Receptor-type tyrosine phosphatase ligands: Looking for the needle in the haystack

FEBS Journal

Volumn 280, Issue 2, 2013, Pages 388-400

  Mohebiany, Alma N ^a   Nikolaienko, Roman M ^b   Bouyain, Samuel ^b   Harroch, Sheila ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

heterophilic interactions; homophilic interactions; ligands; phosphatases; phosphorylation; proteoglycan; receptor clustering; receptor ligand interactions; RPTP; signaling

Indexed keywords

CD45 ANTIGEN; CELL ADHESION MOLECULE; CELL ADHESION MOLECULE CONTACTIN 1; CELL ADHESION MOLECULE CONTACTIN 4; CHONDROITIN SULFATE; CONTACTIN; GALECTIN 1; GALECTIN 3; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE GAMMA; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE ZETA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ASTROCYTE; BINDING AFFINITY; CATALYSIS; CELL MIGRATION; DIMERIZATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; NEUROMUSCULAR SYNAPSE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CONTACTIN 1; HUMANS; ISOENZYMES; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5;

EID: 84872778113     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08653.x     Document Type: Review

References (112)

1. Tonks NK, Diltz CD, &, Fischer EH, (1988) Purification of the major protein-tyrosine-phosphatases of human placenta. J Biol Chem 263, 6722-6730.
2. Andersen JN, Mortensen OH, Peters GH, Drake PG, Iversen LF, Olsen OH, Jansen PG, Andersen HS, Tonks NK, &, Møller NPH, (2001) Sructural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 21, 7117-7136.
3. Johnson KG, &, Van Vactor D, (2003) Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev 83, 1-24.
4. Bilwes AM, den Hertog J, Hunter T, &, Noel JP, (1996) Structural basis for inhibition of receptor protein-tyrosine phosphatase-[alpha] by dimerization. Nature 382, 555-559.
5. Desai DM, Sap J, Schlessinger J, &, Weiss A, (1993) Ligand-mediated negative regulation of a chimeric transmembrane receptor tyrosine phosphatase. Cell 73, 541-554.
6. Hoffmann KMV, Tonks NK, &, Barford D, (1997) The crystal structure of domain 1 of receptor protein-tyrosine phosphatase μ. J Biol Chem 272, 27505-27508.
7. Nam H-J, Poy F, Krueger NX, Saito H, &, Frederick CA, (1999) Crystal structure of the tandem phosphatase domains of RPTP LAR. Cell 97, 449-457.
8. Nam H-J, Poy F, Saito H, &, Frederick CA, (2005) Structural basis for the function and regulation of the receptor protein tyrosine phosphatase CD45. J Exp Med 201, 441-452.
9. Barr AJ, Ugochukwu E, Lee WH, King ON, Filippakopoulos P, Alfano I, Savitsky P, Burgess-Brown NA, Muller S, &, Knapp S, (2009) Large-scale structural analysis of the classical human protein tyrosine phosphatome. Cell 136, 352-363.
10. Tonks NK, (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7, 833-846.
11. Meng K, Rodriguez-Pena A, Dimitrov T, Chen W, Yamin M, Noda M, &, Deuel TF, (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.
12. Fukada M, Fujikawa A, Chow JP, Ikematsu S, Sakuma S, &, Noda M, (2006) Protein tyrosine phosphatase receptor type Z is inactivated by ligand-induced oligomerization. FEBS Lett 580, 4051-4056.
13. Perez-Pinera P, Alcantara S, Dimitrov T, Vega JA, &, Deuel TF, (2006) Pleiotrophin disrupts calcium-dependent homophilic cell-cell adhesion and initiates an epithelial-mesenchymal transition. Proc Natl Acad Sci USA 103, 17795-17800.
