Encyclopedia of Signaling Molecules

2018 Edition
| Editors: Sangdun Choi

Striatal-Enriched Protein-Tyrosine Phosphatase (STEP)

  • Pradeep Kurup
  • Jian Xu
  • Manavi Chatterjee
  • Susan Goebel-Goody
  • Surojit Paul
  • Paul Lombroso
Reference work entry
DOI: https://doi.org/10.1007/978-3-319-67199-4_630

Synonyms

Historical Background

Protein-tyrosine phosphatases (PTPs) play a significant role in diverse signaling mechanisms ranging from cellular differentiation to synaptic plasticity (Paul and Lombroso 2003; Tonks 2006). STriatal-Enriched protein-tyrosine Phosphatase (STEP) is a brain-specific protein tyrosine phosphatase belonging to the non-receptor tyrosine phosphatase family. Although enriched in the striatum, it is also localized to neurons in the cortex, hippocampus, and related brain regions (Boulanger et al. 1995). Interestingly, it is absent in the cerebellum, where a highly related PTP, PTP-STEP-like, is present (Watanabe et al. 1998). STEP exists as two major isoforms, named after their mobility in SDS-PAGE and designated STEP61and...

This is a preview of subscription content, log in to check access.

References

  1. Barsacchi R, Heider H, Girault JA, Meldolesi J. Requirement of Pyk2 for the activation of the MAP kinase cascade induced by Ca2+ (but not by PKC or G protein) in PC12 cells. Febs Lett. 1999;461(3):273–6.  https://doi.org/10.1016/S0014-5793(99)01468-4.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baum ML, Kurup P, Xu J, Lombroso PJ. A STEP forward in neural function and degeneration. Commun Integr Biol. 2010;3(5):419–22.  https://doi.org/10.4161/cib.3.5.12692.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004;27(7):370–7.  https://doi.org/10.1016/j.tins.2004.04.009.CrossRefGoogle Scholar
  4. Ben Hamida S, Darcq E, Wang J, Wu S, Phamluong K, Kharazia V, Ron D. Protein tyrosine phosphatase alpha in the dorsomedial striatum promotes excessive ethanol-drinking behaviors. J Neurosci. 2013;33(36):14369–78.  https://doi.org/10.1523/jneurosci.1954-13.2013.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bingol B, Sheng M. Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron. 2011;69(1):22–32.  https://doi.org/10.1016/j.neuron.2010.11.006.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boulanger LM, Lombroso PJ, Raghunathan A, During MJ, Wahle P, Naegele JR. Cellular and molecular characterization of a brain-enriched protein tyrosine phosphatase. J Neurosci. 1995;15(2):1532–44.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Braithwaite SP, Adkisson M, Leung J, Nava A, Masterson B, Urfer R, Oksenberg D, Nikolich K. Regulation of NMDA receptor trafficking and function by striatal-enriched tyrosine phosphatase (STEP). Eur J Neurosci. 2006;23(11):2847–56.  https://doi.org/10.1111/j.1460-9568.2006.04837.x.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Briggs SW, Walker J, Asik K, Lombroso P, Naegele J, Aaron G. STEP regulation of seizure thresholds in the hippocampus. Epilepsia. 2011;52(3):497–506.  https://doi.org/10.1111/j.1528-1167.2010.02912.x.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bult A, Zhao F, Dirkx Jr R, Raghunathan A, Solimena M, Lombroso PJ. STEP: a family of brain-enriched PTPs. Alternative splicing produces transmembrane, cytosolic and truncated isoforms. Eur J Cell Biol. 1997;72(4):337–44.PubMedPubMedCentralGoogle Scholar
  10. Chin J, Palop JJ, Puolivali J, Massaro C, Bien-Ly N, Gerstein H, Scearce-Levie K, Masliah E, Mucke L. Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J Neurosci. 2005;25(42):9694–703.  https://doi.org/10.1523/JNEUROSCI.2980-05.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Choi YS, Lin SL, Lee B, Kurup P, Cho HY, Naegele JR, Lombroso PJ, Obrietan K. Status epilepticus-induced somatostatinergic hilar interneuron degeneration is regulated by striatal enriched protein tyrosine phosphatase. J Neurosci. 2007;27(11):2999–3009.  https://doi.org/10.1523/JNEUROSCI.4913-06.2007.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell. 2011;146(2):247–61.  https://doi.org/10.1016/j.cell.2011.06.013.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Deb I, Poddar R, Paul S. Oxidative stress-induced oligomerization inhibits the activity of the non-receptor tyrosine phosphatase STEP61. J Neurochem. 2011;116(6):1097–111.  https://doi.org/10.1111/j.1471-4159.2010.07165.x.CrossRefPubMedPubMedCentralGoogle Scholar
