APC/C regulation of axonal growth and synaptic functions in postmitotic neurons: The Liprin-α connection

Cellular and Molecular Life Sciences

Volumn 62, Issue 14, 2005, Pages 1571-1578

  Teng, F Y H ^a   Tang, B L ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Anaphase promoting complex cyclosome (APC C); Cdh 1; Liprin , neuron; Synapse

Indexed keywords

AMPA RECEPTOR; ANAPHASE PROMOTING COMPLEX; CD45 ANTIGEN; CYCLINE; GLUTAMATE RECEPTOR 1; LIPRIN ALPHA PROTEIN; PROTEIN; RAC PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; UVOMORULIN;

BRAIN; CELL CYCLE; CELL DIVISION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DROSOPHILA; EXPERIMENTAL MODEL; GROWTH CONE; INVERTEBRATE; MAMMAL; MAMMAL CELL; MEIOSIS; MITOSIS; NERVE CELL; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROMUSCULAR SYNAPSE; NEUROPATHOLOGY; NEUROPHYSIOLOGY; NONHUMAN; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SYNAPSE; UBIQUITINATION;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; DROSOPHILA; DROSOPHILA PROTEINS; MAMMALS; MODELS, BIOLOGICAL; NEURONS; PHOSPHOPROTEINS; SYNAPSES; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 22544436433     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-005-5043-1     Document Type: Review

References (72)

