Protein tyrosine phosphatases in health and disease

FEBS Journal

Volumn 280, Issue 2, 2013, Pages 708-730

  Hendriks, Wiljan J A J ^a   Elson, Ari ^b   Harroch, Sheila ^c   Pulido, Rafael ^d   Stoker, Andrew ^e   Den Hertog, Jeroen ^f,g  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c INSTITUT PASTEUR   (France)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g LEIDEN UNIVERSITY   (Netherlands)

Author keywords

bone morphogenesis; hereditary disease; neuronal development; post translational modification; protein tyrosine phosphatase; synaptogenesis

Indexed keywords

CD45 ANTIGEN; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE FYN; PROTEIN KINASE YES; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE EPSILON; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ALCOHOL CONSUMPTION; ALZHEIMER DISEASE; ANGIOSARCOMA; AUTISM; BONE DEVELOPMENT; CHROMOSOME DELETION; CHROMOSOME DELETION 3P; DEMYELINATING DISEASE; DEPRESSION; EXCITATORY JUNCTION POTENTIAL; GAIN OF FUNCTION MUTATION; GASTRULATION; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; HUMAN; LEOPARD SYNDROME; LONG TERM DEPRESSION; LOSS OF FUNCTION MUTATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; NOONAN SYNDROME; OSTEOCLAST; PARKINSON DISEASE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PTENA GENE; PTENB GENE; PTPN1 GENE; PTPN11 GENE; PTPN14 GENE; PTPN18 GENE; PTPN2 GENE; PTPN20 GENE; PTPN21 GENE; PTPN22 GENE; PTPN23 GENE; PTPN4 GENE; PTPN5 GENE; PTPRC GENE; PTPRD GENE; PTPRF GENE; PTPRH GENE; PTPRJ GENE; PTPRQ GENE; PTPRS GENE; PTPRT GENE; PTPRU GENE; REVIEW; SYNAPTOGENESIS; ZEBRA FISH;

ANIMALS; BONE DEVELOPMENT; CENTRAL NERVOUS SYSTEM DISEASES; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MUTATION; PROTEIN TYROSINE PHOSPHATASES; SIGNAL TRANSDUCTION; SYNAPSES;

ANIMALIA;

EID: 84872772147     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12000     Document Type: Review

References (160)

1. Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, &, Mustelin T, (2004) Protein tyrosine phosphatases in the human genome. Cell 117, 699-711.
2. Andersen JN, Jansen PG, Echwald SM, Mortensen OH, Fukada T, Del Vecchio R, Tonks NK, &, Moller NP, (2004) A genomic perspective on protein tyrosine phosphatases: gene structure, pseudogenes, and genetic disease linkage. FASEB J 18, 8-30.
3. den Hertog J, Ostman A, &, Bohmer FD, (2008) Protein tyrosine phosphatases: regulatory mechanisms. FEBS J 275, 831-847.
4. Hendriks WJ, Elson A, Harroch S, &, Stoker AW, (2008) Protein tyrosine phosphatases: functional inferences from mouse models and human diseases. FEBS J 275, 816-830.
5. Tonks NK, (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7, 833-846.
6. Hardy S, Julien SG, &, Tremblay ML, (2011) Impact of Oncogenic Protein Tyrosine Phosphatases in Cancer. Anticancer Agents Med Chem 12, 4-18.
7. Julien SG, Dube N, Hardy S, &, Tremblay ML, (2011) Inside the human cancer tyrosine phosphatome. Nat Rev Cancer 11, 35-49.
8. Navis AC, van den Eijnden M, Schepens JT, Hooft van Huijsduijnen R, Wesseling P, &, Hendriks WJ, (2010) Protein tyrosine phosphatases in glioma biology. Acta Neuropathol 119, 157-175.
9. Nunes-Xavier C, Roma-Mateo C, Rios P, Tarrega C, Cejudo-Marin R, Tabernero L, &, Pulido R, (2011) Dual-specificity MAP kinase phosphatases as targets of cancer treatment. Anticancer Agents Med Chem 11, 109-132.
10. Pulido R, &, Hooft van Huijsduijnen R, (2008) Protein tyrosine phosphatases: dual-specificity phosphatases in health and disease. FEBS J 275, 848-866.
11. Bermudez O, Pages G, &, Gimond C, (2010) The dual-specificity MAP kinase phosphatases: critical roles in development and cancer. Am J Physiol Cell Physiol 299, C189-C202.
12. Ruela-de-Sousa RR, Queiroz KC, Peppelenbosch MP, &, Fuhler GM, (2010) Reversible phosphorylation in haematological malignancies: potential role for protein tyrosine phosphatases in treatment? Biochim Biophys Acta 1806, 287-303.
