Mouse ES cells overexpressing DNMT1 produce abnormal neurons with upregulated NMDA/NR1 subunit

Differentiation

Volumn 82, Issue 1, 2011, Pages 9-17

  D'Aiuto, Leonardo ^a   Di Maio, Roberto ^b,c   Mohan, K Naga ^a   Minervini, Crescenzio ^d   Saporiti, Federica ^b   Soreca, Isabella ^b   Greenamyre, J Timothy ^b   Chaillet, J Richard ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c RiMED Foundation Palermo   (Italy)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

DNA methylation; Dnmt1; Epigenetic; Neuronal differentiation; NMDA receptor

Indexed keywords

DNA METHYLTRANSFERASE 1; GLUTAMATE DECARBOXYLASE 67; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; REELIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITE; DNA METHYLATION; DNMT1 GENE; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; GENE REPRESSION; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR UPREGULATION; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; EMBRYONIC STEM CELLS; IMMUNOBLOTTING; MICE; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 79958769687     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.03.003     Document Type: Article

References (40)

1. Biniszkiewicz D., Gribnau J., Ramsahoye B., Gaudet F., Eggan K., Humpherys D., Mastrangelo M.A., Jun Z., Walter J., Jaenisch R. Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell Biol. 2002, 22:2124-2135.
2. Borowczyk E., Mohan K.N., D'Aiuto L., Cirio M.C., Chaillet J.R. Identification of a region of the DNMT1 methyltransferase that regulates the maintenance of genomic imprints. Proc. Natl. Acad. Sci. USA 2009, 106:20806-20811.
3. Chahrour M., Zoghbi H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 2007, 56:422-437.
4. Chen Y., Sharma P.P., Costa R.H., Costa E., Grayson D.R. On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res. 2002, 30:2930-2939.
5. Cirio M.C., Martel J., Mann M., Toppings M., Bartolomei M., Trasler J., Chaillet J.R. DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation. Dev. Biol. 2008, 324:139-150.
6. Costa E., Dong E., Grayson D.R., Guidotti A., Ruzicka W., Veldic M. Reviewing the role of DNA (cytosine-5) methyltransferase overexpression in the cortical GABAergic dysfunction associated with psychosis vulnerability. Epigenetics 2007, 2:29-36.
7. D'Aiuto L., Robison C.S., Gigante M., Nwanegbo E., Shaffer B., Sukhwani M., Castro C.A., Chaillet J.R. Human IL-12 p40 as a reporter gene for high-throughput screening of engineered mouse embryonic stem cells. BMC Biotechnol. 2008, 8:52.
8. Daskalakis Z.J., Christensen B.K., Chen R., Fitzgerald P.B., Zipursky R.B., Kapur S. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch. Gen. Psychiatry 2002, 59:347-354.
9. Deng J., Szyf M. Downregulation of DNA (cytosine-5-)methyltransferase is a late event in NGF-induced PC12 cell differentiation. Brain Res. Mol. Brain Res. 1999, 71:23-31.
10. Detich N., Ramchandani S., Szyf M. A conserved 3'- untranslated element mediates growth regulation of DNA methyltransferase 1 and inhibits its transforming activity. J. Biol. Chem. 2001, 276:24881-24890.
11. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
12. Fan G., Beard C., Chen R.Z., Csankovszki G., Sun Y., Siniaia M., Biniszkiewicz D., Bates B., Lee P.P., Kuhn R., Trumpp A., Poon C., Wilson C.B., Jaenisch R. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 2001, 21:788-797.
13. Gibbons R.J., Wada T., Fisher C.A., Malik N., Mitson M.J., Steensma D.P., Fryer A., Goudie D.R., Krantz I.D., Traeger-Synodinos J. Mutations in the chromatin-associated protein ATRX. Hum. Mutat. 2008, 29:796-802.
14. Hyde T.M., Weinberger D.R. Seizures and schizophrenia. Schizophr. Bull. 1997, 23:611-622.
15. Hutnick L.K., Golshani P., Namihira M., Xue Z., Matynia A., Yang X.W., Silva A.J., Schweizer F.E., Fan G. DNA hypomethylation restricted to the murine forebrain induces cortical degeneration and impairs postnatal neuronal maturation. Hum. Mol. Genet. 2009, 18:2875-2888.
16. Jiang Y., Bressler J., Beaudet A.L. Epigenetics and human disease. Annu. Rev. Genomics Hum. Genet. 2004, 5:479-510.