  14. den Hertog J, Tracy S, Hunter T. Phosphorylation of receptor protein-tyrosine phosphatase alpha on Tyr789, a binding site for the SH3-SH2-SH3 adaptor protein GRB-2 in vivo. EMBO J. 1994;13(13):3020–32.CrossRefGoogle Scholar
  15. den Hertog J, Ostman A, Bohmer FD. Protein tyrosine phosphatases: regulatory mechanisms. FEBS J. 2008;275(5):831–47.  https://doi.org/10.1111/j.1742-4658.2008.06247.x.CrossRefGoogle Scholar
  16. Doshi S, Lynch DR. Calpain and the glutamatergic synapse. Front Biosci (Schol Ed). 2009;1:466–76.CrossRefGoogle Scholar
  17. Dunah AW, Sirianni AC, Fienberg AA, Bastia E, Schwarzschild MA, Standaert DG. Dopamine D1-dependent trafficking of striatal N-methyl-D-aspartate glutamate receptors requires Fyn protein tyrosine kinase but not DARPP-32. Mol Pharmacol. 2004;65(1):121–9.  https://doi.org/10.1124/mol.65.1.121.CrossRefPubMedGoogle Scholar
  18. Elder GA, Gama Sosa MA, De Gasperi R. Transgenic mouse models of Alzheimer's disease. Mt Sinai J Med. 2010;77(1):69–81.  https://doi.org/10.1002/msj.20159.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Engen JR, Wales TE, Hochrein JM, Meyn 3rd MA, Banu Ozkan S, Bahar I, Smithgall TE. Structure and dynamic regulation of Src-family kinases. Cell Mol Life Sci. 2008;65(19):3058–73.  https://doi.org/10.1007/s00018-008-8122-2.CrossRefPubMedGoogle Scholar
  20. Gibb SL, Hamida SB, Lanfranco MF, Ron D. Ethanol-induced increase in Fyn kinase activity in the dorsomedial striatum is associated with subcellular redistribution of protein tyrosine phosphatase alpha. J Neurochem. 2011;119(4):879–89.  https://doi.org/10.1111/j.1471-4159.2011.07485.x.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Girault JA, Costa A, Derkinderen P, Studler JM, Toutant M. FAK and PYK2/CAK beta in the nervous system: a link between neuronal activity, plasticity and survival? Trends Neurosci. 1999;22(6):257–63.  https://doi.org/10.1016/S0166-2236(98)01358-7.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goebel-Goody SM, Davies KD, Alvestad Linger RM, Freund RK, Browning MD. Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices. Neuroscience. 2009;158(4):1446–59.  https://doi.org/10.1016/j.neuroscience.2008.11.006.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Goebel-Goody SM, Baum M, Paspalas CD, Fernandez SM, Carty NC, Kurup P, Lombroso PJ. Therapeutic implications for striatal-enriched protein tyrosine phosphatase (STEP) in neuropsychiatric disorders. Pharmacological Reviews. 2012a;64(1):65–87.  https://doi.org/10.1124/pr.110.003053.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Goebel-Goody SM, Wilson-Wallis ED, Royston S, Tagliatela SM, Naegele JR, Lombroso PJ. Genetic manipulation of STEP reverses behavioral abnormalities in a fragile X syndrome mouse model. Genes Brain, Behav. 2012b;11(5):586–600.  https://doi.org/10.1111/j.1601-183X.2012.00781.x.CrossRefGoogle Scholar
  25. Grosshans DR, Clayton DA, Coultrap SJ, Browning MD. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat Neurosci. 2002;5(1):27–33.  https://doi.org/10.1038/nn779.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Haas KF, Broadie K. Roles of ubiquitination at the synapse. Biochim Biophys Acta. 2008;1779(8):495–506.  https://doi.org/10.1016/j.bbagrm.2007.12.010.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hardingham GE, Bading H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 2003;26(2):81–9.  https://doi.org/10.1016/S0166-2236(02)00040-1.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci. 2002;5(5):405–14.  https://doi.org/10.1038/nn835.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ingley E. Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim Biophys Acta. 2008;1784(1):56–65.  https://doi.org/10.1016/j.bbapap.2007.08.012.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jayaseelan S, Tenenbaum SA. Neurodevelopmental disorders: signalling pathways of fragile X syndrome. Nature. 2012;492(7429):359–60.  https://doi.org/10.1038/nature11764.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kamceva M, Benedict J, Nairn AC, Lombroso PJ. Role of striatal-enriched tyrosine phosphatase in neuronal function. Neural Plast. 2016;Artn8136925.  https://doi.org/10.1155/2016/8136925.