14. Muller S, Kunkel P, Lamszus K, Ulbricht U, Lorente GA, Nelson AM, von Schack D, Chin DJ, Lohr SC, Westphal M, et al. (2003) Arole for receptor tyrosine phosphatase zeta in glioma cell migration. Oncogene 22, 6661-6668.
15. Mikelis C, Sfaelou E, Koutsioumpa M, Kieffer N, &, Papdimitriou E, (2009) Integrin αvβ3 is a pleiotrophin receptor required for pleiotrophin-induced endothelial cell migration through receptor protein tyrosine phosphatase β/ζ. FASEB J 23, 1459-1469.
16. Hodivala-Dilke K, Reynolds A, &, Reynolds L, (2003) Integrins in angiogenesis: multitalented molecules in a balancing act. Cell Tissue Res 314, 131-144.
17. Polytarchou C, Hatziapostolou M, Poimenidi E, Mikelis C, Papadopoulou A, Parthymou A, &, Papadimitriou E, (2009) Nitric oxide stimulates migration of human endothelial and prostate cancer cells through up-regulation of pleiotrophin expression and its receptor protein tyrosine phosphatase β/ζ. Int J Cancer 124, 1785-1793.
18. Diamantopoulou Z, Courty J, &, Katsoris P, (2011) Pleiotrophin biological activity results from the opposing effects of PTPRZ1 and ALK. In Europhosphatases 2011, Protein Phosphatases: From Molecules to Networks. Abstract P18. Baden, Austria.
19. Sakurai T, Lustig M, Nativ M, Hemperly JJ, Schlessinger J, Peles E, &, Grumet M, (1997) Induction of neurite outgrowth through contactin and Nr-CAM by extracellular regions of glial receptor tyrosine phosphatase beta. J Cell Biol 136, 907-918.
20. Hashemi H, Hurley M, Gibson A, Panova V, Tchetchelnitski V, Barr A, &, Stoker AW, (2011) Receptor tyrosine phosphatase PTPgamma is a regulator of spinal cord neurogenesis. Mol Cell Neurosci 46, 469-482.
21. Bouyain S, &, Watkins DJ, (2010) The protein tyrosine phosphatases PTPRZ and PTPRG bind to distinct members of the contactin family of neural recognition molecules. Proc Natl Acad Sci USA 107, 2443-2448.
22. Barnea G, Silvennoinen O, Shaanan B, Honegger AM, Canoll PD, D'Eustachio P, Morse B, Levy JB, Laforgia S, Huebner K, et al. (1993) Identification of a carbonic anhydrase-like domain in the extracellular region of RPTP gamma defines a new subfamily of receptor tyrosine phosphatases. Mol Cell Biol 13, 1497-1506.
23. Krueger NX, &, Saito H, (1992) Ahuman transmembrane protein-tyrosine-phosphatase, PTP zeta, is expressed in brain and has an N-terminal receptor domain homologous to carbonic anhydrases. Proc Natl Acad Sci USA 89, 7417-7421.
24. Peles E, Nativ M, Campbell PL, Sakurai T, Martinez R, Lev S, Clary DO, Schilling J, Barnea G, Plowman GD, et al. (1995) The carbonic anhydrase domain of receptor tyrosine phosphatase beta is a functional ligand for the axonal cell recognition molecule contactin. Cell 82, 251-260.
25. Zuko A, Bouyain S, van der Zwaag B, &, Burbach JP, (2011) Contactins: structural aspects in relation to developmental functions in brain disease. Adv Protein Chem Struct Biol 84, 143-180.
26. Lamprianou S, Chatzopoulou E, Thomas JL, Bouyain S, &, Harroch S, (2011) A complex between contactin-1 and the protein tyrosine phosphatase PTPRZ controls the development of oligodendrocyte precursor cells. Proc Natl Acad Sci USA 108, 17498-17503.
27. Peles E, Schlessinger J, &, Grumet M, (1998) Multi-ligand interactions with receptor-like protein tyrosine phosphatase β: implications for intercellular signaling. Trend Biochem Sci 23, 121-124.