13. Wishart MJ, &, Dixon JE, (2002) PTEN and myotubularin phosphatases: from 3-phosphoinositide dephosphorylation to disease. Trends Cell Biol 12, 579-585.
14. Liu Y, &, Bankaitis VA, (2010) Phosphoinositide phosphatases in cell biology and disease. Prog Lipid Res 49, 201-217.
15. Gentry MS, Dixon JE, &, Worby CA, (2009) Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem Sci 34, 628-639.
16. Loh K, Fukushima A, Zhang X, Galic S, Briggs D, Enriori PJ, Simonds S, Wiede F, Reichenbach A, Hauser C, et al.,. (2011) Elevated hypothalamic TCPTP in obesity contributes to cellular leptin resistance. Cell Metab 14, 684-699.
17. Young JA, Becker AM, Medeiros JJ, Shapiro VS, Wang A, Farrar JD, Quill TA, Hooft van Huijsduijnen R, &, van Oers NS, (2008) The protein tyrosine phosphatase PTPN4/PTP-MEG1, an enzyme capable of dephosphorylating the TCR ITAMs and regulating NF-kappaB, is dispensable for T cell development and/or T cell effector functions. Mol Immunol 45, 3756-3766.
18. Bauler TJ, Hendriks WJ, &, King PD, (2008) The FERM and PDZ domain-containing protein tyrosine phosphatases, PTPN4 and PTPN3, are both dispensable for T cell receptor signal transduction. PLoS One 3, e4014.
19. Eswaran J, von Kries JP, Marsden B, Longman E, Debreczeni JE, Ugochukwu E, Turnbull A, Lee WH, Knapp S, &, Barr AJ, (2006) Crystal structures and inhibitor identification for PTPN5, PTPRR and PTPN7: a family of human MAPK-specific protein tyrosine phosphatases. Biochem J 395, 483-491.
20. Gronda M, Arab S, Iafrate B, Suzuki H, &, Zanke BW, (2001) Hematopoietic protein tyrosine phosphatase suppresses extracellular stimulus-regulated kinase activation. Mol Cell Biol 21, 6851-6858.
21. Chirivi RG, Noordman YE, Van der Zee CE, &, Hendriks WJ, (2007) Altered MAP kinase phosphorylation and impaired motor coordination in PTPRR deficient mice. J Neurochem 101, 829-840.
22. Venkitaramani DV, Paul S, Zhang Y, Kurup P, Ding L, Tressler L, Allen M, Sacca R, Picciotto MR, &, Lombroso PJ, (2009) Knockout of striatal enriched protein tyrosine phosphatase in mice results in increased ERK1/2 phosphorylation. Synapse (New York, NY) 63, 69-81.
23. Baum ML, Kurup P, Xu J, &, Lombroso PJ, (2010) A STEP forward in neural function and degeneration. Commun Integr Biol 3, 419-422.
24. Zhang Y, Kurup P, Xu J, Carty N, Fernandez SM, Nygaard HB, Pittenger C, Greengard P, Strittmatter SM, Nairn AC, et al.,. (2010) Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer's disease mouse model. Proc Natl Acad Sci USA 107, 19014-19019.
25. Gingras MC, Zhang YL, Kharitidi D, Barr AJ, Knapp S, Tremblay ML, &, Pause A, (2009) HD-PTP is a catalytically inactive tyrosine phosphatase due to a conserved divergence in its phosphatase domain. PLoS One 4, e5105.
26. Lin G, Aranda V, Muthuswamy SK, &, Tonks NK, (2011) Identification of PTPN23 as a novel regulator of cell invasion in mammary epithelial cells from a loss-of-function screen of the 'PTP-ome'. Genes Dev 25, 1412-1425.
27. Gingras MC, Kharitidi D, Chenard V, Uetani N, Bouchard M, Tremblay ML, &, Pause A, (2009) Expression analysis and essential role of the putative tyrosine phosphatase His-domain-containing protein tyrosine phosphatase (HD-PTP). Int J Dev Biol 53, 1069-1074.
28. Sadakata H, Okazawa H, Sato T, Supriatna Y, Ohnishi H, Kusakari S, Murata Y, Ito T, Nishiyama U, Minegishi T, et al.,. (2009) SAP-1 is a microvillus-specific protein tyrosine phosphatase that modulates intestinal tumorigenesis. Genes Cells 14, 295-308.