  32. Keshet Y, Seger R. The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions. Methods Mol Biol. 2010;661:3–38.  https://doi.org/10.1007/978-1-60761-795-2_1.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kurup P, Zhang Y, Venkitaramani DV, Xu J, Lombroso PJ. The role of STEP in Alzheimer’s disease. Channels (Austin). 2010a;4(5):347–50.  https://doi.org/10.1523/JNEUROSCI.0157-10.2010.CrossRefGoogle Scholar
  34. Kurup P, Zhang Y, Xu J, Venkitaramani DV, Haroutunian V, Greengard P, Nairn AC, Lombroso PJ. Abeta-mediated NMDA receptor endocytosis in Alzheimer’s disease involves ubiquitination of the tyrosine phosphatase STEP61. J Neurosci. 2010b;30(17):5948–57.  https://doi.org/10.1523/JNEUROSCI.0157-10.2010.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kurup PK, Xu J, Videira RA, Ononenyi C, Baltazar G, Lombroso PJ, Nairn AC. STEP61 is a substrate of the E3 ligase parkin and is upregulated in Parkinson's disease. P Natl Acad Sci USA. 2015;112(4):1202–7.  https://doi.org/10.1073/pnas.1417423112.CrossRefGoogle Scholar
  36. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U. Evidence that fragile X mental retardation protein is a negative regulator of translation. Human Mol Genet. 2001;10(4):329–38.CrossRefGoogle Scholar
  37. Lam YA, Pickart CM, Alban A, Landon M, Jamieson C, Ramage R, Mayer RJ, Layfield R. Inhibition of the ubiquitin-proteasome system in Alzheimer’s disease. Proc Natl Acad Sci U S A. 2000;97(18):9902–6.  https://doi.org/10.1073/pnas.170173897.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lau CG, Zukin RS. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci. 2007;8(6):413–26.  https://doi.org/10.1038/nrn2153.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Legastelois R, Darcq E, Wegner SA, Lombroso PJ, Ron D. Striatal-enriched protein tyrosine phosphatase controls responses to aversive stimuli: implication for ethanol drinking. PLoS One. 2015;10(5):e0127408.  https://doi.org/10.1371/journal.pone.0127408.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lev S, Moreno H, Martinez R, Canoll P, Peles E, Musacchio JM, Plowman GD, Rudy B, Schlessinger J. Protein-tyrosine kinase Pyk2 involved in Ca2+-induced regulation of ion-channel and MAP kinase functions. Nature. 1995;376(6543):737–45.  https://doi.org/10.1038/376737a0.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lombroso PJ, Murdoch G, Lerner M. Molecular characterization of a protein-tyrosine-phosphatase enriched in striatum. Proc Natl Acad Sci U S A. 1991;88(16):7242–6.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Lombroso PJ, Naegele JR, Sharma E, Lerner M. A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures. J Neurosci. 1993;13(7):3064–74.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Maksumova L, Le HT, Muratkhodjaev F, Davidson D, Veillette A, Pallen CJ. Protein tyrosine phosphatase alpha regulates Fyn activity and Cbp/PAG phosphorylation in thymocyte lipid rafts. J Immunol. 2005;175(12):7947–56.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Mori H, Kondo J, Ihara Y. Ubiquitin is a component of paired helical filaments in Alzheimer’s disease. Science. 1987;235(4796):1641–4.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Munoz JJ, Tarrega C, Blanco-Aparicio C, Pulido R. Differential interaction of the tyrosine phosphatases PTP-SL, STEP and HePTP with the mitogen-activated protein kinases ERK1/2 and p38alpha is determined by a kinase specificity sequence and influenced by reducing agents. Biochem J. 2003;372(Pt 1):193–201.  https://doi.org/10.1042/BJ20021941.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, Yamamoto T. Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem. 2001;276(1):693–9.  https://doi.org/10.1074/jbc.M008085200.CrossRefPubMedGoogle Scholar
  47. Nguyen TH, Paul S, Xu Y, Gurd JW, Lombroso PJ. Calcium-dependent cleavage of striatal enriched tyrosine phosphatase (STEP). J Neurochem. 1999;73(5):1995–2001.PubMedPubMedCentralGoogle Scholar
