Generation of neuronal variability and complexity

Nature

Volumn 441, Issue 7097, 2006, Pages 1087-1093

  Muotri, Alysson R ^a   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; BIOMEDICAL ENGINEERING; CELLS; COGNITIVE SYSTEMS; MEDICINE; NEUROLOGY; TISSUE;

NEURONAL CELLS; NEURONS; REGENERATIVE MEDICINE; STEM CELLS; TISSUE REPLACEMENT;

CYTOLOGY;

COGNITION; MEDICINE; NERVOUS SYSTEM;

ALTERNATIVE RNA SPLICING; ANEUPLOIDY; COGNITION; DENTATE GYRUS; DNA TRANSPOSITION; EMBRYO DEVELOPMENT; EPIGENETICS; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; MENTAL DISEASE; NERVE CELL; NERVE CELL DIFFERENTIATION; OPEN READING FRAME; PERSONALITY; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; REGENERATIVE MEDICINE; RETROPOSON; REVIEW; RNA EDITING; STEM CELL; TISSUE REPAIR;

EID: 33745593721     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04959     Document Type: Review

References (96)

1. Koch, C. & Laurent, G. Complexity and the nervous system. Science 284, 96-98 (1999).
2. Vogel, E. K. & Machizawa, M. G. Neural activity predicts individual differences in visual working memory capacity. Nature 428, 748-751 (2004).
3. Williams, R. W. Mapping genes that modulate mouse brain development: a quantitative genetic approach. Results Probl. Cell Differ. 30, 21-49 (2000).
4. Pakkenberg, B. et al. Aging and the human neocortex. Exp. Gerontol. 38, 95-99 (2003).
5. Angevine, J. B. Jr. Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J. Comp. Neurol. 139, 129-187 (1970).
6. Finlay, B. L. & Slattery, M. Local differences in the amount of early cell death in neocortex predict adult local specializations. Science 219, 1349-1351 (1983).
7. Ferrer, I., Soriano, E., del Rio, J. A., Alcantara, S. & Auladell, C. Cell death and removal in the cerebral cortex during development. Prog. Neurobiol. 39, 1-43 (1992).
8. Oppenheim, R.W. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501 (1991).
9. Lie, D. C., Song, H., Colamarino, S. A., Ming, G. L. & Gage, F. H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 44, 399-421 (2004).
10. Taupin, P. & Gage, F. H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745-749 (2002).
11. Gage, F. H. Mammalian neural stem cells. Science 287, 1433-1438 (2000).
12. Jones, J. M. & Gellert, M. The taming of a transposon: V(D)J recombination and the immune system. Immunol. Rev. 200, 233-248 (2004).
13. Gotz, M. & Sommer, L. Cortical development: the art of generating cell diversity. Development 132, 3327-3332 (2005).
14. Burgess, N. & O'Keefe, J. Neural representations in human spatial memory. Trends Cogn. Sci. 7, 517-519 (2003).
15. Gao, Y. et al. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95, 891-902 (1998).
16. Matsuoka, M. et al. Detection of somatic DNA recombination in the transgenic mouse brain. Science 254, 81-86 (1991).
17. Abeliovich, A. et al. On somatic recombination in the central nervous system of transgenic mice. Science 257, 404-410 (1992).
18. Eggan, K. et al. Mice cloned from olfactory sensory neurons. Nature 428, 44-49 (2004).
19. Li J., Ishii, T., Feinstein, P. & Mombaerts, P. Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428, 393-399 (2004).
20. Ogasawara, M., Aoki, K., Okada, S. & Suzumori, K. Embryonic karyotype of abortuses in relation to the number of previous miscarriages. Fertil. Steril. 73, 300-304 (2000).
21. Pathak, S. & Multani, A. S. Aneuploidy, stem cells and cancer. EXS 2006, 49-64 (2006).
22. Palmer, T. D., Takahashi, J. & Gage, F. H. The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 8, 389-404 (1997).
23. Rehen, S. K. et al. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl Acad. Sci. USA 98, 13361-13366 (2001).
24. Rehen, S. K. et al. Constitutional aneuploidy in the normal human brain. J. Neurosci. 25, 2176-2180 (2005).
25. Fuller, C. E. & Perry, A. Fluorescence in situ hybridization (FISH) in diagnostic and investigative neuropathology. Brain Pathol. 12, 67-86 (2002).
26. Kingsbury, M. A. et al. Aneuploid neurons are functionally active and integrated into brain circuitry. Proc. Natl Acad. Sci. USA 102, 6143-6147 (2005).
27. Gaudet, J. & Mango, S. E. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295, 821-825 (2002).
28. Yang, A. H. et al. Chromosome segregation defects contribute to aneuploidy in normal neural progenitor cells. J. Neurosci. 23, 10454-10462 (2003).
29. Muotri, A. R. et al. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435, 903-910 (2005).
30. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
31. Gibbs, R. A. et al. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428, 493-521 (2004).