29. Murata Y, Mori M, Kotani T, Supriatna Y, Okazawa H, Kusakari S, Saito Y, Ohnishi H, &, Matozaki T, (2010) Tyrosine phosphorylation of R3 subtype receptor-type protein tyrosine phosphatases and their complex formations with Grb2 or Fyn. Genes Cells 15, 513-524.
30. Wang Z, Shen D, Parsons DW, Bardelli A, Sager J, Szabo S, Ptak J, Silliman N, Peters BA, van der Heijden MS, et al.,. (2004) Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 304, 1164-1166.
31. Lim SH, Kwon SK, Lee MK, Moon J, Jeong DG, Park E, Kim SJ, Park BC, Lee SC, Ryu SE, et al.,. (2009) Synapse formation regulated by protein tyrosine phosphatase receptor T through interaction with cell adhesion molecules and Fyn. EMBO J 28, 3564-3578.
32. Zhao Y, Zhang X, Guda K, Lawrence E, Sun Q, Watanabe T, Iwakura Y, Asano M, Wei L, Yang Z, et al.,. (2010) Identification and functional characterization of paxillin as a target of protein tyrosine phosphatase receptor T. Proc Natl Acad Sci USA 107, 2592-2597.
33. Zhu JW, Brdicka T, Katsumoto TR, Lin J, &, Weiss A, (2008) Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28, 183-196.
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, Bertozzi K, Chagnon MJ, Hendriks W, Tremblay ML, &, Bouchard M, (2009) Maturation of ureter-bladder connection in mice is controlled by LAR family receptor protein tyrosine phosphatases. J Clin Invest 119, 924-935.
36. Lieschke GJ, &, Currie PD, (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8, 353-367.
37. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, et al.,. (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37-46.
38. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, et al.,. (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1-36.
39. Wienholds E, Schulte-Merker S, Walderich B, &, Plasterk RH, (2002) Target-selected inactivation of the zebrafish rag1 gene. Science 297, 99-102.
40. Meng X, Noyes MB, Zhu LJ, Lawson ND, &, Wolfe SA, (2008) Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 26, 695-701.
41. Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, et al.,. (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26, 702-708.
42. Lele Z, Bakkers J, &, Hammerschmidt M, (2001) Morpholino phenocopies of the swirl, snailhouse, somitabun, minifin, silberblick, and pipetail mutations. Genesis 30, 190-194.
43. Nasevicius A, &, Ekker SC, (2000) Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26, 216-220.
44. Peterson RT, Link BA, Dowling JE, &, Schreiber SL, (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci USA 97, 12965-12969.
45. van Eekelen M, Overvoorde J, van Rooijen C, &, den Hertog J, (2010) Identification and expression of the family of classical protein-tyrosine phosphatases in zebrafish. PLoS One 5, e12573.
46. van Eekelen M, Runtuwene V, Masselink W, &, den Hertog J, (2012) Pair-wise regulation of convergence and extension cell movements by four phosphatases via RhoA. PLoS One 7, e35913.
47. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, et al.,. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957.
48. Vandepoele K, De Vos W, Taylor JS, Meyer A, &, Van de Peer Y, (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci USA 101, 1638-1643.
49. Force A, Lynch M, Pickett FB, Amores A, Yan YL, &, Postlethwait J, (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
50. Solnica-Krezel L, (2006) Gastrulation in zebrafish-all just about adhesion? Curr Opin Genet Dev 16, 433-441.
51. Jopling C, van Geemen D, &, den Hertog J, (2007) Shp2 knockdown and Noonan/LEOPARD mutant Shp2-induced gastrulation defects. PLoS Genet 3, e225.
52. van Eekelen M, Runtuwene V, Overvoorde J, &, den Hertog J, (2010) RPTPalpha and PTPepsilon signaling via Fyn/Yes and RhoA is essential for zebrafish convergence and extension cell movements during gastrulation. Dev Biol 340, 626-639.
53. Aerne B, &, Ish-Horowicz D, (2004) Receptor tyrosine phosphatase psi is required for Delta/Notch signalling and cyclic gene expression in the presomitic mesoderm. Development 131, 3391-3399.
54. Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, Kremer H, van dBI, Crosby AH, Ion A, Jeffery S, et al.,. (2001) Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 29, 465-468.
55. Allanson JE, (1987) Noonan syndrome. J Med Genet 24, 9-13.
56. Gorlin RJ, Anderson RC, &, Moller JH, (1971) The leopard (multiple lentigines) syndrome revisited. Laryngoscope 81, 1674-1681.
57. Stewart RA, Sanda T, Widlund HR, Zhu S, Swanson KD, Hurley AD, Bentires-Alj M, Fisher DE, Kontaridis MI, Look AT, et al.,. (2010) Phosphatase-dependent and -independent functions of Shp2 in neural crest cells underlie LEOPARD syndrome pathogenesis. Dev Cell 18, 750-762.
