Dimerization of Protein Tyrosine Phosphatase σ Governs both Ligand Binding and Isoform Specificity

REFERENCES

• Aicher, B., M. M. Lerch, T. Muller, J. Schilling, and A. Ullrich. 1997. Cellular redistribution of protein tyrosine phosphatases LAR and PTPσ by inducible proteolytic processing. J. Cell Biol. 138:681–696.
   PubMed Web of Science ®Google Scholar
• Alete, D. E., M. E. Weeks, A. G. Hovanession, M. Hawadle, and A. W. Stoker. 2006. Cell surface nucleolin on developing muscle is a potential ligand for the axonal receptor protein tyrosine phosphatase-sigma. FEBS J. 273:4668–4681.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Aricescu, A. R., W. C. Hon, C. Siebold, W. Lu, P. A. van der Merwe, and E. Y. Jones. 2006. Molecular analysis of receptor protein tyrosine phosphatase mu-mediated cell adhesion. EMBO J. 25:701–712.
   PubMedGoogle Scholar
• Aricescu, A. R., I. W. McKinnell, W. Halfter, and A. W. Stoker. 2002. Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol. Cell. Biol. 22:1881–1892.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Beltran, P. J., and J. L. Bixby. 2003. Receptor protein tyrosine phosphatases as mediators of cellular adhesion. Front Biosci. 8:D87–D99.
   PubMed Web of Science ®Google Scholar
• Bilwes, A. M., J. Den Hertog, T. Hunter, and J. P. Noel. 1996. Structural basis for inhibition of receptor protein-tyrosine phosphatase-alpha by dimerization. Nature 382:555–559.
   PubMed Web of Science ®Google Scholar
• Chang, C., T. W. Yu, C. I. Bargmann, and M. Tessier-Lavigne. 2004. Inhibition of netrin-mediated axon attraction by a receptor protein tyrosine phosphatase. Science 305:103–106.
   PubMedGoogle Scholar
• Cheng, H. J., and J. G. Flanagan. 1994. Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 79:157–168.
   PubMed Web of Science ®Google Scholar
• Chin, C. N., J. N. Sachs, and D. M. Engelman. 2005. Transmembrane homodimerization of receptor-like protein tyrosine phosphatases. FEBS Lett. 579:3855–3858.
   PubMed Web of Science ®Google Scholar
• Cismasiu, V. B., S. A. Denes, H. Reilander, H. Michel, and S. E. Szedlacsek. 2004. The MAM (Meprin/A5-protein/PTPmu) domain is a homophilic binding site promoting the lateral dimerization of receptor-like protein-tyrosine phosphatase micro. J. Biol. Chem. 279:26922–26931.
   PubMedGoogle Scholar
• den Hertog, J., A. Groen, and T. van der Wijk. 2005. Redox regulation of protein-tyrosine phosphatases. Arch. Biochem. Biophys. 434:11–15.
   PubMed Web of Science ®Google Scholar
• den Hertog, J., T. van der Wijk, L. G. Tertoolen, and C. Blanchetot. 2003. Receptor protein-tyrosine phosphatase dimerization. Methods Enzymol. 366:224–240.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ferguson, K. M. 2004. Active and inactive conformations of the epidermal growth factor receptor. Biochem. Soc. Trans. 32:742–745.
   PubMed Web of Science ®Google Scholar
• Fernandez-Patron, C., L. Castellanos-Serra, and P. Rodriguez. 1992. Reverse staining of sodium dodecyl sulfate polyacrylamide gels by imidazole-zinc salts: sensitive detection of unmodified proteins. BioTechniques 12:564–573.
   PubMed Web of Science ®Google Scholar
• Fox, A. N., and K. Zinn. 2005. The heparan sulfate proteoglycan syndecan is an in vivo ligand for the Drosophila LAR receptor tyrosine phosphatase. Curr. Biol. 15:1701–1711.
   PubMed Web of Science ®Google Scholar
• Haj, F., I. McKinnell, and A. Stoker. 1999. Retinotectal ligands for the receptor tyrosine phosphatase CRYPα. Mol. Cell Neurosci. 14:225–240.
   PubMedGoogle Scholar
• Hibi, M., and T. Hirano. 1998. Signal transduction through cytokine receptors. Int. Rev. Immunol. 17:75–102.
   PubMedGoogle Scholar
• Hoylaerts, M. F., T. Manes, and J. L. Millan. 1997. Mammalian alkaline phosphatases are allosteric enzymes. J. Biol. Chem. 272:22781–22787.
