Trim11 modulates the function of neurogenic transcription factor Pax6 through ubiquitin-proteosome system

Genes and Development

Volumn 22, Issue 14, 2008, Pages 1972-1986

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

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

Cortex; Neurogenesis; Pax6; Ubiquitin proteosome system

Indexed keywords

PROTEIN TRIM11; TRANSCRIPTION FACTOR PAX6; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION INITIATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; ELECTROPORATION; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOPRECIPITATION; INCLUSION BODIES; MICE; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEASOME ENDOPEPTIDASE COMPLEX; REPRESSOR PROTEINS; SEQUENCE DELETION; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; ZINC FINGERS;

EID: 47549099397     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.471708     Document Type: Article

References (51)

1. Alves-Rodrigues, A., Gregori, L., and Figueiredo-Pereira, M.E. 1998. Ubiquitin, cellular inclusions and their role in neuro-degeneration. Trends Neurosci. 21: 516-520.
2. An, J.Y., Seo, J.W., Tasaki, T., Lee, M.J., Varshavsky, A., and Kwon, Y.T. 2006. 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. 103: 6212-6217.
3. Arnaud, L., Ballif, B.A., and Cooper, J.A. 2003. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23: 9293-9302.
4. Berger, J., Berger, S., Tuoc, T.C., D'Amelio, M., Cecconi, F., Gorski, J.A., Jones, K.R., Gruss, P., and Stoykova, A. 2007. Conditional activation of Pax6 in the developing cortex of transgenic mice causes progenitor apoptosis. Development 134: 1311-1322.
5. Bishop, K.M., Rubenstein, J.L., and O'Leary, D.D. 2002. Distinct actions of Emx1, Emx2, and Pax6 in regulating the specification of areas in the developing neocortex. J. Neurosci. 22:7627-7638.
6. Bock, H.H., Jossin, Y., May, P., Bergner, O., and Herz, J. 2004. Apolipoprotein E receptors are required for reelin-induced proteasomal degradation of the neuronal adaptor protein Disabled-1. J. Biol. Chem. 279: 33471-33479.
7. Callaerts, P., Halder, G., and Gehring, W.J. 1997. PAX-6 in development and evolution. Annu. Rev. Neurosci. 20: 483-532.
8. Cyr, D.M., Hohfeld, J., and Patterson, C. 2002. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27: 368-375.
9. Elsasser, S. and Finley, D. 2005. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7: 742-749.
10. Epstein, J., Cai, J., Glaser, T., Jepeal, L., and Maas, R. 1994. Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes. J. Biol. Chem. 269: 8355-8361.
11. Frydman, J. and Hartl, F.U. 1996. Principles of chaperone-as-sisted protein folding: Differences between in vitro and in vivo mechanisms. Science 272: 1497-1502.
12. Gotz, M., Stoykova, A., and Gruss, P. 1998. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21: 1031-1044.
13. Guillemot, F., Molnar, Z., Tarabykin, V., and Stoykova, A. 2006. Molecular mechanisms of cortical differentiation. Eur. J. Neurosci. 23: 857-868.
14. Hasty, J., McMillen, D., and Collins, J.J. 2002. Engineered gene circuits. Nature 420: 224-230.
15. Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K.L., Hack, M.A., Chapouton, P., Barde, Y.A., and Gotz, M. 2002. Glial cells generate neurons: The role of the transcription factor Pax6. Nat. Neurosci. 5: 308-315.
16. Hershko, A. and Ciechanover, A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67: 425-479.
17. Hicke, L., Schubert, H.L., and Hill, C.P. 2005. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6: 610-621.
18. Hill, R.E., Favor, J., Hogan, B.L., Ton, C.C., Saunders, G.F., Hanson, I.M., Prosser, J., Jordan, T., Hastie, N.D., and van Hey-ningen, V. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354: 522-525.
19. Ishikawa, H., Tachikawa, H., Miura, Y., and Takahashi, N. 2006. TRIM11 binds to and destabilizes a key component of the activator-mediated cofactor complex (ARC105) through the ubiquitin-proteasome system. FEBS Lett. 580: 4784-4792.
20. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yama-mura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. 1998. Mutations in the parkin gene cause auto-somal recessive juvenile parkinsonism. Nature 392: 605-608.
21. Leng, R.P., Lin, Y., Ma, W., Wu, H., Lemmers, B., Chung, S., Parant, J.M., Lozano, G., Hakem, R., and Benchimol, S. 2003. Pirh2, a p53-induced ubiquitin-protein ligase, promotes p53 degradation. Cell 112: 779-791.
22. Mallamaci, A. and Stoykova, A. 2006. Gene networks controlling early cerebral cortex arealization. Eur. J. Neurosci. 23: 847-856.
23. Manuel, M., Georgala, P.A., Carr, C.B., Chanas, S., Kleinjan, D.A., Martynoga, B., Mason, J.O., Molinek, M., Pinson, J., Pratt, T., et al. 2007. 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 134: 545-555.
24. McClellan, A.J., Tam, S., Kaganovich, D., and Frydman, J. 2005. Protein quality control: Chaperones culling corrupt conformations. Nat. Cell Biol. 7: 736-741.