28. Czopka T, von Holst A, ffrench-Constant C, &, Faissner A, (2010) Regulatory mechanisms that mediate tenascin C-dependent inhibition of oligodendrocyte precursor differentiation. J Neurosci 30, 12310-12322.
29. Czopka T, Von Holst A, Schmidt G, ffrench-Constant C, &, Faissner A, (2009) Tenascin C and tenascin R similarly prevent the formation of myelin membranes in a RhoA-dependent manner, but antagonistically regulate the expression of myelin basic protein via a separate pathway. Glia 57, 1790-1801.
30. Desai CJ, Popova E, &, Zinn K, (1994) A Drosophila receptor tyrosine phosphatase expressed in the embryonic CNS and larval optic lobes is a member of the set of proteins bearing the 'HRP' carbohydrate epitope. J Neurosci 14, 7272-7283.
31. Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, Marcu O, Heslip TR, Marsh JL, Schwarz TL, et al. (2006) The HSPGs syndecan and dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49, 517-531.
32. Elchebly M, Wagner J, Kennedy TE, Lanctot C, Michaliszyn E, Itie A, Drouin J, &, Tremblay ML, (1999) Neuroendocrine dysplasia in mice lacking protein tyrosine phosphatase sigma. Nat Genet 21, 330-333.
33. Kolkman MJ, Streijger F, Linkels M, Bloemen M, Heeren DJ, Hendriks WJ, &, Van der Zee CE, (2004) Mice lacking leukocyte common antigen-related (LAR) protein tyrosine phosphatase domains demonstrate spatial learning impairment in the two-trial water maze and hyperactivity in multiple behavioural tests. Behav Brain Res 154, 171-182.
34. Uetani N, Chagnon MJ, Kennedy TE, Iwakura Y, &, Tremblay ML, (2006) Mammalian motoneuron axon targeting requires receptor protein tyrosine phosphatases sigma and delta. J Neurosci 26, 5872-5880.
35. Uetani N, Kato K, Ogura H, Mizuno K, Kawano K, Mikoshiba K, Yakura H, Asano M, &, Iwakura Y, (2000) Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice. EMBO J 19, 2775-2785.
36. Wallace MJ, Batt J, Fladd CA, Henderson JT, Skarnes W, &, Rotin D, (1999) Neuronal defects and posterior pituitary hypoplasia in mice lacking the receptor tyrosine phosphatase PTPsigma. Nat Genet 21, 334-338.
37. 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.
38. Fox AN, &, Zinn K, (2005) The heparan sulfate proteoglycan syndecan is an in vivo ligand for the Drosophila LAR receptor tyrosine phosphatase. Curr Biol 15, 1701-1711.
39. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, &, Flanagan JG, (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326, 592-596.
40. Coles CH, Shen Y, Tenney AP, Siebold C, Sutton GC, Lu W, Gallagher JT, Jones EY, Flanagan JG, &, Aricescu AR, (2011) Proteoglycan-specific molecular switch for RPTPsigma clustering and neuronal extension. Science 332, 484-488.
41. Biersmith BH, Hammel M, Geisbrecht ER, &, Bouyain S, (2011) The immunoglobulin-like domains 1 and 2 of the protein tyrosine phosphatase LAR adopt an unusual horseshoe-like conformation. J Mol Biol 408, 616-627.
42. Kwon SK, Woo J, Kim SY, Kim H, &, Kim E, (2010) Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation. J Biol Chem 285, 13966-13978.
43. Woo J, Kwon SK, Choi S, Kim S, Lee JR, Dunah AW, Sheng M, &, Kim E, (2009) Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat Neurosci 12, 428-437.
44. Takahashi H, Arstikaitis P, Prasad T, Bartlett TE, Wang YT, Murphy TH, &, Craig AM, (2011) Postsynaptic TrkC and presynaptic PTPsigma function as a bidirectional excitatory synaptic organizing complex. Neuron 69, 287-303.