   PubMed Web of Science ®Google Scholar
• Jiang, G., J. den Hertog, and T. Hunter. 2000. Receptor-like protein tyrosine phosphatase alpha homodimerizes on the cell surface. Mol. Cell. Biol. 20:5917–5929.
   PubMedGoogle Scholar
• Jiang, G., J. den Hertog, J. Su, J. Noel, J. Sap, and T. Hunter. 1999. Dimerization inhibits the activity of receptor-like protein-tyrosine phosphatase-alpha. Nature 401:606–610.
   PubMedGoogle Scholar
• Johnson, K. G., A. P. Tenney, A. Ghose, A. M. Duckworth, M. E. Higashi, K. Parfitt, O. Marcu, T. R. Heslip, J. L. Marsh, T. L. Schwarz, J. G. Flanagan, and D. Van Vactor. 2006. The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49:517–531.
   PubMed Web of Science ®Google Scholar
• Johnson, K. G., and D. Van Vactor. 2003. Receptor protein tyrosine phosphatases in nervous system development. Physiol. Rev. 83:1–24.
   PubMedGoogle Scholar
• Krasnoperov, V., M. A. Bittner, W. Mo, L. Buryanovsky, T. A. Neubert, R. W. Holz, K. Ichtchenko, and A. G. Petrenko. 2002. Protein-tyrosine phosphatase-sigma is a novel member of the functional family of alpha-latrotoxin receptors. J. Biol. Chem. 277:35887–35895.
   PubMedGoogle Scholar
• Leahy, D. J., I. Aukhil, and H. P. Erickson. 1996. 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell 84:155–164.
   PubMed Web of Science ®Google Scholar
• Majeti, R., A. M. Bilwes, J. P. Noel, T. Hunter, and A. Weiss. 1998. Dimerization-induced inhibition of receptor protein tyrosine phosphatase function through an inhibitory wedge. Science 279:88–91.
   PubMed Web of Science ®Google Scholar
• Majeti, R., and A. Weiss. 2001. Regulatory mechanisms for receptor protein tyrosine phosphatases. Chem. Rev. 101:2441–2448.
   PubMedGoogle Scholar
• Majeti, R., Z. Xu, T. G. Parslow, J. L. Olson, D. I. Daikh, N. Killeen, and A. Weiss. 2000. An inactivating point mutation in the inhibitory wedge of CD45 causes lymphoproliferation and autoimmunity. Cell 103:1059–1070.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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-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.
   PubMed Web of Science ®Google Scholar
• Nam, H. J., F. Poy, H. Saito, and C. A. Frederick. 2005. Structural basis for the function and regulation of the receptor protein tyrosine phosphatase CD45. J. Exp. Med. 201:441–452.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Ostman, A., and F. D. Bohmer. 2001. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatases. Trends Cell Biol. 11:258–266.
   PubMedGoogle Scholar
• Ottensmeyer, F. P., D. R. Beniac, R. Z. Luo, and C. C. Yip. 2000. Mechanism of transmembrane signaling: insulin binding and the insulin receptor. Biochemistry 39:12103–12112.
   PubMed Web of Science ®Google Scholar
• Pariser, H., P. Perez-Pinera, L. Ezquerra, G. Herradon, and T. F. Deuel. 2005. Pleiotrophin stimulates tyrosine phosphorylation of beta-adducin through inactivation of the transmembrane receptor protein tyrosine phosphatase beta/zeta. Biochem. Biophys. Res. Commun. 335:232–239.
   PubMed Web of Science ®Google Scholar
• Paul, S., and P. J. Lombroso. 2003. Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol. Life Sci. 60:2465–2482.
   PubMedGoogle Scholar
• Pulido, R., N. X. Krueger, C. Serra Pages, H. Saito, and M. Streuli. 1995. Molecular characterization of the human transmembrane protein-tyrosine phosphatase delta. Evidence for tissue-specific expression of alternative human transmembrane protein-tyrosine phosphatase delta isoforms. J. Biol. Chem. 270:6722–6728.
   PubMed Web of Science ®Google Scholar
• Rashid-Doubell, F., I McKinnell, A. R. Aricescu, G. Sajnani, and A. W. Stoker. 2002. Chick PTPσ regulates the targeting of retinal axons within the optic tectum. J. Neurosci. 22:5024–5033.