58. Wyatt L, Wadham C, Crocker LA, Lardelli M, &, Khew-Goodall Y, (2007) The protein tyrosine phosphatase Pez regulates TGFbeta, epithelial-mesenchymal transition, and organ development. J Cell Biol 178, 1223-1235.
59. Chen X, Yoshida T, Sagara H, Mikami Y, &, Mishina M, (2011) Protein tyrosine phosphatase sigma regulates the synapse number of zebrafish olfactory sensory neurons. J Neurochem 119, 532-543.
60. Faucherre A, Taylor GS, Overvoorde J, Dixon JE, &, den Hertog J, (2008) Zebrafish pten genes have overlapping and non-redundant functions in tumorigenesis and embryonic development. Oncogene 27, 1079-1086.
61. Choorapoikayil S, Kuiper RV, de Bruin A, &, den Hertog J, (2012) Haploinsufficiency of the genes encoding the tumor suppressor Pten predisposes zebrafish to hemangiosarcoma. Dis Model Mech, 5, 241-247.
62. Boyle WJ, Simonet WS, &, Lacey DL, (2003) Osteoclast differentiation and activation. Nature 423, 337-342.
63. Ducy P, Schinke T, &, Karsenty G, (2000) The osteoblast: a sophisticated fibroblast under central surveillance. Science 289, 1501-1504.
64. Harada S, &, Rodan GA, (2003) Control of osteoblast function and regulation of bone mass. Nature 423, 349-355.
65. Aguila HL, &, Rowe DW, (2005) Skeletal development, bone remodeling, and hematopoiesis. Immunol Rev 208, 7-18.
66. Bruzzaniti A, &, Baron R, (2006) Molecular regulation of osteoclast activity. Rev Endocr Metab Disord 7, 123-139.
67. Luxenburg C, Parsons JT, Addadi L, &, Geiger B, (2006) Involvement of the Src-cortactin pathway in podosome formation and turnover during polarization of cultured osteoclasts. J Cell Sci 119, 4878-4888.
68. Soriano P, Montgomery C, Geske R, &, Bradley A, (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702.
69. Destaing O, Sanjay A, Itzstein C, Horne WC, Toomre D, De Camilli P, &, Baron R, (2008) The tyrosine kinase activity of c-Src regulates actin dynamics and organization of podosomes in osteoclasts. Mol Biol Cell 19, 394-404.
70. Wada T, Nakashima T, Hiroshi N, &, Penninger JM, (2006) RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol Med 12, 17-25.
71. Ross FP, (2006) M-CSF, c-Fms, and signaling in osteoclasts and their precursors. Ann N Y Acad Sci 1068, 110-116.
72. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, Neff L, Sanjay A, Bruzzaniti A, De Camilli P, Baron R, et al.,. (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178, 1053-1064.
73. Buckbinder L, Crawford DT, Qi H, Ke HZ, Olson LM, Long KR, Bonnette PC, Baumann AP, Hambor JE, Grasser WA III, et al.,. (2007) Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc Natl Acad Sci USA 104, 10619-10624.
74. Luxenburg C, Addadi L, &, Geiger B, (2006) The molecular dynamics of osteoclast adhesions. Eur J Cell Biol 85, 203-211.
75. Chiusaroli R, Knobler H, Luxenburg C, Sanjay A, Granot-Attas S, Tiran Z, Miyazaki T, Harmelin A, Baron R, &, Elson A, (2004) Tyrosine phosphatase epsilon is a positive regulator of osteoclast function in vitro and in vivo. Mol Biol Cell 15, 234-244.
76. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, et al.,. (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12, 657-664.
77. Granot-Attas S, Luxenburg C, Finkelshtein E, &, Elson A, (2009) Protein tyrosine phosphatase epsilon regulates integrin-mediated podosome stability in osteoclasts by activating Src. Mol Biol Cell 20, 4324-4334.
78. Carlson J, Cui W, Zhang Q, Xu X, Mercan F, Bennett AM, &, Vignery A, (2009) Role of MKP-1 in osteoclasts and bone homeostasis. Am J Pathol 175, 1564-1573.
79. Sartori R, Li F, &, Kirkwood KL, (2009) MAP kinase phosphatase-1 protects against inflammatory bone loss. J Dent Res 88, 1125-1130.
80. Umeda S, Beamer WG, Takagi K, Naito M, Hayashi S, Yonemitsu H, Yi T, &, Shultz LD, (1999) Deficiency of SHP-1 protein-tyrosine phosphatase activity results in heightened osteoclast function and decreased bone density. Am J Pathol 155, 223-233.