32. Waterston, R. H. et al. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562 (2002).
33. Wei, W. et al. Human L1 retrotransposition: cis preference versus transcomplementation. Mol. Cell. Biol. 21, 1429-1439 (2001).
34. Esnault, C., Maestre, J. & Heidmann, T. Human LINE retrotransposons generate processed pseudogenes. Nature Genet. 24, 363-367 (2000).
35. Dewannieux, M., Esnault, C. & Heidmann, T. LINE-mediated retrotransposition of marked Alu sequences. Nature Genet. 35, 41-48 (2003).
36. Kajikawa, M. & Okada, N. LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 111, 433-444 (2002).
37. Gilbert, N., Lutz, S., Morrish, T. A. & Moran, J. V. Multiple fates of L1 retrotransposition intermediates in cultured human cells. Mol. Cell. Biol. 25, 7780-7795 (2005).
38. Kazazian, H. H. Jr. Mobile elements: drivers of genome evolution. Science 303, 1626-1632 (2004).
39. Smale, S. T. & Kadonaga, J. T. The RNA polymerase II core promoter. Annu. Rev. Biochem. 72, 449-479 (2003).
40. Ayoubi, T. A. & Van De Ven, W. J. Regulation of gene expression by alternative promoters. FASEB J. 10, 453-460 (1996).
41. Myers, S. J., Dingledine, R. & Borges, K. Genetic regulation of glutamate receptor ion channels. Annu. Rev. Pharmacol. Toxicol. 39, 221-241 (1999).
42. 2+ channels. J. Biol. Chem. 275, 17269-17275 (2000).
43. Liu, Q. R. et al. Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res. 1067, 1-12 (2006).
44. Metsis, M., Timmusk, T., Arenas, E. & Persson, H. Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc. Natl Acad. Sci. USA 90, 8802-8806 (1993).
45. Maniatis, T. & Tasic, B. Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418, 236-243 (2002).
46. Yeo, G., Holste, D., Kreiman, G. & Burge, C. B. Variation in alternative splicing across human tissues. Genome Biol. 5, R74 (2004).
47. Grabowski, P. J. & Black, D. L. Alternative RNA splicing in the nervous system. Prog. Neurobiol. 65, 289-308 (2001).
48. Dredge, B. K., Polydorides, A. D. & Darnell, R. B. The splice of life: alternative splicing and neurological disease. Nature Rev. Neurosci. 2, 43-50 (2001).
49. Schmucker, D. et al. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671-684 (2000).
50. Missler, M. & Sudhof, T. C. Neurexins: three genes and 1001 products. Trends Genet. 14, 20-26 (1998).
51. Wu, Q. & Maniatis, T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790 (1999).
52. Tasic, B. et al. Promoter choice determines splice site selection in protocadherin α and γ pre-mRNA splicing. Mol. Cell 10, 21-33 (2002).
53. Daoud, R., Da Penha Berzaghi, M., Siedler, F., Hubener, M. & Stamm, S. Activity-dependent regulation of alternative splicing patterns in the rat brain. Eur. J. Neurosci. 11, 788-802 (1999).
54. Vezzani, A., Speciale, C., Della Vedova, F., Tamburin, M. & Benatti, L. Alternative splicing at the C-terminal but not at the N-terminal domain of the NMDA receptor NR1 is altered in the kindled hippocampus. Eur. J. Neurosci. 7, 2513-2517 (1995).
55. Wang, Z. & Grabowski, P. J. Cell-and stage-specific splicing events resolved in specialized neurons of the rat cerebellum. RNA 2, 1241-1253 (1996).
56. Black, D. L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72, 291-336 (2003).
57. Young, J. I. et al. Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2. Proc. Natl Acad. Sci. USA 102, 17551-17558 (2005).
58. Edwalds-Gilbert, G., Veraldi, K. L. & Milcarek, C. Alternative poly(A) site selection in complex transcription units: means to an end? Nucleic Acids Res. 25, 2547-2561 (1997).
59. Balmer, D., Goldstine, J., Rao, Y. M. & LaSalle, J. M. Elevated methyl-CpG-binding protein 2 expression is acquired during postnatal human brain development and is correlated with alternative polyadenylation. J. Mol. Med. 81, 61-68 (2003).
60. Pelka, G. J., Watson, C. M., Christodoulou, J. & Tam, P. P. Distinct expression profiles of Mecp2 transcripts with different lengths of 3′ UTR in the brain and visceral organs during mouse development. Genomics 85, 441-452 (2005).
61. Zhang, H., Lee, J. Y. & Tian, B. Biased alternative polyadenylation in human tissues. Genome Biol. 6, R100 (2005).
62. de Moor, C. H., Meijer, H. & Lissenden, S. Mechanisms of translational control by the 3′ UTR in development and differentiation. Semin. Cell Dev. Biol. 16, 49-58 (2005).
63. Keegan, L. P., Gallo, A. & O'Connell, M. A. The many roles of an RNA editor. Nature Rev. Genet. 2, 869-878 (2001).
64. Paul, M. S. &Bass, B. L. Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. EMBO J. 17, 1120-1127 (1998).
65. Tonkin, L. A. et al. RNA editing by ADARs is important for normal behavior in Caenorhabditis elegans. EMBO J. 21, 6025-6035 (2002).