45. Tonks N, Charbonneau H, Diltz C, Fischer E, &, Walsh K, (1988) Demonstration that the leukocyte common antigen CD45 is a protein tyrosine phosphatase. Biochemistry 27, 8695-8701.
46. Charbonneau H, Tonks N, Walsh K, &, Fischer E, (1988) The leukocyte common antigen (CD45): a putative receptor-linked protein tyrosine phosphatase. Proc Natl Acad Sci USA 85, 7182-7186.
47. Trowbridge I, &, Thomas M, (1994) CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu Rev Immunol 12, 85-116.
48. Kung C, Pingel J, Heikinheio M, Klemola T, Varkila K, Yoo L, Vuopala K, Poyhonen M, Uhari M, Rogers M, et al. (2000) Mutations in the tyrosine phosphatase CD45 gene in a child with severe combined immunodeficiency disease. Nat Med 6, 343-345.
49. Kishihara K, Penninger J, Wallace V, Kündig T, Kawai K, Wakeham A, Timms E, PFfeffer K, Ohashi P, &, Thomas M, (1993) Normal B lymphocyte development but impaired T cell maturation in CD45-exon 6 protein tyrosine phosphatase-deficient mice. Cell 74, 143-156.
50. Ledbetter J, Tonks N, Fischer E, &, Clark E, (1988) CD45 regulates signal transduction and lymphocyte activation by specific association with receptor molecules on T or B cells. Proc Natl Acad Sci USA 85, 8628-8632.
51. Janeway CJ, (1992) The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu Rev Immunol 10, 645-674.
52. Hermiston M, Xu Z, &, Weiss A, (2003) CD45: a critical regulator of signaling thresholds in immune cells. Annu Rev Immunol 21, 107-137.
53. Hermiston M, Zikherman J, &, Zhu J, (2009) CD45, CD148, and Lyp/Pep: critical phosphatases regulating Src family kinase signaling networks in immune cells. Immunol Rev 228, 288-311.
54. Irles C, Symons A, Michel F, Bakker T, van der Merwe P, &, Acuto O, (2003) CD45 ectodomain controls interaction with GEMs and Lck activity for optimal TCR signaling. Nat Immunol 4, 189-197.
55. Novak T, Farber D, Leitenberg D, Hong S, Johnson P, &, Bottomly K, (1994) Isoforms of the transmembrane tyrosine phosphatase CD45 differentially affect T cell recognition. Immunity 1, 109-119.
56. Earl L, &, Baum L, (2008) CD45 Glycosylation controls T-cell life and death. Immunol Cell Biol 86, 608-615.
57. Pulido R, &, Sánchez-Madrid F, (1992) Glycosylation of CD45: carbohydrate processing through Golgi appartaus is required for cell surface expression and protein stability. Eur J Immunol 22, 463-468.
58. Earl L, Bi S, &, Baum L, (2010) N- and O-glycans modulate galectin-1 binding, CD45 signaling, and T cell death. J Biol Chem 285, 2232-2244.
59. Perillo N, Pace K, Seilhamer J, &, Baum L, (1995) Apoptosis of T cells mediated by galectin-1. Nature 378, 736-739.
60. Barondes SH, Castronovo V, Cooper DNW, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K-I, et al. (1994) Galectins: a family of animal β-galactoside-binding lectins. Cell 76, 597-598.
61. Hirabayashi J, Hashidate T, Arata Y, Nishi N, Nakamura T, Hirashima M, Urashima T, Oka T, Futai M, Muller WE, et al. (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim Biophys Acta 1572, 232-254.
62. Hughes C, (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473, 172-185.
63. Walzel H, Schulz U, Neels P, &, Brock J, (1999) Galectin-1, a natural ligand for the receptor-type protein tyrosine phosphatase CD45. Immunol Lett 67, 193-202.