81. Aoki K, Didomenico E, Sims NA, Mukhopadhyay K, Neff L, Houghton A, Amling M, Levy JB, Horne WC, &, Baron R, (1999) The tyrosine phosphatase SHP-1 is a negative regulator of osteoclastogenesis and osteoclast resorbing activity: increased resorption and osteopenia in me(v)/me(v) mutant mice. Bone 25, 261-267.
82. Zhang Z, Jimi E, &, Bothwell AL, (2003) Receptor activator of NF-kappa B ligand stimulates recruitment of SHP-1 to the complex containing TNFR-associated factor 6 that regulates osteoclastogenesis. J Immunol 171, 3620-3626.
83. Bauler TJ, Kamiya N, Lapinski PE, Langewisch E, Mishina Y, Wilkinson JE, Feng GS, &, King PD, (2011) Development of severe skeletal defects in induced SHP-2-deficient adult mice: a model of skeletal malformation in humans with SHP-2 mutations. Dis Model Mech 4, 228-239.
84. Amoui M, Baylink DJ, Tillman JB, &, Lau KH, (2003) Expression of a structurally unique osteoclastic protein-tyrosine phosphatase is driven by an alternative intronic, cell type-specific promoter. J Biol Chem 278, 44273-44280.
85. Suhr SM, Pamula S, Baylink DJ, &, Lau KH, (2001) Antisense oligodeoxynucleotide evidence that a unique osteoclastic protein-tyrosine phosphatase is essential for osteoclastic resorption. J Bone Miner Res 16, 1795-1803.
86. Amoui M, Suhr SM, Baylink DJ, &, Lau KH, (2004) An osteoclastic protein-tyrosine phosphatase may play a role in differentiation and activity of human monocytic U-937 cell-derived, osteoclast-like cells. Am J Physiol Cell Physiol 287, C874-C884.
87. Amoui M, Sheng MH, Chen ST, Baylink DJ, &, Lau KH, (2007) A transmembrane osteoclastic protein-tyrosine phosphatase regulates osteoclast activity in part by promoting osteoclast survival through c-Src-dependent activation of NFkappaB and JNK2. Arch Biochem Biophys 463, 47-59.
88. Sheng MH, Amoui M, Stiffel V, Srivastava AK, Wergedal JE, &, Lau KH, (2009) Targeted transgenic expression of an osteoclastic transmembrane protein-tyrosine phosphatase in cells of osteoclastic lineage increases bone resorption and bone loss in male young adult mice. J Biol Chem 284, 11531-11545.
89. Larsen M, Tremblay ML, &, Yamada KM, (2003) Phosphatases in cell-matrix adhesion and migration. Nat Rev Mol Cell Biol 4, 700-711.
90. Sastry SK, Rajfur Z, Liu BP, Cote JF, Tremblay ML, &, Burridge K, (2006) PTP-PEST couples membrane protrusion and tail retraction via VAV2 and p190RhoGAP. J Biol Chem 281, 11627-11636.
91. Cote JF, Chung PL, Theberge JF, Halle M, Spencer S, Lasky LA, &, Tremblay ML, (2002) PSTPIP is a substrate of PTP-PEST and serves as a scaffold guiding PTP-PEST toward a specific dephosphorylation of WASP. J Biol Chem 277, 2973-2986.
92. Badour K, Zhang J, Shi F, Leng Y, Collins M, &, Siminovitch KA, (2004) Fyn and PTP-PEST-mediated regulation of Wiskott-Aldrich syndrome protein (WASp) tyrosine phosphorylation is required for coupling T cell antigen receptor engagement to WASp effector function and T cell activation. J Exp Med 199, 99-112.
93. Garton AJ, &, Tonks NK, (1999) Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J Biol Chem 274, 3811-3818.
94. Lyons PD, Dunty JM, Schaefer EM, &, Schaller MD, (2001) Inhibition of the catalytic activity of cell adhesion kinase beta by protein-tyrosine phosphatase-PEST-mediated dephosphorylation. J Biol Chem 276, 24422-24431.
95. Chellaiah MA, Biswas RS, Yuen D, Alvarez UM, &, Hruska KA, (2001) Phosphatidylinositol 3,4,5-trisphosphate directs association of Src homology 2-containing signaling proteins with gelsolin. J Biol Chem 276, 47434-47444.
96. Gupta A, Lee BS, Khadeer MA, Tang Z, Chellaiah M, Abu-Amer Y, Goldknopf J, &, Hruska KA, (2003) Leupaxin is a critical adaptor protein in the adhesion zone of the osteoclast. J Bone Miner Res 18, 669-685.
