N-cadherin is an in vivo substrate for protein tyrosine phosphatase sigma (PTPσ) and participates in PTPσ-mediated inhibition of axon growth

Molecular and Cellular Biology

Volumn 27, Issue 1, 2007, Pages 208-219

  Siu, Roberta ^a   Fladd, Chris ^a   Rotin, Daniela ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALCIUM; LAMININ; NERVE CELL ADHESION MOLECULE; PEPTIDE; PROTEIN; PROTEIN LAR; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SIGMA; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LYSATE; CONTROLLED STUDY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VIVO STUDY; KNOCKOUT MOUSE; MASS SPECTROMETRY; MOUSE; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SPINAL GANGLION; SUBSTRATE TRAPPING;

ANIMALS; AXONS; BRAIN; CADHERINS; CERCOPITHECUS AETHIOPS; COS CELLS; GANGLIA, SPINAL; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; PROTEIN BINDING; PROTEIN-TYROSINE-PHOSPHATASE; RATS; SCHWANN CELLS; SUBSTRATE SPECIFICITY;

ANIMALIA;

EID: 33845763350     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00707-06     Document Type: Article

References (84)

1. Aberle, H., S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:3655-3663.
2. Aberle, H., H. Schwartz, and R. Kemler. 1996. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell. Biochem. 61:514-523.
3. Alonso, A., J. Sasin, N. Bottini, I. Friedberg, A. Osterman, A. Godzik, T. Hunter, J. Dixon, and T. Mustelin. 2004. Protein tyrosine phosphatases in the human genome. Cell 117:699-711.
4. Andersen, J. N., P. G. Jansen, S. M. Echwald, O. H. Mortensen, T. Fukada, R. Del Vecchio, N. K. Tonks, and N. P. Moller. 2004. A genomic perspective on protein tyrosine phosphatases: gene structure, pseudogenes, and genetic disease linkage. FASEB J. 18:8-30.
5. Arregui, C., P. Pathre, J. Lilien, and J. Balsamo. 2000. The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J. Cell Biol. 149:1263-1274.
6. Baker, M. W., and E. R. Macagno. 2000. RNAi of the receptor tyrosine phosphatase HmLAR2 in a single cell of an intact leech embryo leads to growth-cone collapse. Curr. Biol. 10:1071-1074.
7. Balsamo, J., H. Ernst, M. K. Zanin, S. Hoffman, and J. Lilien. 1995. The interaction of the retina cell surface N-acetylgalactosaminylphosphotransferase with an endogenous proteoglycan ligand results in inhibition of cadherin-mediated adhesion. J. Cell Biol. 129:1391-1401.
8. Batt, J., S. Asa, C. Fladd, and D. Rotin. 2002. Pituitary, pancreatic and gut neuroendocrine defects in protein tyrosine phosphatase-sigma-deficient mice. Mol. Endocrinol. 16:155-169.
9. 2+ influx and neurite growth in response to purified N-cadherin and laminin. J. Cell Biol. 127:1461-1475.
10. Brady-Kalnay, S. M., T. Mourton, J. P. Nixon, G. E. Pietz, M. Kinch, H. Chen, R. Brackenbury, D. L. Rimm, R. L. Del Vecchio, and N. K. Tonks. 1998. Dynamic interaction of PTPmu with multiple cadherins in vivo. J. Cell Biol. 141:287-296.
11. Brady-Kalnay, S. M., D. L. Rimm, and N. K. Tonks. 1995. Receptor protein tyrosine phosphatase PTPmu associates with cadherins and catenins in vivo. J. Cell Biol. 130:977-986.
12. Burden-Gulley, S. M., and S. M. Brady-Kalnay. 1999. PTPmu regulates N-cadherin-dependent neurite outgrowth. J. Cell Biol. 144:1323-1336.
13. Chagnon, M. J., N. Uetani, and M. L. Tremblay. 2004. Functional significance of the LAR receptor protein tyrosine phosphatase family in development and diseases. Biochem. Cell Biol. 82:664-675.