1. Hershko A. and Ciechanover A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67: 425-479
2. Fang S. and Weissman A. M. (2004) A field guide to ubiquitylation. Cell. Mol. Life Sci. 61: 1546-1561
3. Passmore L. A. and Barford D. (2004) Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem. J. 379: 513-525
4. Reed S. I. (2003) Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover. Nat. Rev. Mol. Cell Biol. 4: 855-864
5. Vodermaier H. C. (2004) APC/C and SCF: controlling each other and the cell cycle. Curr. Biol. 14: R787-796
6. Peters J. M. (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9: 931-943
7. Harper J. W., Burton J. L. and Solomon M. J. (2002) The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16: 2179-2206
8. Bence N. F., Sampat R. M. and Kopito R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292: 1552-1555
9. Johnston J. A. and Madura K. (2004) Rings, chains and ladders: ubiquitin goes to work in the neuron. Prog. Neurobiol. 73: 227-257
10. Steward O. and Schuman E. M. (2003) Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40: 347-359
11. Campbell D. S. and Holt C. E. (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32: 1013-1026
12. Van Horck F. P., Weinl C. and Holt C. E. (2004) Retinal axon guidance: novel mechanisms for steering. Curr. Opin. Neurobiol. 14: 61-66
13. Myat A., Henry P., McCabe V., Flintoft L., Rotin D. and Tear G. (2002) Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35: 447-459
14. Keleman K., Rajagopalan S., Cleppien D., Teis D., Paiha K., Huber L. A. et al. (2002) Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110: 415-427
15. Watts R. J., Hoopfer E. D. and Luo L. (2003) Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38: 871-885
16. DiAntonio A., Haghighi A. P., Portman S. L., Lee J. D., Amaranto A. M. and Goodman C. S. (2001) Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412: 449-452
17. Cline H. (2003) Synaptic plasticity: importance of proteosome-mediated protein turnover. Curr. Biol. 13: R514-R516
18. Hegde A. N., Goldberg A. L. and Schwartz J. H. (1993) Regulatory subunits of cAMP-dependent protein kinases are degraded after conjugation to ubiquitin: a molecular mechanism underlying long-term synaptic plasticity. Proc. Natl. Acad. Sci. USA 90: 7436-7440
19. Zhao Y., Hegde A. N. and Martin K. C. (2003) The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Curr. Biol. 13: 887-898
20. Speese S. D., Trotta N., Rodesch C. K., Aravamudan B. and Broadie K. (2003) The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 13: 899-910
21. Patrick G. N., Bingol B., Weld H. A. and Schuman E. M. (2003) Ubiquitin-mediated proteasome activity is required for agonistinduced endocytosis of GluRs. Curr. Biol. 13: 2073-2081
22. Kishino T., Lalande M. and Wagstaff J. (1997) UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15: 70-73
23. Giasson B. I. and Lee V. M. (2003) Are ubiquitination pathways central to Parkinson's disease? Cell 114: 1-8
24. Ross C. A. and Pickart C. M. (2004) The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol. 14: 703-711
25. Petrucelli L. and Dawson T. M. (2004) Mechanism of neurodegenerative disease: role of the ubiquitin proteasome system. Ann. Med. 36: 315-320
26. Imai Y. and Takahasi R. (2004) How do Parkin mutations result in neurodegeneration? Curr. Opin. Neurobiol. 14: 384-389
27. Liu C. L., Martone M. E. and Hu B. R. (2004) Protein ubiquitination in postsynaptic densities after transient cerebral ischemia. J. Cereb. Blood Flow Metab. 24: 1219-1225
28. Zhen M., Huang X., Bamber B. and Jin Y. (2000) Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26: 331-343
29. Schaefer A. M., Hadwiger G. D. and Nonet M. L. (2000) rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26: 345-356
30. Wan H. I., DiAntonio A., Fetter R. D., Bergstrom K., Strauss R. and Goodman C. S. (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26: 313-329
31. Chang Q. and Balice-Gordon R. J. (2000) Highwire, rpm-1 and futsch: balancing synaptic growth and stability. Neuron 26: 287-290
32. Nakata K., Abrams B., Grill B., Goncharov A., Huang X., Chisholm A. D. et al. (2005) Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120: 407-420
33. Liao E. H., Hung W., Abrams B. and Zhen M. (2004) An SCF-like ubiquitin ligase complex that controls presynaptic differentiation. Nature 430: 345-350
34. Wan Y. and Kirschner M. W. (2001) The anaphase-promoting complex mediates TGF-beta signaling by targeting SnoN for destruction. Mol. Cell 8: 1027-1039
35. Reed B. H. and Orr-Weaver T. L. (1997) The Drosophila gene morula inhibits mitotic functions in the endo cell cycle and the mitotic cell cycle. Development 124: 3543-3553
36. Van Roessel P., Elliott D. A., Robinson I. M., Prokop A. and Brand A. H. (2004) Independent regulation of synaptic size and activity by the anaphase-promoting complex. Cell 119: 707-718
37. Juo P. and Kaplan J. M. (2004) The anaphase-promoting complex regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Curr. Biol. 14: 2057-2062
38. Hicke L. (2001) Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2: 195-201
39. Gieffers C., Peters B. H., Kramer E. R., Dotti C. G. and Peters J. M. (1999) Expression of the CDH1-associated form of the anaphase-promoting complex in postmitotic neurons. Proc. Natl. Acad. Sci. USA 96: 11317-11322
40. Wan Y. and Kirschner M. W. (2001) Identification of multiple CDH1 homologues invertebrates conferring different substrate specificities. Proc. Natl. Acad. Sci. USA 98: 13066-13071