97. Chellaiah MA, Kuppuswamy D, Lasky L, &, Linder S, (2007) Phosphorylation of a Wiscott-Aldrich syndrome protein-associated signal complex is critical in osteoclast bone resorption. J Biol Chem 282, 10104-10116.
98. Chellaiah MA, &, Schaller MD, (2009) Activation of Src kinase by protein-tyrosine phosphatase-PEST in osteoclasts: comparative analysis of the effects of bisphosphonate and protein-tyrosine phosphatase inhibitor on Src activation in vitro. J Cell Physiol 220, 382-393.
99. Shivtiel S, Kollet O, Lapid K, Schajnovitz A, Goichberg P, Kalinkovich A, Shezen E, Tesio M, Netzer N, Petit I, et al.,. (2008) CD45 regulates retention, motility, and numbers of hematopoietic progenitors, and affects osteoclast remodeling of metaphyseal trabecules. J Exp Med 205, 2381-2395.
100. Wu H, Xiong WC, &, Mei L, (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137, 1017-1033.
101. Mei L, &, Si J, (1995) Tyrosine phosphorylation and synapse formation at the neuromuscular junction. Life Sci 57, 1459-1466.
102. Tanowitz M, Si J, Yu DH, Feng GS, &, Mei L, (1999) Regulation of neuregulin-mediated acetylcholine receptor synthesis by protein tyrosine phosphatase SHP2. J Neurosci 19, 9426-9435.
103. Madhavan R, Zhao XT, Ruegg MA, &, Peng HB, (2005) Tyrosine phosphatase regulation of MuSK-dependent acetylcholine receptor clustering. Mol Cell Neurosci 28, 403-416.
104. Camilleri AA, Willmann R, Sadasivam G, Lin S, Ruegg MA, Gesemann M, &, Fuhrer C, (2007) Tyrosine phosphatases such as SHP-2 act in a balance with Src-family kinases in stabilization of postsynaptic clusters of acetylcholine receptors. BMC Neurosci 8, 46.
105. Stryker E, &, Johnson KG, (2007) LAR, liprin alpha and the regulation of active zone morphogenesis. J Cell Sci 120, 3723-3728.
106. 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.
107. 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.
108. 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.
109. 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.
110. Dickinson BA, Jo J, Seok H, Son GH, Whitcomb DJ, Davies CH, Sheng M, Collingridge GL, &, Cho K, (2009) A novel mechanism of hippocampal LTD involving muscarinic receptor-triggered interactions between AMPARs, GRIP and liprin-alpha. Mol Brain 2, 18.
111. Murase S, Mosser E, &, Schuman EM, (2002) Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91-105.
112. Brigidi GS, &, Bamji SX, (2011) Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol 21, 208-214.
113. Lee SH, Peng IF, Ng YG, Yanagisawa M, Bamji SX, Elia LP, Balsamo J, Lilien J, Anastasiadis PZ, Ullian EM, et al.,. (2008) Synapses are regulated by the cytoplasmic tyrosine kinase Fer in a pathway mediated by p120catenin, Fer, SHP-2, and beta-catenin. J Cell Biol 183, 893-908.
114. 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.
115. 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.
116. Yoshida T, Yasumura M, Uemura T, Lee SJ, Ra M, Taguchi R, Iwakura Y, &, Mishina M, (2011) IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase delta. J Neurosci 31, 13485-13499.
117. Valnegri P, Montrasio C, Brambilla D, Ko J, Passafaro M, &, Sala C, (2011) The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTPdelta and RhoGAP2. Hum Mol Genet 20, 4797-4809.
118. 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.
119. Yamaguchi Y, (2002) Glycobiology of the synapse: the role of glycans in the formation, maturation, and modulation of synapses. Biochim Biophys Acta 1573, 369-376.
120. Yang T, Massa SM, &, Longo FM, (2006) LAR protein tyrosine phosphatase receptor associates with TrkB and modulates neurotrophic signaling pathways. J Neurobiol 66, 1420-1436.
121. Faux C, Hawadle M, Nixon J, Wallace A, Lee S, Murray S, &, Stoker A, (2007) PTPsigma binds and dephosphorylates neurotrophin receptors and can suppress NGF-dependent neurite outgrowth from sensory neurons. Biochim Biophys Acta 1773, 1689-1700.
122. Niisato K, Fujikawa A, Komai S, Shintani T, Watanabe E, Sakaguchi G, Katsuura G, Manabe T, &, Noda M, (2005) Age-dependent enhancement of hippocampal long-term potentiation and impairment of spatial learning through the Rho-associated kinase pathway in protein tyrosine phosphatase receptor type Z-deficient mice. J Neurosci 25, 1081-1088.