14. Clandinin, T. R., C. H. Lee, T. Herman, R. C. Lee, A. Y. Yang, S. Ovasapyan, and S. L. Zipursky. 2001. Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32:237-248.
15. Conacci-Sorrell, M., J. Zhurinsky, and A. Ben-Ze'ev. 2002. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Investig. 109:987-991.
16. Debant, A., C. Serra-Pages, K. Seipel, S. O'Brien, M. Tang, S. H. Park, and M. Streuli. 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.
17. Desai, C., and J. Purdy. 2003. The neural receptor protein tyrosine phosphatase DPTP69D is required during periods of axon outgrowth in Drosophila. Genetics 164:575-588.
18. Desai, C. J., J. G. Gindhart, Jr., L. S. Goldstein, and K. Zinn. 1996. Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84:599-609.
19. Desai, C. J., N. X. Krueger, H. Saito, and K. Zinn. 1997. Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila. Development 124:1941-1952.
20. Dunah, A. W., E. Hueske, M. Wyszynski, C. C. Hoogenraad, J. Jaworski, D. T. Pak, A. Simonetta, G. Liu, and M. Sheng. 2005. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat. Neurosci. 8:458-467.
21. Elchebly, M., J. Wagner, T. E. Kennedy, C. Lanctot, E. Michaliszyn, A. Itie, J. Drouin, and M. L. Tremblay. 1999. Neuroendocrine dysplasia in mice lacking protein tyrosine phosphatase sigma. Nat. Genet. 21:330-333.
22. Ensslen-Craig, S. E., and S. M. Brady-Kalnay. 2004. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev. Biol. 275:12-22.
23. Figeys, D., L. D. McBroom, and M. F. Moran. 2001. Mass spectrometry for the study of protein-protein interactions. Methods 24:230-239.
24. Flint, A. J., T. Tiganis, D. Barford, and N. K. Tonks. 1997. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 94:1680-1685.
25. Fuchs, M., T. Muller, M. M. Lerch, and A. Ullrich. 1996. Association of human protein-tyrosine phosphatase kappa with members of the armadillo family. J. Biol. Chem. 271:16712-16719.
26. Gershon, T. R., M. W. Baker, M. Nitabach, and E. R. Macagno. 1998. The leech receptor protein tyrosine phosphatase HmLAR2 is concentrated in growth cones and is involved in process outgrowth. Development 125:1183-1190.
27. Johnson, K. G., and C. E. Holt. 2000. Expression of CRYP-alpha, LAR, PTP-delta, and PTP-rho in the developing Xenopus visual system. Mech. Dev. 92:291-294.
28. Kaufmann, N., J. DeProto, R. Ranjan, H. Wan, and D. Van Vactor. 2002. Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34:27-38.
29. Kim, H., H. Yeger, R. Han, M. Wallace, B. Goldstein, and D. Rotin. 1996. Expression of LAR-PTP2 in rat lung is confined to proliferating epithelia lining the airways and air sacs. Am. J. Physiol. 270:L566-L576.
30. Krueger, N. X., D. Van Vactor, H. I. Wan, W. M. Gelbart, C. S. Goodman, and H. Saito. 1996. The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84:611-622.
31. Ledig, M. M., F. Haj, J. L. Bixby, A. W. Stoker, and B. K. Mueller. 1999. The receptor tyrosine phosphatase CRYPalpha promotes intraretinal axon growth. J. Cell Biol. 147:375-388.
32. Letourneau, P. C., F. K. Roche, T. A. Shattuck, V. Lemmon, and M. Takeichi. 1991. Interactions of Schwann cells with neurites and with other Schwann cells involve the calcium-dependent adhesion molecule, N-cadherin. J. Neurobiol. 22:707-720.
33. Lilien, J., C. Arregui, H. Li, and J. Balsamo. 1999. The juxtamembrane domain of cadherin regulates integrin-mediated adhesion and neurite outgrowth. J. Neurosci. Res. 58:727-734.
