Epigenetic regulation of motor neuron cell death through DNA methylation

Journal of Neuroscience

Volumn 31, Issue 46, 2011, Pages 16619-16636

  Chestnut, Barry A ^a   Chang, Qing ^a   Price, Ann ^a   Lesuisse, Catherine ^a   Wong, Margaret ^a   Martin, Lee J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; CASPASE 3; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CATALYSIS; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IMMUNOREACTIVITY; IN VIVO STUDY; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SYNAPSE; UPREGULATION;

AGE FACTORS; AMYLOID PRECURSOR PROTEIN SECRETASES; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; ASPARTIC ACID ENDOPEPTIDASES; CAMPTOTHECIN; CASPASE 3; CELL LINE, TRANSFORMED; CENTRAL NERVOUS SYSTEM; CYTOSINE; DISEASE MODELS, ANIMAL; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENZYME INHIBITORS; EPIGENOMICS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HUMANS; INDOLES; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUTATION; PROPIONIC ACIDS; RNA, SMALL INTERFERING; SCIATIC NEUROPATHY; SUPEROXIDE DISMUTASE; TRANSFECTION; UP-REGULATION;

EID: 81255143014     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1639-11.2011     Document Type: Article

References (73)

1. Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9:2395-2402.
2. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6-21.
3. Brenner C, Fuks F (2006) DNA methyltransferases: facts, clues, mysteries. Curr Top Microbiol Immunol 301:45-66.
4. Brooks P, Marietta C, Goldman D (1996) DNA mismatch repair and DNA methylation in adult brain neurons. J Neurosci 16:939-945.
5. Brueckner B, Garcia Boy R, Siedlecki P, Musch T, Kliem HC, Zielenkiewicz P, Suhai S, Wiessler M, Lyko F (2005) Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res 65:6305-6311.
6. Calhoun ME, Jucker M, Martin LJ, Thinakaran G, Price DL, Mouton PR (1996) Comparative evaluation of synaptophysin-based methods for quantification of synapses. J Neurocytol 25:821-828.
7. Cashman NR, Durham HD, Blusztajn JK, Oda K, Tabira T, Shaw IT, Dahrouge S, Antel JP (1992) Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn 194:209-221.
8. Chang Q, Martin LJ (2009) Glycinergic innervation of motoneurons is deficient in amyotrophic lateral sclerosis mice: a confocal quantitative analysis. Am J Pathol 174:574-585.
9. Chang Q, Martin LJ (2011) Glycine receptor channels in spinal motoneurons are abnormal in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 31:2815-2827.
10. Cheng X (1995) Structure and function of DNA methyltransferases. Annu Rev Biophys Biomol Struct 24:293-318.
11. Curradi M, Izzo A, Badaracco G, Landsberger N (2002) Molecular mechanisms of gene silencing mediated by DNA methylation. Mol Cell Biol 22:3157-3173.
12. Dittmer A, Dittmer J (2006) β-Actin is not a reliable loading control in Western blot analysis. Electrophoresis 27:2844-2845.
13. Endres M, Meisel A, Biniskiewicz D, Namura S, Prass K, Ruscher K, Lipski A, Jaenisch R, Moskowitz MA, Dirnagl U (2000) DNA methytransferase contributes to delayed ischemia brain injury. J Neurosci 20:3175-3181.
14. Endres M, Fan G, Meisel A, Dirnagl U, Jaenisch R (2001) Effects of cerebral ischemia in mice lacking DNA methyltransferase I in post-mitotic neurons. NeuroReport 12:3763-3766.
15. Fatemi M, Pao MM, Jeong S, Gal-Yam EN, Egger G, Weisenberger DJ, Jones PA (2005) Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic Acids Res 33:e176.
16. Feng J, Chang H, Li E, Fan G (2005) Dynamic expression of de novo DNA methytransferase DNMT3A and DNMT3B in the central nervous system. J Neurosci Res 79:734-746.
17. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, Silva AJ, Fan G (2010) Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13:423-430.
18. Ferguson RE, Carroll HP, Harris A, Maher ER, Selby PJ, Banks RE (2005) Housekeeping proteins: a preliminary study illustrating some limitations as useful references in protein expression studies. Proteomics 5:566-571.
19. Gardiner-Garden M, Frommer M (1987) CpG islands in vertebrate genomes. J Mol Biol 196:261-282.
20. Goto K, Numata M, Komura JI, Ono T, Bestor TH, Kondo H (1994) Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation 56:39-44.
