Stage-specific induction of DNA methyltransferases in olfactory receptor neuron development

Developmental Biology

Volumn 288, Issue 2, 2005, Pages 461-473

  MacDonald, Jessica L ^a   Gin, Christopher S Y ^a   Roskams, A Jane ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Epigenetics; Lineage restriction; Methyl binding domain proteins; Neuronal differentiation

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE DEACETYLASE 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL MATURATION; CHROMATIN CONDENSATION; EMBRYO; FEMALE; GENE EXPRESSION; METHYLATION; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE ENDING; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALIA; MAMMALIA;

EID: 29144513565     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.09.048     Document Type: Article

References (69)

1. H.M. Abdolmaleky, C.L. Smith, S.V. Faraone, R. Shafa, W. Stone, S.J. Glatt, and M.T. Tsuang Methylomics in psychiatry: modulation of gene-environment interactions may be through DNA methylation Am. J. Med. Genet., Part B Neuropsychiatr. Genet. 127 2004 51 59
2. R.E. Amir, I.B. Van den Veyver, M. Wan, C.Q. Tran, U. Francke, and H.Y. Zoghbi Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2 Nat. Genet. 23 1999 185 188
3. E. Au, and A.J. Roskams Olfactory ensheathing cells of the lamina propria in vivo and in vitro Glia 41 2003 224 236
4. T.H. Bestor The DNA methyltransferases of mammals Hum. Mol. Genet. 9 2000 2395 2402
5. T. Bestor, A. Laudano, R. Mattaliano, and V. Ingram Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases J. Mol. Biol. 203 1988 971 983
6. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21
7. P.J. Brooks, C. Marietta, and D. Goldman DNA mismatch repair and DNA methylation in adult brain neurons J. Neurosci. 16 1996 939 945
8. M. Caggiano, J.S. Kauer, and D.D. Hunter Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus Neuron 13 1994 339 352
9. V.M. Carr, and A.I. Farbman Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium Exp. Neurol. 115 1992 55 59
10. L.A. Carter, J.L. MacDonald, and A.J. Roskams Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype J. Neurosci. 24 2004 5670 5683
11. T. Chen, Y. Ueda, J.E. Dodge, Z. Wang, and E. Li Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b Mol. Cell. Biol. 23 2003 5594 5605
12. X. Chen, H. Fang, and J.E. Schwob Multipotency of purified, transplanted globose basal cells in olfactory epithelium J. Comp. Neurol. 469 2004 457 474
13. A. Chess, I. Simon, H. Cedar, and R. Axel Allelic inactivation regulates olfactory receptor gene expression Cell 78 1994 823 834
14. D.R. Cohen, V. Matarazzo, A.M. Palmer, Y. Tu, O.H. Jeon, J. Pevsner, and G.V. Ronnett Expression of MeCP2 in olfactory receptor neurons is developmentally regulated and occurs before synaptogenesis Mol. Cell. Neurosci. 22 2003 417 429
15. C.M. Cowan, J. Thai, S. Krajewski, J.C. Reed, D.W. Nicholson, S.H. Kaufmann, and A.J. Roskams Caspases 3 and 9 send a pro-apoptotic signal from synapse to cell body in olfactory receptor neurons J. Neurosci. 21 2001 7099 7109
16. M. Endres, A. Meisel, D. Biniszkiewicz, S. Namura, K. Prass, K. Ruscher, A. Lipski, R. Jaenisch, M.A. Moskowitz, and U. Dirnagl DNA methyltransferase contributes to delayed ischemic brain injury J. Neurosci. 20 2000 3175 3181
17. B.J. Goldstein, and J.E. Schwob Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells J. Neurosci. 16 1996 4005 4016
18. K. Goto, M. Numata, J.I. Komura, T. Ono, T.H. Bestor, and H. Kondo Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice Differentiation 56 1994 39 44
19. G.A. Graziadei, and P.P. Graziadei Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy J. Neurocytol. 8 1979 197 213
20. J. Guy, B. Hendrich, M. Holmes, J.E. Martin, and A. Bird A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome Nat. Genet. 27 2001 322 326