64. Symons A, Cooper D, &, Barclay A, (2000) Characterization of the interaction between galectin-1 and lymphocyte glycoproteins CD45 and Thy-1. Glycobiology 10, 559-563.
65. Pace K, Lee C, Steward P, &, Baum L, (1999) Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J Immunol 163, 3801-3811.
66. Nguyen J, Evans D, Galvan M, Pace K, Leitenberg D, Bui T, &, Baum L, (2001) CD45 modulates galectin-1-induced T cell death: regulation by expression of core 2 O-glycans. J Immunol 167, 5697-5707.
67. Kim Y-S, Kang H-Y, Kim J-Y, Oh S, Kim C-H, Ryo CJ, Miyoshi E, Taniguchi N, &, Ko JH, (2006) Identification of target proteins of N-acetylgulcosaminyl transferase V in huan colon cancer and implications of protein tyrosine phosphatase kappa in enhanced cancer cell migration. Proteomics 6, 1187-1191.
68. Kim Y-S, Jung J-A, Kim H-J, Ahn YH, Yoo JS, Oh S, Cho C, Yoo H-S, &, Ko J-K, (2011) Galectin-3 binding protein promotes cell motility in colon cancer by stimulating the shedding of protein tyrosine prhosphatase kappa by proprotein convertase 5. Biochem Biophys Res Commun 404, 96-102.
69. Seetharaman J, Kanigsberg A, Slaaby R, Leffler H, Barondes SH, &, Rini JM, (1998) X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1 Å resolution. J Biol Chem 273, 13047-13052.
70. Zondag GCM, Koningstein GM, Jiang YP, Sap J, Moolenaar WH, &, Gebbink MFBG, (1995) Homophilic interactions mediated by receptor tyrosine phosphatases μ and κ. Acritical role for the novel extracellular MAM domain. J Biol Chem 270, 14247-14250.
71. Brady-Kalnay S, Flint A, &, Tonks N, (1993) Homophilic binding of PTPu, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol 122, 961-972.
72. Sap J, Jiany Y, Friedlander D, Grumet M, &, Schlessinger J, (1994) Receptor tyrosine phosphatase R-PTP-kappa mediates homophilic binding. Mol Cell Biol 14, 1-9.
73. Wang J, &, Bixby JL, (1999) Receptor tyrosine phosphatase-δ is a homophilic, neurite-promoting cell adhesion molecule for CNS neurons. Mol Cell Neurosci 14, 370-384.
74. Cheng J, Wu K, Armanini M, O'Rourke N, Dowbenko D, &, Lasky L, (1997) A novel protein-tyrosine phosphatase related to the homotypically adhering k and u receptors. J Biol Chem 272, 7264-7277.
75. Yu J, Becka S, Zhang P, Zhang X, Brady-Kalnay SM, &, Wang Z, (2008) Tumor-derived extracellular mutations of PTPRT/PTPρ are defective in cell adhesion. Mol Cancer Res 6, 1106-1113.
76. Becka S, Zhang P, Craig SE, Lodowski DT, Wang Z, &, Brady-Kalnay S, (2010) Characterization of the adhesive properties of the type iib subfamily of RPTPs. Cell Commun Adhes 17, 34-47.
77. Gebbink M, Zondag G, Wubbolts R, Beijersbergen R, van Etten I, &, Moolenaar W, (1993) Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem 268, 16101-16104.
78. Zhang P, Becka S, Craig SE, Lodowski DT, Brady-Kalnay S, &, Wang Z, (2009) Cancer-derived mutations in the fibronectin III repeats of PTPRT/PTPrho inhibit cell-cell aggregation. Cell Commun Adhes 16, 146-153.
79. Brady-Kalnay S, &, Tonks N, (1994) identification of the homophilic binding site of the receptor protein tyrosine phosphatase PTPM. J Biol Chem 269, 28472-28477.