21. Hauke J, Riessland M, Lunke S, Eyüpoglu IY, Blümcke I, El-Osta A, Wirth B, Hahnen E (2009) Survival motor neuron gene 2 silencing by DNA methylation correlates with spinal muscular atrophy disease severity and can be bypassed by histone deacetylase inhibition. Hum Mol Genet 18:304-317.
22. Inano K, Suetake I, Ueda T, Miyake Y, Nakamura M, Okada M, Tajima S (2000) Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J Biochem 128:315-321.
23. Iskandar BJ, Rizk E, Meier B, Hariharan N, Bottiglieri T, Finnell RH, Jarrard DF, Banerjee RV, Skene JH, Nelson A, Patel N, Gherasim C, Simon K, Cook TD, Hogan KJ (2010) Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 120:1603-1616.
24. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449:248-251.
25. Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068-1070.
26. Kang JS, Wanibuchi H, Morimura K, Totsuka Y, Yoshimura I, Fukushima S (2006) Existence of a no effect level for MeIQx hepatocarcinogenicity on a background of thioacetaminde-induced liver damage in rats. Cancer Sci 97:453-458.
27. Kimura H, Shiota K (2003) Methyl-CpG-binding protein, MeCP2, is a target molecule for maintenance DNA methyltransferase, Dnmt1. J Biol Chem 278:4806-4812.
28. Kondo T, Bobek MP, Kuick R, Lamb B, Zhu X, Narayan A, Bourc'his D, Viegas-Péquignot E, Ehrlich M, Hanash SM (2000) Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum Mol Genet 9:597-604.
29. LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iñiguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolan ̃os CA, Kabbaj M, et al. (2001) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137-1143.
30. Lee BH, Yegnasubramanian S, Lin X, Nelson WG (2005) Procainamide is a specific inhibitor of DNA methyltransferase 1. J Biol Chem 280: 40749-40756.
31. Lefebvre S, Bürglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, Le Paslier D, Frezal J, Cohen D, Weissenbach J, Munnich A, Melki J (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80:155-165.
32. Lesuisse C, Martin LJ (2002) Immature and mature cortical neurons engage different apoptotic mechanisms involving caspase-3 and the mitogenactivated protein kinase pathway. J Cereb Blood Flow Metab 22:935-950.
33. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, Malone LM, Sweatt JD (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281: 5763-15773.
34. Liu N-K, Xu X-M (2006) β-Tubulin is a more suitable internal control that _-actin in western blot analysis of spinal cord tissues after traumatic injury. J Neurotrauma 23:1794-1801.
35. Lok J, Martin LJ (2002) Rapid subcellular redistribution of Bax precedes caspase-3 and endonuclease activation during excitotoxic neuronal apoptosis in rat brain. J Neurotrauma 19:815-828.
36. Martin LJ (1999) Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol 58:459-471.
37. Martin LJ (2000) p53 is abnormally elevated and active in the CNS of patients with amyotrophic lateral sclerosis. Neurobiol Dis 7:613-622.
38. Martin LJ (2010) Mitochondrial and cell death mechanisms in neurodegenerative diseases. Pharmaceuticals 3:839-915.
39. Martin LJ (2011) An approach to experimental synaptic pathology using green fluorescent protein-transgenic mice and gene knockout mice: excitotoxic vulnerability of interneurons and motoneurons is associated with mitochondrial accumulation and mediated by the mitochondrial permeability transition pore. Toxicol Pathol 39:220-233.
40. Martin LJ, Liu Z (2002) Injury-induced spinal motor neuron apoptosis is preceded by DNA single-strand breaks and is p53-and bax-dependent. J Neurobiol 50:181-197.
41. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C (1998) Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46:281-309.
42. Martin LJ, Kaiser A, Price AC (1999) Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J Neurobiol 40:185-201.
43. Martin LJ, Sieber FE, Traystman RJ (2000) Apoptosis and necrosis occur in separate neuronal populations in hippocampus and cerebellum after ischemia and are associated with alterations in metabotropic glutamate receptor signaling pathways. J Cereb Blood Flow Metab 20:153-167.
44. Martin LJ, Price AC, McClendon KB, Al-Abdulla NA, Subramaniam JR, Wong PC, Liu Z (2003) Early events of target deprivation/axotomyinduced neuronal apoptosis in vivo: oxidative stress, DNA damage, p53 phosphorylation and subcellular redistribution of death proteins. J Neurochem 85:234-247.