  48. Nguyen TH, Liu J, Lombroso PJ. Striatal enriched phosphatase 61 dephosphorylates Fyn at phosphotyrosine 420. J Biol Chem. 2002;277(27):24274–9.  https://doi.org/10.1074/jbc.M111683200.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Oyama T, Goto S, Nishi T, Sato K, Yamada K, Yoshikawa M, Ushio Y. Immunocytochemical localization of the striatal enriched protein tyrosine phosphatase in the rat striatum: a light and electron microscopic study with a complementary DNA-generated polyclonal antibody. Neuroscience. 1995;69(3):869–80.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Paoletti P, Neyton J. NMDA receptor subunits: function and pharmacology. Curr Opin Pharmacol. 2007;7(1):39–47.  https://doi.org/10.1016/j.coph.2006.08.011.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Paul S, Connor JA. NR2B-NMDA receptor-mediated increases in intracellular Ca2+ concentration regulate the tyrosine phosphatase, STEP, and ERK MAP kinase signaling. J Neurochem. 2010;114(4):1107–18.  https://doi.org/10.1111/j.1471-4159.2010.06835.x.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Paul S, Lombroso PJ. Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci. 2003;60(11):2465–82.  https://doi.org/10.1007/s00018-003-3123-7.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Paul S, Snyder GL, Yokakura H, Picciotto MR, Nairn AC, Lombroso PJ. The Dopamine/D1 receptor mediates the phosphorylation and inactivation of the protein tyrosine phosphatase STEP via a PKA-dependent pathway. J Neurosci. 2000;20(15):5630–8.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Paul S, Nairn AC, Wang P, Lombroso PJ. NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat Neurosci. 2003;6(1):34–42.  https://doi.org/10.1038/nn989.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Paul S, Olausson P, Venkitaramani DV, Ruchkina I, Moran TD, Tronson N, Mills E, Hakim S, Salter MW, Taylor JR, Lombroso PJ. The striatal-enriched protein tyrosine phosphatase gates long-term potentiation and fear memory in the lateral amygdala. Biol Psychiatry. 2007;61(9):1049–61.  https://doi.org/10.1016/j.biopsych.2006.08.005.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pelkey KA, Askalan R, Paul S, Kalia LV, Nguyen TH, Pitcher GM, Salter MW, Lombroso PJ. Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation. Neuron. 2002;34(1):127–38.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Peng S, Zhang Y, Zhang J, Wang H, Ren B. Glutamate receptors and signal transduction in learning and memory. Mol Biol Rep. 2011;38(1):453–60.  https://doi.org/10.1007/s11033-010-0128-9.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Petrone A, Battaglia F, Wang C, Dusa A, Su J, Zagzag D, Bianchi R, Casaccia-Bonnefil P, Arancio O, Sap J. Receptor protein tyrosine phosphatase alpha is essential for hippocampal neuronal migration and long-term potentiation. EMBO J. 2003;22(16):4121–31.  https://doi.org/10.1093/emboj/cdg399.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Poddar R, Deb I, Mukherjee S, Paul S. NR2B-NMDA receptor mediated modulation of the tyrosine phosphatase STEP regulates glutamate induced neuronal cell death. J Neurochem. 2010;115(6):1350–62.  https://doi.org/10.1111/j.1471-4159.2010.07035.x.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pulido R, Zuniga A, Ullrich A. PTP-SL and STEP protein tyrosine phosphatases regulate the activation of the extracellular signal-regulated kinases ERK1 and ERK2 by association through a kinase interaction motif. EMBO J. 1998;17(24):7337–50.  https://doi.org/10.1093/emboj/17.24.7337.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Rajagopal S, Deb I, Poddar R, Paul S. Aging is associated with dimerization and inactivation of the brain-enriched tyrosine phosphatase STEP. Neurobiol Aging. 2016;41:25–38.  https://doi.org/10.1016/j.neurobiolaging.2016.02.004.