradation of sense and antisense C9orf72 RNA foci as therapy for ALS and frontotemporal degeneration. Proc. Natl Acad. Sci. USA 110, E4530–E4539 (2013).
Bader, A. G., Brown, D. & Winkler, M. The promise of microRNA replacement therapy. Cancer Res. 70, 7027–7030 (2010).
Lanford, R. E. et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198–201 (2010).
Corbett, G. T., Roy, A. & Pahan, K. Sodium phenylbutyrate enhances astrocytic neurotrophin synthesis via protein kinase C (PKC)-mediated activation of cAMP-response element-binding protein (CREB): implications for Alzheimer disease therapy. J. Biol. Chem. 288, 8299–8312 (2013).
Del Signore, S. J. et al. Combined riluzole and sodium phenylbutyrate therapy in transgenic amyotrophic lateral sclerosis mice. Amyotroph. Lateral Scler. 10, 85–94 (2009).
Cudkowicz, M. E. et al. Phase 2 study of sodium phenylbutyrate in ALS. Amyotroph. Lateral Scler. 10, 99–106 (2009).
Ho, A. S., Turcan, S. & Chan, T. A. Epigenetic therapy: use of agents targeting deacetylation and methylation in cancer management. Onco Targets Ther. 6, 223–232 (2013).
Veerappan, C. S., Sleiman, S. & Coppola, G. Epigenetics of Alzheimer's disease and frontotemporal dementia. Neurotherapeutics 10, 709–721 (2013).
Zhang, Z. et al. Downregulation of microRNA-9 in iPSC-derived neurons of FTD/ALS patients with TDP-43 mutations. PloS ONE 8, e76055 (2013).
Kye, M. J. & Goncalves Ido, C. The role of miRNA in motor neuron disease. Front. Cell. Neurosci. 8, 15 (2014).
Waddington, C. H. Preliminary notes on the development of the wings in normal and mutant strains of Drosophila. Proc. Natl Acad. Sci. USA 25, 299–307 (1939).
Riggs A. D., Martienssen, R. A. & Russo, V. E. In Epigenetic mechanisms of gene regulation (Eds Russo, V. E. et al.) 1–4 (Cold Spring Harbor Laboratory Press, 1996).
Berger, S. L., Kouzarides, T., Shiekhattar, R. & Shilatifard, A. An operational definition of epigenetics. Genes Dev. 23, 781–783 (2009).