45. Martin LJ, Chen K, Liu Z (2005) Adult motor neuron apoptosis is mediated by nitric oxide and Fas death receptor linked by DNA damage and p53 activation. J Neurosci 25:6449-6459.
46. Martin LJ, Liu Z, Chen K, Price AC, Pan Y, Swaby JA, Golden WC (2007) Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death. J Comp Neurol 500:20-46.
47. Martin LJ, Liu Z, Pipino J, Chestnut B, Landek MA (2009a) Molecular regulation of DNA damage-induced apoptosis in neurons of cerebral cortex. Cereb Cortex 19:1273-1293.
48. Martin LJ, Gertz B, Pan Y, Price AC, Molkentin JD, Chang Q (2009b) The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Exp Neurol 218:333-346.
49. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE (2003) DNA methylation-related chromatin remodeling in activity-dependent Bdnf gene regulation. Science 302:890-893.
50. Miller CA, Sweatt JD (2007) Covalent modification ofDNAregulates memory formation. Neuron 53:857-869.
51. Morahan JM, Yu B, Trent RJ, Pamphlett R (2007) Are metallothionein genes silenced in ALS? Toxicol Lett 168:83-87.
52. Morahan JM, Yu B, Trent RJ, Pamphlett R (2009) A genome-wide analysis of brain DNA methylation identifies new candidate genes for sporadic amyotrophic lateral sclerosis 10:418-429.
53. Nelson ED, Kavalali ET, Monteggia LM (2008) Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J Neurosci 28:395-406.
54. Northington FJ, Chavez-Valdez R, Martin LJ (2011) Neuronal cell death in neonatal hypoxia ischemia. Ann Neurol 69:743-758.
55. Oates N, Pamphlett R (2007) An epigenetic analysis of SOD1 and VEGF in ALS. Amyotroph Lateral Scler 8:83-86.
56. Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247-257.
57. Pollack Y, Kasir J, Shemer R, Metzger S, Szyf M (1984) Methylation pattern of mouse mitochondrial DNA. Nucleic Acids Res 12:4811-4824.
58. Pradhan S, Bacolla A, Wells RD, Roberts RJ (1999) Recombinant human DNA (cytosine-5) methyltransferase. I. expression, purification, and comparison of de novo and maintenance methylation. J Biol Chem 274:33002-33010.
59. Puyal J, Vaslin A, Mottier V, Clarke PGH (2009) Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 66:378-389.
60. Razin A (1998) CpG methylation, chromatin structure and gene silencing- a three-way connection. EMBO J 17:4905-4908.
61. Robertson KD (2001) DNA methylation, methyltransferases, and cancer. Oncogene, 20:3139-3155.
62. Schaefer M, Lyko F (2010) Solving the Dnmt2 enigma. Chromosoma 119:35-40.
63. Shaikh AY, Martin LJ (2002) DNA base-excision repair enzyme apurinic/ apyrimidinic endonuclease/redox factor-1 is increased and competent in brain and spinal cord of individuals with amyotrophic lateral sclerosis. Neuromol Med 2:47-60.
64. Shmookler Reis RJ, Goldstein S (1983) Mitochondrial DNA in mortal and immortal cells: genome number, integrity, and methylation. J Biol Chem 258:9078-9085.
65. Shock LS, Thakkar PV, Peterson EJ, Moran RG, Taylor SM (2011) DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci U S A 108:3630-3635.
66. Sleiman SF, Basso M, Mahishi L, Kozikowski AP, Donohoe ME, Langley B, Ratan RR (2009) Putting the "HAT" back on survival signaling: the promises and challenges of HDAC inhibition in the treatment of neurological conditions. Expert Opin Investig Drugs 18:573-584.
67. Szyf M (2005) DNA methylation and demethylation as targets for anticancer therapy. Biochemistry 70:533-549.
68. Tovar-y-Romo LB, Santa-Cruz LD, Tapia R (2009) Experimental models for the study of neurodegeneration in amyotrophic lateral sclerosis. Mol Neurodegeneration 4:31.
69. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397.
70. Wong M, Martin LJ (2010) Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum Mol Genet 19:2284-2302.
71. Xie S, Wang Z, Okano M, Nogami M, Li Y, He WW, Okumura K, Li E (1999) Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene 236:87-95.
72. Yang Y, Gozen O, Vidensky S, Robinson MB, Rothstein JD (2010) Epigenetic regulation of neuron-dependent induction of astroglial synaptic protein GLT1. Glia 58:277-286.
73. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189-1201.