66. Palladino, M. J., Keegan, L. P., O'Connell, M. A. & Reenan, R. A. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102, 437-449 (2000).
67. Keegan, L. P., Gallo, A. & O'Connell, M. A. Development. Survival is impossible without an editor. Science 290, 1707-1709 (2000).
68. Dingledine, R., Borges, K., Bowie, D. & Traynelis, S. F. The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61 (1999).
69. Vissel, B. et al. The role of RNA editing of kainate receptors in synaptic plasticity and seizures. Neuron 29, 217-227 (2001).
70. Kwak, S. & Kawahara, Y. Deficient RNA editing of Glu R2 and neuronal death in amyotropic lateral sclerosis. J. Mol. Med. 83, 110-120 (2005).
71. Niswender, C. M., Copeland, S. C., Herrick-Davis, K., Emeson, R. B. & Sanders-Bush, E. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J. Biol. Chem. 274, 9472-9478 (1999).
72. 2C receptor: alterations in suicide and implications for serotonergic pharmacotherapy. Neuropsychopharmacology 24, 478-491 (2001).
73. Akbarian, S., Smith, M. A. & Jones, E. G. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res. 699, 297-304 (1995).
74. Gurevich, I. et al. Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims. Neuron 34, 349-356 (2002).
75. Grant, S. G. The synapse proteome and phosphoproteome: a new paradigm for synapse biology. Biochem. Soc. Trans. 34, 59-63 (2006).
76. Flavell, S. W. et al. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012 (2006).
77. Shalizi, A. et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017 (2006).
78. Gottesman, I. I. & Hanson, D. R. Human development: biological and genetic processes. Annu. Rev. Psychol. 56, 263-286 (2005).
79. Branchi, I., Francia, N. &Alleva, E. Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behav. Pharmacol. 15, 353-362 (2004).
80. Sims, R. J., Nishioka, K. & Reinberg, D. Histone lysine methylation: a signature for chromatin function. Trends Genet. 19, 629-639 (2003).
81. Stadler, F. et al. Histone methylation at gene promoters is associated with developmental regulation and region-specific expression of ionotropic and metabotropic glutamate receptors in human brain. J. Neurochem. 94, 324-336 (2005).
82. Karlsson, H. et al. Retroviral RNA identified in the cerebrospinal fluids and brains of individuals with schizophrenia. Proc. Natl Acad. Sci USA 98, 4634-4639 (2001).
83. Yee, F. & Yolken, R. H. Identification of differentially expressed RNA transcripts in neuropsychiatric disorders. Biol. Psychiatry 41, 759-761 (1997).
84. Kim, H. S., Takenaka, O. & Crow, T. J. Isolation and phylogeny of endogenous retrovirus sequences belonging to the HERV-W family in primates. J. Gen. Virol. 80, 2613-2619 (1999).
85. Frank, O. et al. Human endogenous retrovirus expression profiles in samples from brains of patients with schizophrenia and bipolar disorders. J. Virol. 79, 10890-10901 (2005).
86. Yolken, R. H., Karlsson, H., Yee, F., Johnston-Wilson, N. L. & Torrey, E. F. Endogenous retroviruses and schizophrenia. Brain Res. Brain Res. Rev. 31, 193-199 (2000).
87. Kan, P. X., Popendikyte, V., Kaminsky, Z. A., Yolken, R. H. & Petronis, A. Epigenetic studies of genomic retroelements in major psychosis. Schizophr. Res. 67, 95-106 (2004).
88. Cao, X., Yeo, G., Muotri, A. R., Kuwabara, T. & Gage, F. H. Noncoding RNAs in the mammalian central nervous system. Annu. Rev. Neurosci. Published online 15 Mar 2006 (doi:10.1146/annurev.neuro.29.051605.112839).
89. Kosik, K. S. & Krichevsky, A. M. The elegance of the microRNAs: a neuronal perspective. Neuron 47, 779-782 (2005).
90. Pasquinelli, A. E., Hunter, S. & Bracht, J. MicroRNAs: a developing story. Curr. Opin. Genet. Dev. 15, 200-205 (2005).
91. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
92. Kuwabara, T., Hsieh J., Nakashima, K., Taira, K. & Gage, F. H. A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116, 779-793 (2004).
93. Belancio, V. P., Hedges, D. J. & Deininger, P. LINE-1RNA splicing and influences on mammalian gene expression. Nucleic Acids Res. 34, 1512-1521 (2006).
94. Roy-Engel, A. M. et al. Human retroelements may introduce intragenic polyadenylation signals. Cytogenet. Genome Res. 110, 365-371 (2005).
95. Meischl, C., Boer, M., Ahlin, A. & Roos, D. A new exon created by intronic insertion of a rearranged LINE-1 element as the cause of chronic granulomatous disease. Eur. J. Hum. Genet. 8, 697-703 (2000).
96. Francesconi, A. & Duvoisin, R. M. Alternative splicing un masks dendritic and axonal targeting signals in metabotropic glutamate receptor 1. J. Neurosci. 22, 2196-2205 (2002).