41. Konishi Y., Stegmuller J., Matsuda T., Bonni A. and Bonni A. (2004) Cdh1-APC controls axonal growth and patterning in mammalian brain. Science 303: 1026-1030
42. King R. W., Glotzer M. and Kirschner M. W. (1996) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7: 1343-1357
43. Pfleger C. M. and Kirschner M. W. (2000) The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14: 655-665
44. Serra-Pages C., Medley Q. G., Tang M., Hart A. and Streuli M. (1998) Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J. Biol. Chem. 273: 15611-15620
45. Krueger N. X., Van Vactor D., Wan H. I., Gelbart W. M., Goodman C. S. and Saito H. (1996) The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84: 611-622
46. Sun Q., Schindelholz B., Knirr M., Schmid A. and Zinn K. (2001) Complex genetic interactions among four receptor tyrosine phosphatases regulate axon guidance in Drosophila. Mol. Cell Neurosci. 17: 274-291
47. Kaufmann N., DeProto J., Ranjan R., Wan H. and Van Vactor D. (2002) Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34: 27-38
48. Zhen M. and Jin Y. (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401: 371-375
49. Ko J., Na M., Kim S., Lee J. R. and Kim E. (2003) Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J. Biol. Chem. 278: 42377-42385
50. Shin H., Wyszynski M., Huh K. H., Valtschanoff J. G., Lee J. R., Ko J. et al. (2003) Association of the kinesin motor KIF1A with the multimodular protein liprin-alpha. J. Biol. Chem. 278: 11393-11401
51. Wyszynski M., Kim E., Dunah A. W., Passafaro M., Valtschanoff J. G., Serra-Pages C. et al. (2002) Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron 34: 39-52
52. Ko J., Kim S., Valtschanoff J. G., Shin H., Lee J. R., Sheng M. et al. (2003) Interaction between liprin-alpha and GIT1 is required for AMPA receptor targeting. J. Neurosci. 23: 1667-1677
53. Kim S., Ko J., Shin H., Lee J. R., Lim C., Han J. H. et al. (2003) The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J. Biol. Chem. 278: 6291-6300
54. Wills Z., Bateman J., Korey C. A., Comer A. and Van Vactor D. (1999) The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22: 301-312
55. Lanier L. M. and Gertler F. B (2000) From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr. Opin. Neurobiol. 10: 80-87
56. Bateman J., Shu H. and Van Vactor D. (2000) The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 26: 93-106
57. Lin M. Z. and Greenberg M. E. (2000) Orchestral maneuvers in the axon: Trio and the control of axon guidance. Cell 101: 239-242
58. Debant A., Serra-Pages C., Seipel K., O'Brien S., Tang M., Park S. H. et al. (1996) The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain and has separate Rac-specific and Rho-specific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. USA 93: 5466-5471
59. Zukerberg L. R., Patrick G. N., Nikolic M., Humbert S., Wu C. L., Lanier L. M. et al. (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation and neurite outgrowth. Neuron 26: 633-646
60. Yeo T. T., Yang T., Massa S. M., Zhang J. S., Honkaniemi J., Butcher L. L. et al. (1997) Deficient LAR expression decreases basal forebrain cholinergic neuronal size and hippocampal cholinergic innervation. J. Neurosci Res. 47: 348-360
61. Van Lieshout E. M., Van der Heijden I., Hendriks W. J. and Van der Zee C. E. (2001) A decrease in size and number of basal forebrain cholinergic neurons is paralleled by diminished hippocampal cholinergic innervation in mice lacking leukocyte common antigen-related protein tyrosine phosphatase activity. Neuroscience 102: 833-841
62. Elchebly M., Wagner J., Kennedy T. E., Lanctot C., Michaliszyn E., Itie A. et al. (1999) Neuroendocrine dysplasia in mice lacking protein tyrosine phosphatase sigma. Nat. Genet. 21: 330-333
63. Wallace M. J., Batt J., Fladd C. A., Henderson J. T., Skarnes W. and Rotin D. (1999) Neuronal defects and posterior pituitary hypoplasia in mice lacking the receptor tyrosine phosphatase PTPsigma. Nat. Genet. 21: 334-338
64. Meathrel K., Adamek T., Batt J., Rotin D. and Doering L. C. (2002) Protein tyrosine phosphatase sigma-deficient mice show aberrant cytoarchitecture and structural abnormalities in the central nervous system. J. Neurosci Res. 70: 24-35
65. Xie Y., Yeo T. T., Zhang C., Yang T., Tisi M. A., Massa S. M. et al. (2001) The leukocyte common antigen-related protein tyrosine phosphatase receptor regulates regenerative neurite outgrowth in vivo. J. Neurosci. 21: 5130-5138
66. Van der Zee C. E., Man T. Y., Van Lieshout E. M., Van der Heijden I., Van Bree M. and Hendriks W. J. (2003) Delayed peripheral nerve regeneration and central nervous system collateral sprouting in leucocyte common antigen-related protein tyrosine phosphatase-deficient mice. Eur. J. Neurosci. 17: 991-1005
67. McLean J., Batt J., Doering L. C., Rotin D. and Bain J. R. (2002) Enhanced rate of nerve regeneration and directional errors after sciatic nerve injury in receptor protein tyrosine phosphatase sigma knock-out mice. J. Neurosci. 22: 5481-5491
68. Goldberg J. L. and Barres B. A. (2000) The relationship between neuronal survival and regeneration. Annu. Rev. Neurosci. 23: 579-612
69. Filbrin M. T. (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4: 1-11
70. He Z. and Koprivica V. (2004) The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27: 341-368
71. Bradbury E. J., Moon L. D., Popat R. J., King V. R., Bennett G. S., Patel P. N. et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640
72. Cai D., Deng K., Mellado W., Lee J., Ratan R. R. and Filbin M. T. (2002) Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35: 711-719