21. M. Halpern, and A. Martinez-Marcos Structure and function of the vomeronasal system: an update Prog. Neurobiol. 70 2003 245 318
22. R.S. Hansen, C. Wijmenga, P. Luo, A.M. Stanek, T.K. Canfield, C.M. Weemaes, and S.M. Gartler The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome Proc. Natl. Acad. Sci. U. S. A. 96 1999 14412 14417
23. A. Hermann, S. Schmitt, and A. Jeltsch The human Dnmt2 has residual DNA-(cytosine-C5) methyltransferase activity J. Biol. Chem. 278 2003 31717 31721
24. E.H. Holbrook, K.E. Szumowski, and J.E. Schwob An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium J. Comp. Neurol. 363 1995 129 146
25. J. Hsieh, K. Nakashima, T. Kuwabara, E. Mejia, and F.H. Gage Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells Proc. Natl. Acad. Sci. U. S. A. 101 2004 16659 16664
26. J.M. Huard, S.L. Youngentob, B.J. Goldstein, M.B. Luskin, and J.E. Schwob Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells J. Comp. Neurol. 400 1998 469 486
27. N. Illing, S. Boolay, J. Siwoski, D. Casper, M. Lucero, and R. AJ Conditionally immortalized lines from the olfactory placode differentiate into olfactory neurons Mol. Cell. Neurosci. 20 2002 225 243
28. K. Inano, I. Suetake, T. Ueda, Y. Miyake, M. Nakamura, M. Okada, and S. Tajima Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment J. Biochem. (Tokyo) 128 2000 315 321
29. A.R. Isles, M.J. Baum, D. Ma, E.B. Keverne, and N.D. Allen Urinary odour preferences in mice Nature 409 2001 783 784
30. C.L. Iwema, H. Fang, D.B. Kurtz, S.L. Youngentob, and J.E. Schwob Odorant receptor expression patterns are restored in lesion-recovered rat olfactory epithelium J. Neurosci. 24 2004 356 369
31. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Nat. Genet. 33 2003 245 254
32. Y.H. Jiang, T. Sahoo, R.C. Michaelis, D. Bercovich, J. Bressler, C.D. Kashork, Q. Liu, L.G. Shaffer, R.J. Schroer, and D.W. Stockton A mixed epigenetic/genetic model for oligogenic inheritance of autism with a limited role for UBE3A Am. J. Med. Genet. 131A 2004 1 10
33. P.A. Jones, and S.B. Baylin The fundamental role of epigenetic events in cancer Nat. Rev., Genet. 3 2002 415 428
34. B.P. Jung, G. Zhang, W. Ho, J. Francis, and J.H. Eubanks Transient forebrain ischemia alters the mRNA expression of methyl DNA-binding factors in the adult rat hippocampus Neuroscience 115 2002 515 524
35. B.P. Jung, G. Zhang, R. Nitsch, J. Trogadis, S. Nag, and J.H. Eubanks Differential expression of methyl CpG-binding domain containing factor MBD3 in the developing and adult rat brain J. Neurobiol. 55 2003 220 232
36. N. Kishi, and J.D. Macklis MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions Mol. Cell. Neurosci. 27 2004 306 321
37. E. Korzus, M.G. Rosenfeld, and M. Mayford CBP histone acetyltransferase activity is a critical component of memory consolidation Neuron 42 2004 961 972
38. P. Kurki, M. Vanderlaan, F. Dolbeare, J. Gray, and E.M. Tan Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle Exp. Cell Res. 166 1986 209 219
39. E. Li Chromatin modification and epigenetic reprogramming in mammalian development Nat. Rev., Genet. 3 2002 662 673
40. E. Li, T.H. Bestor, and R. Jaenisch Targeted mutation of the DNA methyltransferase gene results in embryonic lethality Cell 69 1992 915 926
41. E. Li, C. Beard, and R. Jaenisch Role for DNA methylation in genomic imprinting Nature 366 1993 362 365
42. F.L. Margolis, J. Verhaagen, S. Biffo, F.L. Huang, and M. Grillo Regulation of gene expression in the olfactory neuroepithelium: a neurogenetic matrix Prog. Brain Res. 89 1991 97 122
43. J.B. Margot, M.C. Cardoso, and H. Leonhardt Mammalian DNA methyltransferases show different subnuclear distributions J. Cell. Biochem. 83 2001 373 379
44. M. Namihira, K. Nakashima, and T. Taga Developmental stage dependent regulation of DNA methylation and chromatin modification in a immature astrocyte specific gene promoter FEBS Lett. 572 2004 184 188