123. Santos SD, Carvalho AL, Caldeira MV, &, Duarte CB, (2009) Regulation of AMPA receptors and synaptic plasticity. Neuroscience 158, 105-125.
124. Moult PR, Gladding CM, Sanderson TM, Fitzjohn SM, Bashir ZI, Molnar E, &, Collingridge GL, (2006) Tyrosine phosphatases regulate AMPA receptor trafficking during metabotropic glutamate receptor-mediated long-term depression. J Neurosci 26, 2544-2554.
125. Gladding CM, Collett VJ, Jia Z, Bashir ZI, Collingridge GL, &, Molnar E, (2009) Tyrosine dephosphorylation regulates AMPAR internalisation in mGluR-LTD. Mol Cell Neurosci 40, 267-279.
126. Hayashi T, &, Huganir RL, (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J Neurosci 24, 6152-6160.
127. Zhang Y, Venkitaramani DV, Gladding CM, Kurup P, Molnar E, Collingridge GL, &, Lombroso PJ, (2008) The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J Neurosci 28, 10561-10566.
128. Prybylowski K, Chang K, Sans N, Kan L, Vicini S, &, Wenthold RJ, (2005) The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron, 47, 845-857.
129. Braithwaite SP, Paul S, Nairn AC, &, Lombroso PJ, (2006) Synaptic plasticity: one STEP at a time. Trends Neurosci 29, 452-458.
130. Lei G, Xue S, Chery N, Liu Q, Xu J, Kwan CL, Fu YP, Lu YM, Liu M, Harder KW, et al.,. (2002) Gain control of N-methyl- d -aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha. EMBO J 21, 2977-2989.
131. Le HT, Maksumova L, Wang J, &, Pallen CJ, (2006) Reduced NMDA receptor tyrosine phosphorylation in PTPalpha-deficient mouse synaptosomes is accompanied by inhibition of four src family kinases and Pyk2: an upstream role for PTPalpha in NMDA receptor regulation. J Neurochem 98, 1798-1809.
132. Harroch S, Furtado GC, Brueck W, Rosenbluth J, Lafaille J, Chao M, Buxbaum JD, &, Schlessinger J, (2002) A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat Genet 32, 411-414.
133. 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.
134. Ottervald J, Franzen B, Nilsson K, Andersson LI, Khademi M, Eriksson B, Kjellstrom S, Marko-Varga G, Vegvari A, Harris RA, et al.,. (2010) Multiple sclerosis: identification and clinical evaluation of novel CSF biomarkers. J Proteomics 73, 1117-1132.
135. Susumu K, Hiromi A, Jyoji M, &, Shogo O, (2010) Anti-phosphacan antibody in CIDP. J Neuroimmunol 228, 179.
136. Jacobsen M, Schweer D, Ziegler A, Gaber R, Schock S, Schwinzer R, Wonigeit K, Lindert RB, Kantarci O, Schaefer-Klein J, et al.,. (2000) A point mutation in PTPRC is associated with the development of multiple sclerosis. Nat Genet 26, 495-499.
137. Nakahara J, Seiwa C, Tan-Takeuchi K, Gotoh M, Kishihara K, Ogawa M, Asou H, &, Aiso S, (2005) Involvement of CD45 in central nervous system myelination. Neurosci Lett 379, 116-121.
138. Cohen S, Shoshana O, Zelman-Toiste E, Maharshak N, Binsky- Ehrenreich I, Gordin M, Shvidel L, Haran M, Leng L, Bucala R, et al.,. (2012) The cytokine midkine and its receptor RPTPζ regulate B cell survival in a pathway induced by CD74. J Immunol 188, 259-269.
139. Himburg HA, Muramoto GG, Daher P, Meadows SK, Russell JL, Doan P, Chi JT, Salter AB, Lento WE, Reya T, et al.,. (2010) Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat Med 16, 475-482.
140. Hermiston ML, Zikherman J, Tan AL, Lam VC, Cresalia NM, Oksenberg N, Goren N, Brassat D, Oksenberg JR, &, Weiss A, (2009) Differential impact of the CD45 juxtamembrane wedge on central and peripheral T cell receptor responses. Proc Natl Acad Sci USA 106, 546-551.
141. Liu X, Li Y, Zhang Y, Lu Y, Guo W, Liu P, Zhou J, Xiang Z, &, He C, (2011) SHP-2 promotes the maturation of oligodendrocyte precursor cells through Akt and ERK1/2 signaling in vitro. PLoS One 6, e21058.
