The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation

Journal of Neuroscience

Volumn 25, Issue 33, 2005, Pages 7517-7528

  Ackley, Brian D ^a,b   Harrington, Robert J ^a   Hudson, Martin L ^a   Williams, Lisa ^c   Kenyon, Cynthia J ^c   Chisholm, Andrew D ^a   Jin, Yishi ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

liprin; Axon guidance; Cell adhesion; LAR receptor tyrosine phosphatase; Nidogen; syd 2; Synaptogenesis

Indexed keywords

ADAPTOR PROTEIN; ALPHA LIPRIN; CD45 ANTIGEN; ISOPROTEIN; PHOSPHATASE; PROTEIN NID1; PROTEIN RIM; PROTEIN SYD2; PROTEIN TYROSINE PHOSPHATASE 3; UNCLASSIFIED DRUG;

ANTIGEN DETECTION; ARTICLE; CAENORHABDITIS ELEGANS; CELL ADHESION; EXTRACELLULAR MATRIX; GENE; GENE MUTATION; MOLECULAR BIOLOGY; NERVE FIBER; NID1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PTP 3 GENE; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PROTEIN ISOFORMS; PROTEIN-TYROSINE-PHOSPHATASE; RECEPTORS, CELL SURFACE; SYNAPSES;

EID: 23844534710     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2010-05.2005     Document Type: Article

References (47)

1. Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, Kramer JM (2001) The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J Cell Biol 152:1219-1232.
2. Ackley BD, Kang SH, Crew IR, Suh C, Jin Y, Kramer JM (2003) The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J Neurosci 23:3577-3587.
3. Altun-Gultekin Z, Andachi Y, Tsalik EL, Pilgrim D, Kohara Y, Hobert O (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128:1951-1969.
4. Aricescu AR, McKinnell IW, Halfter W, Stoker AW (2002) Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol Cell Biol 22:1881-1892.
5. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
6. Chin-Sang ID, Moseley SL, Ding M, Harrington RJ, George SE, Chisholm AD (2002) The divergent C. elegans ephrin EFN-4 functions inembryonic morphogenesis in a pathway independent of the VAB-1 Eph receptor. Development 129:5499-5510.
7. Ch'ng Q, Williams L, Lie YS, Sym M, Whangbo I, Kenyon C (2003) Identification of genes that regulate a left-right asymmetric neuronal migration in Caenorhabditis elegans. Genetics 164:1355-1367.
8. Clandinin TR, Lee CH, Herman T, Lee RC, Yang AY, Ovasapyan S, Zipursky SL (2001) Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32:237-248.
9. Debant A, Serra-Pages C, Seipel K, O'Brien S, Tang M, Park SH, Streuli M (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.
10. den Hertog J, Blanchetot C, Buist A, Overvoorde J, van der Sar A, Tertoolen LG (1999) Receptor protein-tyrosine phosphatase signalling in development. Int J Dev Biol 43:723-733.
11. Desai CJ, Gindhart Jr JG, Goldstein LS, Zinn K (1996) Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84:599-609,
12. Dong L, Chen Y, Lewis M, Hsieh JC, Reing J, Chaillet JR, Howell CY, Melhem M, Inoue S, Kuszak JR, DeGeest K, Chung AE (2002) Neurologic defects and selective disruption of basement membranes in mice lacking entactin-1/nidogen-1. Lab Invest 82:1617-1630.
13. Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8:458-467.
14. Edgley ML, Riddle DL (2001) LG II balancer chromosomes in Caenorhabditis elegans: mT1(II;III) and the mInI set of dominantly and recessively marked inversions. Mol Genet Genomics 266:385-395.
15. Ensslen-Craig SE, Brady-Kalnay SM (2004) Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev Biol 275:12-22.
16. Finney M, Ruvkun G (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895-905.
17. Gally C, Bessereau JL (2003) GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J Neurosci 23:2591-2599.
18. Garrity PA, Lee CH, Salecker I, Robertson HC, Desai CJ, Zinn K, Zipursky SL (1999) Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22:707-717.
19. Hall DH, Hedgecock EM (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837-847.
20. Hallam SJ, Jin Y (1998) lin-14 regulates the timing of synaptic remodelling in Caenorhabaitis elegans. Nature 395:78-82.
21. Harrington RJ, Gutch MJ, Hengartner MO, Tonks NK, Chisholm AD (2002) The C. elegans LAR-like receptor tyrosine phosphatase PTP-3 and the VAB-1 Eph receptor tyrosine kinase have partly redundant functions in morphogenesis. Development 129:2141-2153.
22. Honkaniemi J, Zhang JS, Yang T, Zhang C, Tisi MA, Longo FM (1998) LAR tyrosine phosphatase receptor: proximal membrane alternative splicing is coordinated with regional expression and intraneuronal localization. Brain Res Mol Brain Res 60:1-12.
23. Huang X, Cheng HJ, Tessier-Lavigne M, Jin Y (2002) MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion. Neuron 34:563-576.
24. Johnson KG, Van Vactor D (2003) Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev 83:1-24.
25. Kang SH, Kramer JM (2000) Nidogen is nonessential and not required for normal type IV collagen localization in Caenorhabditis elegans. Mol Biol Cell 11:3911-3923.
26. Kaufmann N, DeProto J, Ranjan R, Wan H, Van Vactor D (2002) Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34:27-38.
27. Kim S, Wadsworth WG (2000) Positioning of longitudinal nerves in C. elegans by nidogen. Science 288:150-154.
28. Kliemann SE, Waetge RT, Suzuki OT, Passos-Bueno MR, Rosemberg S (2003) Evidence of neuronal migration disorders in Knobloch syndrome: clinical and molecular analysis of two novel families. Am I Med Genet A 119:15-19.
29. Koushilta SP, Richmond IE, Hadwiger G, Weimer RM, Jorgensen EM, Nonet ML (2001) A post-docking role for active zone protein Rim. Nat Neurosci 4:997-1005.
30. Krueger NX, Van Vactor D, Wan HI, Gelbart WM, Goodman CS, Saito H (1996) The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84:611-622.
31. Kypta RM, Su H, Reichardt LF (1996) Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex. J Cell Biol 134:1519-1529.
32. Maurel-Zaffran C, Suzuki T, Gahmon G, Treisman JE, Dickson BJ (2001) Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32:225-235.
33. Mello CC, Kramer IM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970.
34. Nonet ML (1999) Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J Neurosci Methods 89:33-40.
35. Nonet ML, Grundahl K, Meyer BI, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305.
36. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, Horvitz HR, Jorgensen EM, Meyer BJ (1997) Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J Neurosci 17:8061-8073.
37. O'Grady P, Krueger NX, Streuli M, Saito H (1994) Genomic organization of the human LAR protein tyrosine phosphatase gene and alternative splicing in the extracellular fibronectin type-III domains. J Biol Chem 269:25193-25199.
38. O'Grady P, Thai TC, Saito H (1998) The laminin-nidogen complex is a ligand for a specific splice isoform of the transmembrane protein tyrosine phosphatase LAR. J Cell Biol 141:1675-1684.
39. Paul S, Lombroso PJ (2003) Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci 60:2465-2482.
40. PulidoR,Serra-PagesC,TangM,StreuliM (1995) The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosine-phosphatases: multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP. 1. Proc Natl Acad Sci USA 92:11686-11690.
41. Serra-Pages C, Medley QG, Tang M, Hart A, Streuli M (1998) Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J Biol Chem 273:15611-15620.
42. Stepanek L, Stoker AW, Stoeckli E, Bixby JL (2005) Receptor tyrosine phosphatases guide vertebrate motor axons during development. J Neurosci 25:3813-3823.
43. Williams L (2002) A genetic analysis of the left-right asymmetric polarizations and migrations of the Q neuroblasts in Caenorhabditis elegans. PhD thesis, University of California, San Francisco.
44. Wills Z, Bateman J, Korey CA, Comer A, 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.
45. Xie Y, Yeo TT, Zhang C, Yang T, Tisi MA, Massa SM, Longo FM (2001) The leukocyte common antigen-related protein tyrosine phosphatase receptor regulates regenerative neurite outgrowth in vivo. J Neurosci 21:5130-5138.
46. Yeh E, Kawano T, Weimer RM, Bessereau JL, Zhen M (2005) Identification of genes involved in synaptogenesis using a fluorescent active zone marker in Caenorhabditis elegans. J Neurosci 25:3833-3841.
47. Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371-375.