34. Maurel-Zaffran, C., T. Suzuki, G. Gahmon, J. E. Treisman, and B. J. Dickson. 2001. Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32:225-235.
35. McLean, J., J. Batt, L. C. Doering, D. Rotin, and J. R. Bain. 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.
36. Meathrel, K., T. Adamek, J. Batt, D. Rotin, and L. C. Doering. 2002. Protein tyrosine phosphatase sigma-deficient mice show aberrant cytoarchitecture and structural abnormalities in the central nervous system. J. Neurosci. Res. 70:24-35.
37. Meng, K., A. Rodriguez-Pena, T. Dimitrov, W. Chen, M. Yamin, M. Noda, and T. F. Deuel. 2000. Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc. Natl. Acad. Sci. USA 97:2603-2608.
38. Mueller, B. K., M. M. Ledig, and S. Wahl. 2000. The receptor tyrosine phosphatase CRYPalpha affects growth cone morphology. J. Neurobiol. 44:204-218.
39. Muller, T., A. Choidas, E. Reichmann, and A. Ullrich. 1999. Phosphorylation and free pool of beta-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J. Biol. Chem. 274:10173-10183.
40. Newsome, T. P., S. Schmidt, G. Dietzl, K. Keleman, B. Asling, A. Debant, and B. J. Dickson. 2000. Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101:283-294.
41. O'Grady, P., T. C. Thai, and H. Saito. 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.
42. Pan, M. G., C. Rim, K. P. Lu, T. Florio, and P. J. Stork. 1993. Cloning and expression of two structurally distinct receptor-linked protein-tyrosine phosphatases generated by RNA processing from a single gene. J. Biol. Chem. 268:19284-19291.
43. Pathre, P., C. Arregui, T. Wampler, I. Kue, T. C. Leung, J. Lilien, and J. Balsamo. 2001. PTP1B regulates neurite extension mediated by cell-cell and cell-matrix adhesion molecules. J. Neurosci. Res. 63:143-150.
44. Perron, J. C., and J. L. Bixby. 1999. Distinct neurite outgrowth signaling pathways converge on ERK activation. Mol. Cell. Neurosci. 13:362-378.
45. Piedra, J., D. Martinez, J. Castano, S. Miravet, M. Dunach, and A. G. de Herreros. 2001. Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J. Biol. Chem. 276:20436-20443.
46. Pulido, R., C. Serra-Pages, M. Tang, and M. Streuli. 1995. The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosine-phosphatases: multiple human LAR, FTP delta, and FTP 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.
47. Rashid-Doubell, F., I. McKinnell, A. R. Aricescu, G. Sajnani, and A. Stoker. 2002. Chick PTPsigma regulates the targeting of retinal axons within the optic tectum. J. Neurosci. 22:5024-5033.
48. Retta, S. F., F. Balzac, and M. Avolio. 2006. Rap1: a turnabout for the crosstalk between cadherins and integrins. Eur. J. Cell Biol. 85:283-293.
49. Rhee, J., N. S. Mahfooz, C. Arregui, J. Lilien, J. Balsamo, and M. F. VanBerkum. 2002. Activation of the repulsive receptor Roundabout inhibits N-cadherin-mediated cell adhesion. Nat. Cell Biol. 4:798-805.
50. Roura, S., S. Miravet, J. Piedra, A. Garcia de Herreros, and M. Dunach. 1999. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J. Biol. Chem. 274:36734-36740.
51. Sahin, M., J. J. Dowling, and S. Hockfield. 1995. Seven protein tyrosine phosphatases are differentially expressed in the developing rat brain. J. Comp. Neurol. 351:617-631.
52. Sahin, M., and S. Hockfield. 1993. Protein tyrosine phosphatases expressed in the developing rat brain. J. Neurosci. 13:4968-4978.
