Roles of the ubiquitin-proteosome system in neurogenesis

Cell Cycle

Volumn 9, Issue 16, 2010, Pages 3194-3200

  Tuoc, Tran Cong ^a,b   Stoykova, Anastassia ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

E3 ligases; Neurogenesis; Ubiquitin proteosome system (UPS)

Indexed keywords

HELIX LOOP HELIX PROTEIN; KI 67 ANTIGEN; NOTCH RECEPTOR; PROTEASOME; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR PAX6; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3;

CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; CELL SPECIFICITY; ENDOCYTOSIS; GENE EXPRESSION; HUMAN; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; NEUROPATHOLOGY; NONHUMAN; ONCOGENE C MYB; ONCOGENE C MYC; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; REVIEW; TELENCEPHALON; UBIQUITINATION;

EID: 77955729735     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.16.12551     Document Type: Review

References (64)

1. Bayer SA, Altman J. Neocortical Development 1991.
2. Guillemot F. Cell fate specification in the mammalian telencephalon. Prog Neurobiol 2007; 83:37-52. (Pubitemid 47243778)
3. Schwartz AL, Ciechanover A. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 2009; 49:73-96.
4. Tai HC, Schuman EM. Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat Rev Neurosci 2008; 9:826-38.
5. Mallamaci A, Stoykova A. Gene networks controlling early cerebral cortex arealization. Eur J Neurosci 2006; 23:847-56. (Pubitemid 43344681)
6. Gotz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005; 6:777-88.
7. Yoon K, Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 2005; 8:709-15. (Pubitemid 43085834)
8. Gaiano N, Nye JS, Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 2000; 26:395-404.
9. Louvi A, Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat Rev Neurosci 2006; 7:93-102. (Pubitemid 43151596)
10. Lai EC. Protein degradation: four E3s for the notch pathway. Curr Biol 2002; 12:74-8.
11. Koo BK, Lim HS, Song R, Yoon MJ, Yoon KJ, Moon JS, et al. Mind bomb 1 is essential for generating functional Notch ligands to activate Notch. Development 2005; 132:3459-70.
12. Itoh M, Kim CH, Palardy G, Oda T, Jiang YJ, Maust D, et al. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 2003; 4:67-82.
13. Yoon KJ, Koo BK, Im SK, Jeong HW, Ghim J, Kwon MC, et al. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 2008; 58:519-31. (Pubitemid 351672356)
14. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 2002; 3:517-30. (Pubitemid 135706662)
15. Chang PJ, Hsiao YL, Tien AC, Li YC, Pi H. Negative-feedback regulation of proneural proteins controls the timing of neural precursor division. Development 2008; 135:3021-30.
16. Shou J, Rim PC, Calof AL. BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat Neurosci 1999; 2:339-45. (Pubitemid 30491276)
17. kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev 2006; 20:1511-24.
18. Gotz M, Stoykova A, Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 1998; 21:1031-44. (Pubitemid 29018073)
19. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, et al. Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 2002; 5:308-15. (Pubitemid 34279810)
20. Stoykova A, Fritsch R, Walther C, Gruss P. Forebrain patterning defects in Small eye mutant mice. Development 1996; 122:3453-65. (Pubitemid 26395987)
21. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, et al. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 2006; 22:22.
22. Tuoc TC, Radyushkin K, Tonchev AB, Piñon MC, Ashery-Padan R, Molnár Z, et al. Selective cortical layering abnormalities and behavioral deficits in cortex-specific Pax6 knock-out mice. J Neurosci 2009; 29:8335-49.
23. Schedl A, Ross A, Lee M, Engelkamp D, Rashbass P, van Heyningen V, et al. Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 1996; 86:71-82. (Pubitemid 26256579)
24. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, et al. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 1991; 354:522-5. (Pubitemid 21896831)
25. Berger J, Berger S, Tuoc TC, D'Amelio M, Cecconi F, Gorski JA, et al. Conditional activation of Pax6 in the developing cortex of transgenic mice causes progenitor apoptosis. Development 2007; 134:1311-22. (Pubitemid 46706038)
26. Manuel M, Georgala PA, Carr CB, Chanas S, Kleinjan DA, Martynoga B, et al. Controlled overexpression of Pax6 in vivo negatively autoregulates the Pax6 locus, causing cell-autonomous defects of late cortical progenitor proliferation with little effect on cortical arealization. Development 2007; 134:545-55.
27. Schmahl W, Knoedlseder M, Favor J, Davidson D. Defects of neuronal migration and the pathogenesis of cortical malformations are associated with Small eye (Sey) in the mouse, a point mutation at the Pax-6-locus. Acta Neuropathol (Berl) 1993; 86:126-35. (Pubitemid 23265600)
28. Tuoc TC, Stoykova A. Trim11 modulates the function of neurogenic transcription factor Pax6 through ubiquitin-proteosome system. Genes Dev 2008; 22:1972-86. (Pubitemid 352008644)
29. Niikura T, Hashimoto Y, Tajima H, Ishizaka M, Yamagishi Y, Kawasumi M, et al. A tripartite motif protein TRIM11 binds and destabilizes Humanin, a neuroprotective peptide against Alzheimer's disease-relevant insults. Eur J Neurosci 2003; 17:1150-8.