80. Cismasiu V, Denes S, Reiländer H, Michel H, &, Szedlacsek S, (2004) The MAM (meprin/A5-protein/PTPmu) domain is a homophilic binding site promoting the lateral dimerization of receptor-like protein-tyrosine phosphatase mu. J Biol Chem 279, 26922-26931.
81. Aricescu AR, Hon W-C, Siebold C, Lu W, van der Merwe PA, &, Jones EY, (2006) Molecular analysis of receptor protein tyrosine phosphatase [mu]-mediated cell adhesion. EMBO J 25, 701-712.
82. Aricescu AR, &, Jones EY, (2007) Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Curr Opin Cell Biol 19, 543-550.
83. Rosdahl J, Ensslen S, Niedenthal J, &, Brady-Kalnay S, (2003) PTPμ-dependent growth cone rearrangement is regulated by Cdc42. J Neurobiol 56, 199-208.
84. Ensslen-Craig SE, &, Brady-Kalnay SM, (2005) PTPμ expression and catalytic activity are required for PTPμ-mediated neurite outgrowth and repulsion. Mol Cell Neurosci 28, 177-188.
85. Aricescu AR, Siebold C, Choudhuri K, Chang VT, Lu W, Davis SJ, van der Merwe PA, &, Jones EY, (2007) Structure of a tyrosine phosphatase adhesive interaction reveals a spacer-clamp mechanism. Science 317, 1217-1220.
86. Majeti R, Bilwes AM, Noel JP, Hunter T, &, Weiss A, (1998) Dimerization-induced inhibition of receptor protein tyrosine phosphatase function through an inhibitory wedge. Science 279, 88-91.
87. Takeda A, Wu JJ, &, Maizel AL, (1992) Evidence for monomeric and dimeric forms of CD45 associated with a 30-kDa phosphorylated protein. J Biol Chem 267, 16651-16659.
88. Lee S, Faux C, Nixon J, Alete D, Chilton J, Hawadle M, &, Stoker AW, (2007) Dimerization of protein tyrosine phosphatase σ governs both ligand binding and isoform specificity. Mol Cell Biol 27, 1795-1808.
89. Heldin C, &, Ostman A, (1996) Ligand-induced dimerization of growth factor receptors: variations on the theme. Cytokine Growth Factor Rev 7, 3-10.
90. Hubbard S, Mohammadi M, &, Schlessinger J, (1998) Autoregulatory mechanisms in protein-tyrosine kinases. J Biol Chem 15, 11987-11990.
91. Hower A, Beltran P, &, Bixby J, (2009) Dimerization of tyrosine phosphatase PTPRO decreases its activity and ability to inactivate TrkC. J Neurochem 110, 1635-1647.
92. Perez-Pinera P, Zhang W, Chang Y, Vega JA, &, Deuel TF, (2007) Anaplastic lymphoma kinase is activated through the pleiotrophin/receptor protein-tyrosine phosphatase β/ζ signaling pathway. J Biol Chem 282, 28683-28690.
93. Shintani T, &, Noda M, (2008) Protein tyrosine phosphatase receptor type Z dephosphorylates TrkA receptors and attenuates NGF-dependent neurite outgrowth of PC12 cells. J Biochem 144, 259-266.
94. Xu Y, Xia W, Baker D, Zhou J, Cha HC, Voorhees JJ, &, Fisher GJ, (2011) Receptor-type protein tyrosine phsphatase β (RPTP-β) directly dephosphorylates and regulates hepatocyte growth factor receptor (HGFR/Met) function. J Biol Chem 286, 15980-15988.
95. Beltran P, Bixby J, &, Masters B, (2003) Expression of PTPRO during mouse development suggests involvement in axonogenesis and differentiation of NT-3 and NGF-dependent neurons. J Comp Neurol 456, 384-395.
96. Gonzalez-Brito M, &, Bixby J, (2009) Protein tyrosine phosphatase receptor type O regulates development and function of the sensory nervous system. Mol Cell Neurosci 42, 458-465.