53. Sapieha, P. S., L. Duplan, N. Uetani, S. Joly, M. L. Tremblay, T. E. Kennedy, and A. Di Polo. 2005. Receptor protein tyrosine phosphatase sigma inhibits axon regrowth in the adult injured CNS. Mol. Cell. Neurosci. 28:625-635.
54. Serra-Pages, C., N. L. Kedersha, L. Fazikas, Q. Medley, A. Debant, and M. Streuli. 1995. The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR-interacting protein co-localize at focal adhesions. EMBO J. 14:2827-2838.
55. Serra-Pages, C., Q. G. Medley, M. Tang, A. Hart, and M. Streuli. 1998. Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J. Biol. Chem. 273:15611-15620.
56. Shapiro, L., A. M. Fannon, P. D. Kwong, A. Thompson, M. S. Lehmann, G. Grubel, J. F. Legrand, J. Als-Nielsen, D. R. Colman, and W. A. Hendrickson. 1995. Structural basis of cell-cell adhesion by cadherins. Nature 374:327-337.
57. Shibuya, Y., J. Takeuchi, M. Kobayashi, M. Murata, S. Munemoto, S. Yokoo, M. Umeda, and T. Komori. 2005. N-/R-cadherin expression in dorsal root ganglia and spinal cord. Kobe J. Med. Sci. 51:35-40.
58. Stoker, A. W. 1994. Isoforms of a novel cell adhesion molecule-like protein tyrosine phosphatase are implicated in neural development. Mech. Dev. 46:201-217.
59. Stoker, A. W. 2001. Receptor tyrosine phosphatases in axon growth and guidance. Curr. Opin. Neurobiol. 11:95-102.
60. Stoker, A. W., B. Gehrig, F. Haj, and B. H. Bay. 1995. Axonal localisation of the CAM-like tyrosine phosphatase CRYP alpha: a signalling molecule of embryonic growth cones. Development 121:1833-1844.
61. Streuli, M., N. X. Krueger, L. R. Hall, S. F. Schlossman, and H. Saito. 1988. A new member of the immunoglobulin superfamily that has a cytoplasmic region homologous to the leukocyte common antigen. J. Exp. Med. 168:1523-1530.
62. Streuli, M., N. X. Krueger, A. Y. Tsai, and H. Saito. 1989. A family of receptor-linked protein tyrosine phosphatases in humans and Drosophila. Proc. Natl. Acad. Sci. USA 86:8698-8702.
63. Sun, Q. L., J. Wang, R. J. Bookman, and J. L. Bixby. 2000. Growth cone steering by receptor tyrosine phosphatase delta defines a distinct class of guidance cue. Mol. Cell. Neurosci. 16:686-695.
64. Tamura, K., W. S. Shan, W. A. Hendrickson, D. R. Colman, and L. Shapiro. 1998. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20:1153-1163.
65. Thompson, K. M., N. Uetani, C. Manitt, M. Elchebly, M. L. Tremblay, and T. E. Kennedy. 2003. Receptor protein tyrosine phosphatase sigma inhibits axonal regeneration and the rate of axon extension. Mol. Cell. Neurosci. 23:681-692.
66. Tomaselli, K. J., P. Doherty, C. J. Emmett, C. H. Damsky, F. S. Walsh, and L. F. Reichardt. 1993. Expression of beta 1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J. Neurosci. 13:4880-4888.
67. Utton, M. A., B. Eickholt, F. V. Howell, J. Wallis, and P. Doherty. 2001. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J. Neurochem. 76:1421-1430.
68. Wagner, J., D. Boerboom, and M. L. Tremblay. 1994. Molecular cloning and tissue-specific RNA processing of a murine receptor-type protein tyrosine phosphatase. Eur. J. Biochem. 226:773-782.
69. Wallace, M. J., J. Batt, C. A. Fladd, J. T. Henderson, W. Skarnes, and D. Rotin. 1999. Neuronal defects and posterior pituitary hypoplasia in mice lacking the receptor tyrosine phosphatase PTPsigma. Nat. Genet. 21:334-338.