142. Domercq M, Alberdi E, Sanchez-Gomez MV, Ariz U, Perez-Samartin A, &, Matute C, (2011) Dual-specific phosphatase-6 (Dusp6) and ERK mediate AMPA receptor-induced oligodendrocyte death. J Biol Chem 286, 11825-11836.
143. Fujita Y, Endo S, Takai T, &, Yamashita T, (2011) Myelin suppresses axon regeneration by PIR-B/SHP-mediated inhibition of Trk activity. EMBO J 30, 1389-1401.
144. Ferrario JE, Rojas-Mayorquin AE, Saldana-Ortega M, Salum C, Gomes MZ, Hunot S, &, Raisman-Vozari R, (2008) Pleiotrophin receptor RPTP-zeta/beta expression is up-regulated by L-DOPA in striatal medium spiny neurons of parkinsonian rats. J Neurochem 107, 443-452.
145. Marchionini DM, Lehrmann E, Chu Y, He B, Sortwell CE, Becker KG, Freed WJ, Kordower JH, &, Collier TJ, (2007) Role of heparin binding growth factors in nigrostriatal dopamine system development and Parkinson's disease. Brain Res 1147, 77-88.
146. Herradon G, &, Ezquerra L, (2009) Blocking receptor protein tyrosine phosphatase beta/zeta: a potential therapeutic strategy for Parkinson's disease. Curr Med Chem 16, 3322-3329.
147. Fitzpatrick CJ, &, Lombroso PJ, (2011) The role of striatal-enriched protein tyrosine phosphatase (STEP) in cognition. Front Neuroanat 5, 47.
148. Goebel-Goody SM, Baum M, Paspalas CD, Fernandez SM, Carty NC, Kurup P, &, Lombroso PJ, (2012) Therapeutic implications for striatal-enriched protein tyrosine Phosphatase (STEP) in neuropsychiatric disorders. Pharmacol Rev 64, 65-87.
149. Shi C, Zhang K, &, Xu Q, (2012) Gender-specific role of the protein tyrosine phosphatase receptor type R gene in major depressive disorder. J Affect Disord 136, 591-598.
150. Shi J, Potash JB, Knowles JA, Weissman MM, Coryell W, Scheftner WA, Lawson WB, DePaulo JR Jr, Gejman PV, Sanders AR, et al.,. (2011) Genome-wide association study of recurrent early-onset major depressive disorder. Mol Psychiatry 16, 193-201.
151. Lamprianou S, &, Harroch S, (2006) Receptor protein tyrosine phosphatase from stem cells to mature glial cells of the central nervous system. J Mol Neurosci 29, 241-255.
152. Bouyain S, &, Watkins DJ, (2010) Identification of tyrosine phosphatase ligands for contactin cell adhesion molecules. Commun Integr Biol 3, 284-286.
153. 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.
154. Hamshere ML, Green EK, Jones IR, Jones L, Moskvina V, Kirov G, Grozeva D, Nikolov I, Vukcevic D, Caesar S, et al.,. (2009) Genetic utility of broadly defined bipolar schizoaffective disorder as a diagnostic concept. Br J Psychiatry 195, 23-29.
155. Karege F, Perroud N, Burkhardt S, Fernandez R, Ballmann E, La Harpe R, &, Malafosse A, (2011) Alterations in phosphatidylinositol 3-kinase activity and PTEN phosphatase in the prefrontal cortex of depressed suicide victims. Neuropsychobiology 63, 224-231.
156. Thalmeier A, Dickmann M, Giegling I, Schneider B, Hartmann MA, Maurer K,
157. Muglia P, Tozzi F, Galwey NW, Francks C, Upmanyu R, Kong XQ, Antoniades A, Domenici E, Perry J, Rothen S, et al.,. (2010) Genome-wide association study of recurrent major depressive disorder in two European case-control cohorts. Mol Psychiatry 15, 589-601.
158. Joslyn G, Ravindranathan A, Brush G, Schuckit M, &, White RL, (2010) Human variation in alcohol response is influenced by variation in neuronal signaling genes. Alcohol Clin Exp Res 34, 800-812.
159. Cottrell CE, Bir N, Varga E, Alvarez CE, Bouyain S, Zernzach R, Thrush DL, Evans J, Trimarchi M, Butter EM, et al.,. (2011) Contactin 4 as an autism susceptibility locus. Autism Res 4, 189-199.
160. Fernandez T, Morgan T, Davis N, Klin A, Morris A, Farhi A, Lifton RP, &, State MW, (2008) Disruption of Contactin 4 (CNTN4) results in developmental delay and other features of 3p deletion syndrome. Am J Hum Genet 82, 1385.