45. A. Nomura Nuclear distribution of proliferating cell nuclear antigen (PCNA) in fertilized eggs of the starfish Asterina pectinifera J. Cell Sci. 107 Pt. 12 1994 3291 3300
46. M. Okano, S. Xie, and E. Li Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases Nat. Genet. 19 1998 219 220
47. M. Okano, S. Xie, and E. Li Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells Nucleic Acids Res. 26 1998 2536 2540
48. M. Okano, D.W. Bell, D.A. Haber, and E. Li DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development Cell 99 1999 247 257
49. S. Pradhan, A. Bacolla, R.D. Wells, and R.J. Roberts Recombinant human DNA (cytosine-5) methyltransferase: I. Expression, purification, and comparison of de novo and maintenance methylation J. Biol. Chem. 274 1999 33002 33010
50. A. Razin, and H. Cedar DNA methylation and gene expression Microbiol. Rev. 55 1991 451 458
51. A. Razin, and H. Cedar DNA methylation and genomic imprinting Cell 77 1994 473 476
52. K.D. Robertson, E. Uzvolgyi, G. Liang, C. Talmadge, J. Sumegi, F.A. Gonzales, and P.A. Jones The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors Nucleic Acids Res. 27 1999 2291 2298
53. A.J. Roskams, D.S. Bredt, T.M. Dawson, and G.V. Ronnett Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons Neuron 13 1994 289 299
54. A.J. Roskams, X. Cai, and G.V. Ronnett Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat Neuroscience 83 1998 191 200
55. M. Schwartz Levey, D.M. Chikaraishi, and J.S. Kauer Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography J. Neurosci. 11 1991 3556 3564
56. J.E. Schwob Neural regeneration and the peripheral olfactory system Anat. Rec. 269 2002 33 49
57. M.D. Shahbazian, B. Antalffy, D.L. Armstrong, and H.Y. Zoghbi Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation Hum. Mol. Genet. 11 2002 115 124
58. R. Sheaff, D. Ilsley, and R. Kuchta Mechanism of DNA polymerase alpha inhibition by aphidicolin Biochemistry 30 1991 8590 8597
59. I.H. Smart Location and orientation of mitotic figures in the developing mouse olfactory epithelium J. Anat. 109 1971 243 251
60. M.R. Song, and A. Ghosh FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation Nat. Neurosci. 7 2004 229 235
61. T. Takizawa, K. Nakashima, M. Namihira, W. Ochiai, A. Uemura, M. Yanagisawa, N. Fujita, M. Nakao, and T. Taga DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain Dev. Cell 1 2001 749 758
62. D.J. Weisenberger, M. Velicescu, J.C. Cheng, F.A. Gonzales, G. Liang, and P.A. Jones Role of the DNA methyltransferase variant DNMT3b3 in DNA methylation Mol. Cancer Res. 2 2004 62 72
63. A. Weiss, and H. Cedar The role of DNA demethylation during development Genes Cells 2 1997 481 486
64. L. Wong, B. Oakley, A. Lawton, and Y. Shiba Keratin 19-like immunoreactivity in receptor cells of mammalian taste buds Chem. Senses 19 1994 251 264
65. S. Xie, Z. Wang, M. Okano, M. Nogami, Y. Li, W.W. He, K. Okumura, and E. Li Cloning, expression and chromosome locations of the human DNMT3 gene family Gene 236 1999 87 95
66. G.L. Xu, T.H. Bestor, D. Bourc'his, C.L. Hsieh, N. Tommerup, M. Bugge, M. Hulten, X. Qu, J.J. Russo, and E. Viegas-Pequignot Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene Nature 402 1999 187 191
67. J.A. Yoder, N.S. Soman, G.L. Verdine, and T.H. Bestor DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe J. Mol. Biol. 270 1997 385 395
68. T.T. Yu, J.C. McIntyre, S.C. Bose, D. Hardin, M.C. Owen, and T.S. McClintock Differentially expressed transcripts from phenotypically identified olfactory sensory neurons J. Comp. Neurol. 483 2005 251 262
69. X. Zhao, T. Ueba, B.R. Christie, B. Barkho, M.J. McConnell, K. Nakashima, E.S. Lein, B.D. Eadie, A.R. Willhoite, and A.R. Muotri Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function Proc. Natl. Acad. Sci. U. S. A. 100 2003 6777 6782