30. Ishikawa H, Tachikawa H, Miura Y, Takahashi N. TRIM11 binds to and destabilizes a key component of the activator-mediated cofactor complex (ARC105) through the ubiquitin-proteasome system. FEBS Lett 2006; 580:4784-92. (Pubitemid 44286834)
31. Suzumori N, Burns KH, Yan W, Matzuk MM. RFPL4 interacts with oocyte proteins of the ubiquitin-proteasome degradation pathway. Proc Natl Acad Sci USA 2003; 100:550-5.
32. Cyr DM, Hohfeld J, Patterson C. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci 2002; 27:368-75. (Pubitemid 34756520)
33. Elsasser S, Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat Cell Biol 2005; 7:742-9. (Pubitemid 41079042)
34. McClellan AJ, Tam S, Kaganovich D, Frydman J. Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 2005; 7:736-41. (Pubitemid 41079041)
35. Hasty J, McMillen D, Collins JJ. Engineered gene circuits. Nature 2002; 420:224-30.
36. Scardigli R, Baumer N, Gruss P, Guillemot F, Le Roux I. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 2003; 130:3269-81. (Pubitemid 36926963)
37. Tuoc TC, Stoykova A. Er81 is a downstream target of Pax6 in cortical progenitors. BMC Dev Biol 2008; 8:23. (Pubitemid 351661399)
38. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 2005; 121:645-57. (Pubitemid 40720016)
39. Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A, et al. SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 2008; 452:370-4.
40. Dehay C, Kennedy H. Cell cycle control and cortical development. Nat Rev Neurosci 2007; 8:438-50. (Pubitemid 46789227)
41. Fults D, Pedone C, Dai C, Holland EC. MYC expression promotes the proliferation of neural progenitor cells in culture and in vivo. Neoplasia 2002; 4:32-9. (Pubitemid 34075888)
42. Lassman AB, Dai C, Fuller GN, Vickers AJ, Holland EC. Overexpression of c-MYC promotes an undifferentiated phenotype in cultured astrocytes and allows elevated Ras and Akt signaling to induce gliomas from GFAP-expressing cells in mice. Neuron Glia Biol 2004; 1:157-63.
43. Schwamborn JC, Berezikov E, Knoblich JA. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 2009; 136:913-25.
44. Knoepfler PS, Cheng PF, Eisenman RN. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 2002; 16:2699-712.
45. Zhao X, Heng JI, Guardavaccaro D, Jiang R, Pagano M, Guillemot F, et al. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat Cell Biol 2008; 10:643-53. (Pubitemid 351772930)
46. Yu ZK, Gervais JL, Zhang H. Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. Proc Natl Acad Sci USA 1998; 95:11324-9. (Pubitemid 28450127)
47. Nakayama K, Nagahama H, Minamishima YA, Matsumoto M, Nakamichi I, Kitagawa K, et al. Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J 2002; 19:2069-81.
48. Cip1 in S phase. J Biol Chem 2003; 278:25752-7.
49. Boix-Perales H, Horan I, Wise H, Lin HR, Chuang LC, Yew PR, et al. The E3 ubiquitin ligase skp2 regulates neural differentiation independent from the cell cycle. Neural Develop 2007; 2:27.
50. Kriegstein AR, Noctor SC. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 2004; 27:392-9.
51. Arnaud L, Ballif BA, Cooper JA. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol Cell Biol 2003; 23:9293-302. (Pubitemid 37499816)
52. Feng L, Allen NS, Simo S, Cooper J.A. Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes Dev 2007; 21:2717-30. (Pubitemid 350070719)
53. Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN, et al. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation- dependent c-Myc protein degradation. Proc Natl Acad Sci USA 2004; 101:9085-90. (Pubitemid 38781615)
54. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, Radtke F, et al. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 2008; 60:273-84.
55. Schwamborn JC, Muller M, Becker AH, Puschel AW. Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 2007; 26:1410-22. (Pubitemid 46398703)
56. Patrick GN, Zhou P, Kwon YT, Howley PM, Tsai LH. p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J Biol Chem 1998; 273:24057-64. (Pubitemid 28435748)
57. Qiu L, Joazeiro C, Fang N, Wang HY, Elly C, Altman Y, et al. Recognition and ubiquitination of Notch by Itch, a hect-type E3 ubiquitin ligase. J Biol Chem 2000; 275:35734-7.
58. Bock HH, Jossin Y, May P, Bergner O, Herz J. Apolipoprotein E receptors are required for reelin-induced proteasomal degradation of the neuronal adaptor protein Disabled-1. J Biol Chem 2004; 279:33471-9. (Pubitemid 39062996)
59. Mavrakis KJ, Andrew RL, Lee KL, Petropoulou C, Dixon JE, Navaratnam N, et al. Arkadia enhances Nodal/TGF-beta signaling by coupling phospho-Smad2/3 activity and turnover. PLoS Biol 2007; 5:67.
60. Angers S, Thorpe CJ, Biechele TL, Goldenberg SJ, Zheng N, MacCoss MJ, et al. The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nat Cell Biol 2006; 8:348-57.
61. An JY, Seo JW, Tasaki T, Lee MJ, Varshavsky A, Kwon YT. Impaired neurogenesis and cardiovascular development in mice lacking the E3 ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Proc Natl Acad Sci USA 2006; 103:6212-7.
62. Gray PA, Fu H, Luo P, Zhao Q, Yu J, Ferrari A, et al. Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 2004; 306:2255-7.
63. Freemont PS. RING for destruction? Curr Biol 2000; 10:84-7.
64. Joazeiro CA, Weissman AM. RING finger proteins: mediators of ubiquitin ligase activity. Cell 2000; 102:549-52.