97. Segal RA, (2003) Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 26, 299-330.
98. Bowden ET, Stoica GE, &, Wellstein A, (2002) Anti-apoptotic signaling of pleiotrophin through its receptor, anaplastic lymphoma kinase. J Biol Chem 277, 35862-35868.
99. Powers C, Aigner A, Stoica GE, McDonnell K, &, Wellstein A, (2002) Pleiotrophin signaling through anaplastic lymphoma kinase is rate-limiting for glioblastoma growth. J Biol Chem 277, 14153-14158.
100. Stoica GE, Kuo A, Aigner A, Sunitha I, Souttou B, Malerczyk C, Caughey DJ, Wen D, Karavanov A, Riegel AT, et al. (2001) Identification of anaplastic lymphoma kinase as a receptor for the growth factor pleiotrophin. J Biol Chem 276, 16772-16779.
101. Fischer E, (1999) Cell signaling by protein tyrosine phosphorylation. Adv Enzyme Regul 39, 359-369.
102. Mauro L, &, Dixon J, (1994) 'Zip codes' direct intracellular protein tyrosine phosphatases to the corect cellular 'address'. Trends Biochem Sci 19, 151-155.
103. Andersen J, Elson A, Lammers R, Rømer J, Clausen J, Møller K, &, Møller N, (2001) Comparative study of protein tyrosine phopshatase-epsilon isoforms: membrane localization confers specificity in cellular signalling. Biochem J 354, 581-590.
104. Møller N, Møller K, Lammers R, Kharitonenkov A, Hoppe E, Wiberg F, Sures I, &, Ullrich A, (1995) Selective down-regulation of the insulin receptor signal by protein-tyrosine phosphatase epsilon. J Biol Chem 270, 126-131.
105. Dilaver G, van de Vorstenbosch R, Tárrega C, Ríos P, Pulido R, van Aerde K, Fransen J, &, Hendriks W, (2007) Proteolytic processing of the receptor-type protein tyrosine phosphatase PTPBR7. FEBS J 274, 96-108.
106. Gil-Henn H, Volohonsky G, &, Elson A, (2001) Regulation of protein-tyrosine phosphatases alpha and epsilon by calpain-mediated proteolytic cleavage. J Biol Chem 276, 31772-31779.
107. Chow J, Fujikawa A, Shimizu H, &, Noda M, (2008) Plasmin-mediated processing of protein tyrosine phosphatase receptor type Z in the mouse brain. Neuroletters 442, 208-212.
108. Aicher B, Lerch MM, Müller T, Schilling J, &, Ullrich A, (1997) Cellular redistribution of protein tyrosine phosphatases LAR and PTPσ by inducible proteolytic processing. J Cell Biol 138, 681-696.
109. Serra-Pages C, Saito H, &, Streuli M, (1994) Mutational analysis of proprotein processing, subunit association, and shedding of the LAR transmembrane protein tyrosine phosphatase. J Biol Chem 269, 23632-23641.
110. Streuli M, Krueger NX, Ariniello PD, Tang M, Munro JM, Blattler WA, Adler DA, Disteche CM, &, Saito H, (1992) Expression of the receptor-linked protein tyrosine phosphatase LAR: proteolytic cleavage and shedding of the CAM-like extracellular region. EMBO J 11, 897-907.
111. Maeda N, Hamanaka H, Shintani T, Nishiwaki T, &, Noda M, (1994) Multiple receptor-like protein tyrosine phosphatases in the form of chondroitin sulfate proteoglycan. FEBS Lett 354, 67-70.
112. Sakurai T, Friedlander D, &, Grumet M, (1996) Expression of polypeptide variants of receptor-type protein tyrosine phosphatase beta: the secreted form, phosphacan, increase dramatically during embryonic development and modulates glial cell behavior in vitro. J Neurosci Res 43, 694-706.