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ. Molecular determinants of NMDA receptor internalization. Nat Neurosci. 2001;4(8):794–802.  https://doi.org/10.1038/90498.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sahin M, Dowling JJ, Hockfield S. Seven protein tyrosine phosphatases are differentially expressed in the developing rat brain. J Comp Neurol. 1995;351(4):617–31.  https://doi.org/10.1002/cne.903510410.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Saiki S, Sato S, Hattori N. Molecular pathogenesis of Parkinson’s disease: update. Journal of Neurol Neurosurg Psychiatry. 2012;83(4):430–6.  https://doi.org/10.1136/jnnp-2011-301205.CrossRefGoogle Scholar
  65. Sap J, D'Eustachio P, Givol D, Schlessinger J. Cloning and expression of a widely expressed receptor tyrosine phosphatase. Proc Natl Acad Sci U S A. 1990;87(16):6112–6.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Selkoe DJ. Alzheimer’s disease is a synaptic failure. Science. 2002;298(5594):789–91.  https://doi.org/10.1126/science.1074069.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sharma E, Zhao F, Bult A, Lombroso PJ. Identification of two alternatively spliced transcripts of STEP: a subfamily of brain-enriched protein tyrosine phosphatases. Brain Res Mol Brain Res. 1995;32(1):87–93.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Skelton MR, Ponniah S, Wang DZ, Doetschman T, Vorhees CV, Pallen CJ. Protein tyrosine phosphatase alpha (PTP alpha) knockout mice show deficits in Morris water maze learning, decreased locomotor activity, and decreases in anxiety. Brain Res. 2003;984(1-2):1–10.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, Nairn AC, Salter MW, Lombroso PJ, Gouras GK, Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci. 2005;8(8):1051–8.  https://doi.org/10.1038/nn1503.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sweatt JD. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem. 2001;76(1):1–10.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol. 2006;7(11):833–46.  https://doi.org/10.1038/nrm2039.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Turner PR, O'Connor K, Tate WP, Abraham WC. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol. 2003;70(1):1–32.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC, Stipanovich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve D, Girault JA. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci U S A. 2005;102(2):491–6.  https://doi.org/10.1073/pnas.0408305102.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Venkitaramani DV, Paul S, Zhang Y, Kurup P, Ding L, Tressler L, Allen M, Sacca R, Picciotto MR, Lombroso PJ. Knockout of striatal enriched protein tyrosine phosphatase in mice results in increased ERK1/2 phosphorylation. Synapse. 2009;63(1):69–81.  https://doi.org/10.1002/syn.20608.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Venkitaramani DV, Moura PJ, Picciotto MR, Lombroso PJ. Striatal-enriched protein tyrosine phosphatase (STEP) knockout mice have enhanced hippocampal memory. Eur J Neurosci. 2011;33(12):2288–98.  https://doi.org/10.1111/j.1460-9568.2011.07687.x.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang J, Carnicella S, Phamluong K, Jeanblanc J, Ronesi JA, Chaudhri N, Janak PH, Lovinger DM, Ron D. Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: implications for alcohol drinking behavior. J Neurosci. 2007;27(13):3593–602.  https://doi.org/10.1523/jneurosci.4749-06.2007.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Wang DO, Martin KC, Zukin RS. Spatially restricting gene expression by local translation at synapses. Trends Neurosci. 2010;33(4):173–82.  https://doi.org/10.1016/j.tins.2010.01.005.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Watanabe Y, Shiozuka K, Ikeda T, Hoshi N, Hiraki H, Suzuki T, Hashimoto S, Kawashima H. Cloning of PCPTP1-Ce encoding protein tyrosine phosphatase from the rat cerebellum and its restricted expression in Purkinje cells. Brain Res Mol Brain Res. 1998;58(1-2):83–94.