17. Kramer J.M., van Bokhoven H. Genetic and epigenetic defects in mental retardation. Int. J. Biochem. Cell Biol. 2008, 41:96-107.
18. Lafon-Cazal M., Pietri S., Culcasi M., Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature 1993, 364:535-537.
19. Lei H., Oh S.P., Okano M., Juttermann R., Goss K.A., Jaenisch R., Li E. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 1996, 122:3195-3205.
20. Leite J.P., Babb T.L., Pretorius J.K., Kulman P.A., Yeoman K.M., Mathern G.W. Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats. Epilepsy Res. 1996, 26:219-231.
21. Levenson J.M., Sweatt J.D. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6:108-118.
22. Levenson J.M., Roth T.L., Lubin F.D., Miller C.A., Huang I., Desai P., Malone L.M., Sweatt J.D. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J. Biol. Chem. 2006, 281:15763-15773.
23. Liu Y., Sun L., Jost J.P. In differentiating mouse myoblasts DNA methyltransferase is posttranscriptionally and posttranslationally regulated. Nucleic Acids Res. 1996, 24:2718-2722.
24. Lucifero D., Mertineit C., Clarke H.J., Bestor T.H., Trasler J.M. Methylation dynamics of imprinted genes in mouse germ cells. Genomics 2002, 79:530-538.
25. Massalini S., Pellegatta S., Pisati F., Finocchiaro G., Farace M.G., Ciafrè S.A. Reelin affects chain-migration and differentiation of neural precursor cells. Mol. Cell Neurosci. 2009, 42:341-349.
26. Mathern G.W., Pretorius J.K., Mendoza D., Lozada A., Kornblum H.I. Hippocampal AMPA and NMDA mRNA levels correlate with aberrant fascia dentata mossy fiber sprouting in the pilocarpine model of spontaneous limbic epilepsy. J. Neurosci. Res. 1998, 54:734-753.
27. Mattay V.S., Callicott J.H., Bertolino A., Santha A.K., Tallent K.A., Goldberg T.E., Frank J.A., Weinberger D.R. Abnormal functional lateralization of the sensorimotor cortex in patients with schizophrenia. Neuroreport 1997, 8:2977-2984.
28. Novakovic B., Wong N.C., Sibson M., Ng H.K., Morley R., Manuelpillai U., Down T., Rakyan V.K., Beck S., Hiendleder S., Roberts C.T., Craig J.M., Saffery R. DNA methylation-mediated down-regulation of DNA methyltransferase-1 (DNMT1), is co-incident with, but not essential for, global hypomethylation in human placenta. J. Biol. Chem. 2010, 285:9583-9593.
29. Pacheco Otalora L.F., Couoh J., Shigamoto R., Zarei M.M., Garrido Sanabria E.R. Abnormal mGluR2/3 expression in the perforant path termination zones and mossy fibers of chronically epileptic rats. Brain Res. 2006, 1098:170-185.
30. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebeis J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
31. Patel M., Day B.J., Crapo J.D., Fridovich I., McNamara O. Requirement for superoxide in excitotoxic cell death. Neuron 1996, 16:345-355.
32. Reinhart B., Chaillet J.R. Genomic imprinting: cis-acting sequences and regional control. Int. Rev. Cytol. 2005, 243:173-213.
33. Sen G.L., Reuter J.A., Webster D.E., Zhu L., Khavari P.A. DNMT1 maintains progenitor function in self-renewing somatic tissue. Nature 2010, 463:563-567.
34. Singh R.P., Shiue K., Schomberg D., Zhou F.C. Cellular epigenetic modifications of neural stem cell differentiation. Cell Transplant 2009, 18:1197-1211.
35. Smith A.G. Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 2001, 17:435-462.
36. Tanaka K.F., Ahmari S.E., Leonardo E.D., Richardson-Jones J.W., Budreck E.C., Scheiffele P., Sugio S., Inamura N., Ikenaka K., Hen R. Flexible accelerated STOP Tetracycline Operator-Knockin (FAST): a versatile and efficient new gene modulating system. Biol. Psychiatry 2010, 67:770-773.
37. Tucker K.L. Methylated cytosine and the brain: a new base for neuroscience. Neuron 2001, 30:649-652.
38. Tueting P., Doueiri M.S., Guidotti A., Davis J.M., Costa E. Reelin down-regulation in mice and psychosis endophenotypes. Neurosci. Biobehav. Rev. 2006, 30:1065-1077.
39. Veldic M., Guidotti A., Maloku E., Davis J.M., Costa E. In psychosis, cortical interneurons overexpress DNA-methyltransferase 1. Proc. Natl. Acad. Sci. USA 2005, 102:2152-2157.
40. Vergun O., Han Y.Y., Reynolds I.J. Glucosedeprivation produces a prolonged increase in sensitivity to glutamate in cultured rat cortical neurons. Exp. Neurol. 2003, 183:682-694.