70. Wallace, M. J., C. Fladd, J. Batt, and D. Rotin. 1998. The second catalytic domain of protein tyrosine phosphatase delta (PTP delta) binds to and inhibits the first catalytic domain of PTP sigma. Mol. Cell. Biol. 18:2608-2616.
71. Walton, K. M., K. J. Martell, S. P. Kwak, J. E. Dixon, and B. L. Largent. 1993. A novel receptor-type protein tyrosine phosphatase is expressed during neurogenesis in the olfactory neuroepithelium. Neuron 11:387-400.
72. Wang, H., H. Yan, P. D. Canoll, O. Silvennoinen, J. Schlessinger, and J. M. Musacchio. 1995. Expression of receptor protein tyrosine phosphatase-sigma (RPTP-sigma) in the nervous system of the developing and adult rat. J. Neurosci. Res. 41:297-310.
73. Wang, J., and J. L. Bixby. 1999. Receptor tyrosine phosphatase-delta is a homophilic, neurite-promoting cell adhesion molecular for CNS neurons. Mol. Cell. Neurosci. 14:370-384.
74. Wanner, I. B., and P. M. Wood. 2002. N-cadherin mediates axon-aligned process growth and cell-cell interaction in rat Schwann cells. J. Neurosci. 22:4066-4079.
75. Williams, E., G. Williams, B. J. Gour, O. W. Blaschuk, and P. Doherty. 2000. A novel family of cyclic peptide antagonists suggests that N-cadherin specificity is determined by amino acids that flank the HAV motif. J. Biol. Chem. 275:4007-4012.
76. Williams, E. J., G. Williams, B. Gour, O. Blaschuk, and P. Doherty. 2000. INP, a novel N-cadherin antagonist targeted to the amino acids that flank the HAV motif. Mol. Cell. Neurosci. 15:456-464.
77. Williams, G., E. J. Williams, and P. Doherty. 2002. Dimeric versions of two short N-cadherin binding motifs (HAVDI and INPISG) function as N-cadherin agonists. J. Biol. Chem. 277:4361-4367.
78. Wills, Z., J. Bateman, C. A. Korey, A. Comer, and D. Van Vactor. 1999. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22:301-312.
79. Wu, D. Y., and D. J. Goldberg. 1993. Regulated tyrosine phosphorylation at the tips of growth cone filopodia. J. Cell Biol. 123:653-664.
80. Wu, D. Y., L. C. Wang, C. A. Mason, and D. J. Goldberg. 1996. Association of beta 1 integrin with phosphotyrosine in growth cone filopodia. J. Neurosci. 16:1470-1478.
81. Yan, H., A. Grossman, H. Wang, P. D'Eustachio, K. Mossie, J. M. Musacchio, O. Silvennoinen, and J. Schlessinger. 1993. A novel receptor tyrosine phosphatase-sigma that is highly expressed in the nervous system. J. Biol. Chem. 268:24880-24886.
82. Yang, T., R. Bernabeu, Y. Xie, J. S. Zhang, S. M. Massa, H. C. Rempel, and F. M. Longo. 2003. Leukocyte antigen-related protein tyrosine phosphatase receptor: a small ectodomain isoform functions as a homophilic ligand and promotes neurite outgrowth. J. Neurosci. 23:3353-3363.
83. Yang, T., W. Yin, V. D. Derevyanny, L. A. Moore, and F. M. Longo. 2005. Identification of an ectodomain within the LAR protein tyrosine phosphatase receptor that binds homophilically and activates signalling pathways promoting neurite outgrowth. Eur. J. Neurosci. 22:2159-2170.
84. Zhang, W. R., N. Hashimoto, F. Ahmad, W. Ding, and B. J. Goldstein. 1994. Molecular cloning and expression of a unique receptor-like protein-tyrosine- phosphatase in the leucocyte-common-antigen-related phosphate family. Biochem. J. 302:39-47.