25. Meroni, G. and Diez-Roux, G. 2005. TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. Bioessays 27: 1147-1157.
26. Miller, V.M., Nelson, R.F., Gouvion, C.M., Williams, A., Rodriguez-Lebron, E., Harper, S.Q., Davidson, B.L., Rebagliati, M.R., and Paulson, H.L. 2005. CHIP suppresses polyglutamine aggregation and toxicity in vitro and in vivo. J. Neurosci. 25: 9152-9161.
27. Muchowski, P.J. and Wacker, J.L. 2005. Modulation of neuro-degeneration by molecular chaperones. Nat. Rev. Neurosci. 6: 11-22.
28. Muzio, L., DiBenedetto, B., Stoykova, A., Boncinelli, E., Gruss, P., and Mallamaci, A. 2002. Emx2 and Pax6 control region-alization of the pre-neuronogenic cortical primordium. Cereb. Cortex 12: 129-139.
29. Nasrallah, I.M., Minarcik, J.C., and Golden, J.A. 2004. A polyalanine tract expansion in Arx forms intranuclear inclusions and results in increased cell death. J. Cell Biol. 167: 411-416.
30. Niikura, T., Hashimoto, Y., Tajima, H., Ishizaka, M., Yamagi-shi, Y., Kawasumi, M., Nawa, M., Terashita, K., Aiso, S., and Nishimoto, I. 2003. A tripartite motif protein TRIM11 binds and destabilizes Humanin, a neuroprotective peptide against Alzheimer's disease-relevant insults. Eur. J. Neurosci. 17: 1150-1158.
31. Niwa, J., Ishigaki, S., Hishikawa, N., Yamamoto, M., Doyu, M., Murata, S., Tanaka, K., Taniguchi, N., and Sobue, G. 2002. Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J. Biol. Chem. 277: 36793-36798.
32. Patrick, G.N., Zhou, P., Kwon, Y.T., Howley, P.M., and Tsai, L.H. 1998. p35, the neuronal-specific activator of cyclin-de-pendent kinase 5 (Cdk5) is degraded by the ubiquitin-protea-some pathway. J. Biol. Chem. 273: 24057-24064.
33. Qiu, L., Joazeiro, C., Fang, N., Wang, H.Y., Elly, C., Altman, Y., Fang, D., Hunter, T., and Liu, Y.C. 2000. Recognition and ubiquitination of Notch by Itch, a hect-type E3 ubiquitin ligase. J. Biol. Chem. 275: 35734-35737.
34. Quinn, J.C., Molinek, M., Martynoga, B.S., Zaki, P.A., Faedo, A., Bulfone, A., Hevner, R.F., West, J.D., and Price, D.J. 2006. 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. 302: 50-65.
35. Remedios, R., Huilgol, D., Saha, B., Hari, P., Bhatnagar, L., Kowalczyk, T., Hevner, R.F., Suda, Y., Aizawa, S., Ohshima, T., et al. 2007. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neo-cortex. Nat. Neurosci. 10: 1141-1150.
36. Reymond, A., Meroni, G., Fantozzi, A., Merla, G., Cairo, S., Luzi, L., Riganelli, D., Zanaria, E., Messali, S., Cainarca, S., et al. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20: 2140-2151.
37. Rubinsztein, D.C. 2006. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443: 780-786.
38. Sakurai, M., Ayukawa, K., Setsuie, R., Nishikawa, K., Hara, Y., Ohashi, H., Nishimoto, M., Abe, T., Kudo, Y., Sekiguchi, M., et al. 2006. Ubiquitin C-terminal hydrolase L1 regulates the morphology of neural progenitor cells and modulates their differentiation. J. Cell Sci. 119: 162-171.
39. Scardigli, R., Baumer, N., Gruss, P., Guillemot, F., and Le Roux, I. 2003. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 130: 3269-3281.
40. Schedl, A., Ross, A., Lee, M., Engelkamp, D., Rashbass, P., van Heyningen, V., and Hastie, N.D. 1996. Influence of PAX6 gene dosage on development: Overexpression causes severe eye abnormalities. Cell 86: 71-82.
41. Schmahl, W., Knoedlseder, M., Favor, J., and Davidson, D. 1993. 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.) 86: 126-135.
42. Schubert, U., Anton, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W., and Bennink, J.R. 2000. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
43. Simpson, T.I. and Price, D.J. 2002. Pax6; a pleiotropic player in development. Bioessays 24: 1041-1051.
44. Stoykova, A., Fritsch, R., Walther, C., and Gruss, P. 1996. Fore-brain patterning defects in Small eye mutant mice. Development 122: 3453-3465.
45. Stoykova, A., Gotz, M., Gruss, P., and Price, J. 1997. Pax6-de-pendent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124: 3765-3777.
46. Stoykova, A., Treichel, D., Hallonet, M., and Gruss, P. 2000. Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20: 8042-8050.
47. Suzumori, N., Burns, K.H., Yan, W., and Matzuk, M.M. 2003. RFPL4 interacts with oocyte proteins of the ubiquitin-pro-teasome degradation pathway. Proc. Natl. Acad. Sci. 100: 550-555.
48. Tole, S., Remedios, R., Saha, B., and Stoykova, A. 2005. Selective requirement of Pax6, but not Emx2, in the specification and development of several nuclei of the amygdaloid complex. J. Neurosci. 25: 2753-2760.
49. Tuoc, T.C. and Stoykova, A. 2008. Er81 is a downstream target of Pax6 in cortical progenitors. BMC Dev. Biol. 8: 23. doi: 10.1186/1471-213X-8-23.
50. Warren, N., Caric, D., Pratt, T., Clausen, J.A., Asavaritikrai, P., Mason, J.O., Hill, R.E., and Price, D.J. 1999. The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb. Cortex 9: 627-635.
51. Wu, X., Bayle, J.H., Olson, D., and Levine, A.J. 1993. The p53-mdm-2 autoregulatory feedback loop. Genes & Dev. 7: 1126-1132.