   PubMedGoogle Scholar
• Remy, I., I. A. Wilson, and S. W. Michnick. 1999. Erythropoietin receptor activation by a ligand-induced conformation change. Science 283:990–993.
   PubMed Web of Science ®Google Scholar
• Sajnani, G., A. R. Aricescu, E. Y. Jones, J. Gallagher, D. Alete, and A. Stoker. 2005. PTPσ promotes retinal neurite outgrowth non-cell-autonomously. J. Neurobiol. 65:59–71.
   PubMedGoogle Scholar
• Sajnani-Perez, G., J. K. Chilton, A. R. Aricescu, F. Haj, and A. W. Stoker. 2003. Isoform-specific binding of the tyrosine phosphatase PTPσ to a ligand in developing muscle. Mol. Cell Neurosci. 22:37–48.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• SerraPages, C., H. Saito, and M. Streuli. 1994. Mutational analysis of proprotein processing, subunit association, and shedding of the LAR transmembrane protein tyrosine phosphatase. J. Biol. Chem. 269:23632–23641.
   PubMed Web of Science ®Google Scholar
• Shiang, R., L. M. Thompson, Y. Z. Zhu, D. M. Church, T. J. Fielder, M. Bocian, S. T. Winokur, and J. J. Wasmuth. 1994. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell 78:335–342.
   PubMed Web of Science ®Google Scholar
• Stepanek, L., A. W. Stoker, E. Stoeckli, and J. L. Bixby. 2005. Receptor tyrosine phosphatases guide vertebrate motor axons during development. J. Neurosci. 25:3813–3823.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Stoker, A. W. 2005. Protein tyrosine phosphatases and signalling. J. Endocrinol. 185:19–33.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Stoker, A. W., B. Gehrig, M. R. Newton, and B. H. Bay. 1995. Comparative localisation of CRYP-alpha, a CAM-like tyrosine phosphatase, and NgCAM in the developing chick visual system. Dev. Brain Res. 90:129–140.
   PubMedGoogle Scholar
• Takeda, A., A. Matsuda, R. M. Paul, and N. R. Yaseen. 2004. CD45-associated protein inhibits CD45 dimerization and upregulates its protein tyrosine phosphatase activity. Blood 103:3440–3447.
   PubMedGoogle Scholar
• Tertoolen, L. G., C. Blanchetot, G. Jiang, J. Overvoorde, T. W. Gadella, Jr., T. Hunter, and J. den Hertog. 2001. Dimerization of receptor protein-tyrosine phosphatase alpha in living cells. BMC Cell Biol 2:8.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• van der Wijk, T., C. Blanchetot, J. Overvoorde, and J. den Hertog. 2003. Redox-regulated rotational coupling of receptor protein-tyrosine phosphatase alpha dimers. J. Biol. Chem. 278:13968–13974.
   PubMedGoogle Scholar
• van der Wijk, T., J. Overvoorde, and J. den Hertog. 2004. H2O2-induced intermolecular disulfide bond formation between receptor protein-tyrosine phosphatases. J. Biol. Chem. 279:44355–44361.
   PubMed Web of Science ®Google Scholar
• Walchli, S., X. Espanel, and R. H. van Huijsduijnen. 2005. Sap-1/PTPRH activity is regulated by reversible dimerization. Biochem. Biophys. Res. Commun. 331:497–502.
   PubMedGoogle Scholar
• 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 PTPσ. Nat. Genet. 21:334–338.
   PubMedGoogle Scholar
• Weiner, D. B., J. Liu, J. A. Cohen, W. V. Williams, and M. I. Greene. 1989. A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature 339:230–231.
   PubMed Web of Science ®Google Scholar
• West, M., and V. G. Wilson. 2002. Method for transferring mutations between plasmids. BioTechniques 32:44, 46.
   PubMedGoogle Scholar
• Westermark, B., L. Claesson-Welsh, and C. H. Heldin. 1989. Structural and functional aspects of the receptors for platelet-derived growth factor. Prog. Growth Factor Res. 1:253–266.
   PubMedGoogle Scholar
• Xu, Z., and A. Weiss. 2002. Negative regulation of CD45 by differential homodimerization of the alternatively spliced isoforms. Nat. Immunol. 3:764–771.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Zhang, J. S., and F. M. Longo. 1995. LAR tyrosine phosphatase receptor: alternative splicing is preferential to the nervous system, coordinated with cell growth and generates novel isoforms containing extensive CAG repeats. J. Cell Biol. 128:415–431.
   PubMedGoogle Scholar