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Waung MW, Huber KM. Protein translation in synaptic plasticity: mGluR-LTD, Fragile X. Curr Opin Neurobiol. 2009;19(3):319–26.  https://doi.org/10.1016/j.conb.2009.03.011.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Xu J, Kurup P, Zhang Y, Goebel-Goody SM, Wu PH, Hawasli AH, Baum ML, Bibb JA, Lombroso PJ. Extrasynaptic NMDA receptors couple preferentially to excitotoxicity via calpain-mediated cleavage of STEP. J Neurosci. 2009;29(29):9330–43.  https://doi.org/10.1523/JNEUROSCI.2212-09.2009.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Xu J, Kurup P, Bartos JA, Patriarchi T, Hell JW, Lombroso PJ. Striatal-enriched protein-tyrosine phosphatase (STEP) regulates Pyk2 kinase activity. J Biol Chem. 2012;287(25):20942–56.  https://doi.org/10.1074/jbc.M112.368654.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Xu J, Chatterjee M, Baguley TD, Brouillette J, Kurup P, Ghosh D, Kanyo J, Zhang Y, Seyb K, Ononenyi C, Foscue E, Anderson GM, Gresack J, Cuny GD, Glicksman MA, Greengard P, Lam TT, Tautz L, Nairn AC, Ellman JA, Lombroso PJ. Inhibitor of the tyrosine phosphatase STEP reverses cognitive deficits in a mouse model of Alzheimer's disease. PLoS Biol. 2014;12(8):e1001923.  https://doi.org/10.1371/journal.pbio.1001923.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Xu J, Kurup P, Foscue E, Lombroso PJ. Striatal-enriched protein tyrosine phosphatase regulates the PTPalpha/Fyn signaling pathway. J Neurochem. 2015;134(4):629–41.  https://doi.org/10.1111/jnc.13160.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Xu J, Kurup P, Azkona G, Baguley TD, Saavedra A, Nairn AC, Ellman JA, Perez-Navarro E, Lombroso PJ. Down-regulation of BDNF in cell and animal models increases striatal-enriched protein tyrosine phosphatase 61 (STEP61) levels. Journal of Neurochem. 2016a;136(2):285–94.  https://doi.org/10.1111/jnc.13295.CrossRefGoogle Scholar
  85. Xu J, Kurup P, Baguley TD, Foscue E, Ellman JA, Nairn AC, Lombroso PJ. Inhibition of the tyrosine phosphatase STEP61 restores BDNF expression and reverses motor and cognitive deficits in phencyclidine-treated mice. Cell Mol Life Sci. 2016b;73(7):1503–14.  https://doi.org/10.1007/s00018-015-2057-1.CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yi JJ, Ehlers MD. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol Rev. 2007;59(1):14–39.  https://doi.org/10.1124/pr.59.1.4.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Yoshii A, Constantine-Paton M. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol. 2010;70(5):304–22.  https://doi.org/10.1002/dneu.20765.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zhang Y, Venkitaramani DV, Gladding CM, Zhang Y, Kurup P, Molnar E, Collingridge GL, Lombroso PJ. The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J Neurosci. 2008;28(42):10561–6.  https://doi.org/10.1523/JNEUROSCI.2666-08.2008.CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zhang Y, Kurup P, Xu J, Carty N, Fernandez SM, Nygaard HB, Pittenger C, Greengard P, Strittmatter SM, Nairn AC, Lombroso PJ. Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer’s disease mouse model. Proc Natl Acad Sci U S A. 2010;107(44):19014–9.  https://doi.org/10.1073/pnas.1013543107.CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zheng XM, Resnick RJ, Shalloway D. A phosphotyrosine displacement mechanism for activation of Src by PTPalpha. EMBO J. 2000;19(5):964–78.  https://doi.org/10.1093/emboj/19.5.964.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Pradeep Kurup
    • 1
  • Jian Xu
    • 1
  • Manavi Chatterjee
    • 1
  • Susan Goebel-Goody
    • 1
  • Surojit Paul
    • 1
    • 2
  • Paul Lombroso
    • 1
  1. 1.Child Study CenterYale University, School of MedicineNew HavenUSA
  2. 2.NeurologyUniversity of New Mexico Health Sciences CenterAlbuquerqueUSA