Literature DB >> 26316048

Down-regulation of BDNF in cell and animal models increases striatal-enriched protein tyrosine phosphatase 61 (STEP61 ) levels.

Jian Xu1, Pradeep Kurup1, Garikoitz Azkona2,3,4, Tyler D Baguley5, Ana Saavedra2,3,4, Angus C Nairn1, Jonathan A Ellman5, Esther Pérez-Navarro2,3,4, Paul J Lombroso1.   

Abstract

Brain-derived neurotrophic factor (BDNF) regulates synaptic strengthening and memory consolidation, and altered BDNF expression is implicated in a number of neuropsychiatric and neurodegenerative disorders. BDNF potentiates N-methyl-D-aspartate receptor function through activation of Fyn and ERK1/2. STriatal-Enriched protein tyrosine Phosphatase (STEP) is also implicated in many of the same disorders as BDNF but, in contrast to BDNF, STEP opposes the development of synaptic strengthening. STEP-mediated dephosphorylation of the NMDA receptor subunit GluN2B promotes internalization of GluN2B-containing NMDA receptors, while dephosphorylation of the kinases Fyn, Pyk2, and ERK1/2 leads to their inactivation. Thus, STEP and BDNF have opposing functions. In this study, we demonstrate that manipulation of BDNF expression has a reciprocal effect on STEP61 levels. Reduced BDNF signaling leads to elevation of STEP61 both in BDNF(+/-) mice and after acute BDNF knockdown in cortical cultures. Moreover, a newly identified STEP inhibitor reverses the biochemical and motor abnormalities in BDNF(+/-) mice. In contrast, increased BDNF signaling upon treatment with a tropomyosin receptor kinase B agonist results in degradation of STEP61 and a subsequent increase in the tyrosine phosphorylation of STEP substrates in cultured neurons and in mouse frontal cortex. These findings indicate that BDNF-tropomyosin receptor kinase B signaling leads to degradation of STEP61 , while decreased BDNF expression results in increased STEP61 activity. A better understanding of the opposing interaction between STEP and BDNF in normal cognitive functions and in neuropsychiatric disorders will hopefully lead to better therapeutic strategies. Altered expression of BDNF and STEP61 has been implicated in several neurological disorders. BDNF and STEP61 are known to regulate synaptic strengthening, but in opposite directions. Here, we report that reduced BDNF signaling leads to elevation of STEP61 both in BDNF(+/-) mice and after acute BDNF knockdown in cortical cultures. In contrast, activation of TrkB receptor results in the degradation of STEP61 and reverses hyperlocomotor activity in BDNF(+/-) mice. Moreover, inhibition of STEP61 by TC-2153 is sufficient to enhance the Tyr phosphorylation of STEP substrates and also reverses hyperlocomotion in BDNF(+/-) mice. These findings give us a better understanding of the regulation of STEP61 by BDNF in normal cognitive functions and in neuropsychiatric disorders.
© 2015 International Society for Neurochemistry.

Entities:  

Keywords:  STEP; STEP inhibitor; TrkB agonist; brain-derived neurotrophic factor; locomotor activity; ubiquitination

Mesh:

Substances:

Year:  2015        PMID: 26316048      PMCID: PMC4769989          DOI: 10.1111/jnc.13295

Source DB:  PubMed          Journal:  J Neurochem        ISSN: 0022-3042            Impact factor:   5.372


  61 in total

1.  Molecular characterization of a protein-tyrosine-phosphatase enriched in striatum.

Authors:  P J Lombroso; G Murdoch; M Lerner
Journal:  Proc Natl Acad Sci U S A       Date:  1991-08-15       Impact factor: 11.205

Review 2.  Neurotrophins and schizophrenia.

Authors:  Peter F Buckley; Sahebarao Mahadik; Anilkumar Pillai; Alvin Terry
Journal:  Schizophr Res       Date:  2007-05-23       Impact factor: 4.939

Review 3.  Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease.

Authors:  Akira Yoshii; Martha Constantine-Paton
Journal:  Dev Neurobiol       Date:  2010-04       Impact factor: 3.964

4.  STEP61: a member of a family of brain-enriched PTPs is localized to the endoplasmic reticulum.

Authors:  A Bult; F Zhao; R Dirkx; E Sharma; E Lukacsi; M Solimena; J R Naegele; P J Lombroso
Journal:  J Neurosci       Date:  1996-12-15       Impact factor: 6.167

5.  A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures.

Authors:  P J Lombroso; J R Naegele; E Sharma; M Lerner
Journal:  J Neurosci       Date:  1993-07       Impact factor: 6.167

6.  Striatal-enriched protein tyrosine phosphatase regulates the PTPα/Fyn signaling pathway.

Authors:  Jian Xu; Pradeep Kurup; Ethan Foscue; Paul J Lombroso
Journal:  J Neurochem       Date:  2015-05-25       Impact factor: 5.372

7.  Brain-derived neurotrophic factor-tropomyosin-related kinase B signaling contributes to activity-dependent changes in synaptic proteins.

Authors:  Jie-Min Jia; Qian Chen; Yang Zhou; Sheng Miao; Jing Zheng; Chi Zhang; Zhi-Qi Xiong
Journal:  J Biol Chem       Date:  2008-05-12       Impact factor: 5.157

8.  Brain-derived neurotrophic factor modulates the severity of cognitive alterations induced by mutant huntingtin: involvement of phospholipaseCgamma activity and glutamate receptor expression.

Authors:  A Giralt; T Rodrigo; E D Martín; J R Gonzalez; M Milà; V Ceña; M Dierssen; J M Canals; J Alberch
Journal:  Neuroscience       Date:  2008-11-21       Impact factor: 3.590

9.  Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain.

Authors:  L A Mamounas; M E Blue; J A Siuciak; C A Altar
Journal:  J Neurosci       Date:  1995-12       Impact factor: 6.167

10.  7,8-Dihydroxyflavone, a small molecule TrkB agonist, improves spatial memory and increases thin spine density in a mouse model of Alzheimer disease-like neuronal loss.

Authors:  Nicholas A Castello; Michael H Nguyen; Jenny D Tran; David Cheng; Kim N Green; Frank M LaFerla
Journal:  PLoS One       Date:  2014-03-10       Impact factor: 3.240

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  7 in total

1.  Proteolytic Degradation of Hippocampal STEP61 in LTP and Learning.

Authors:  Ana Saavedra; Jesús J Ballesteros; Shiraz Tyebji; Sara Martínez-Torres; Gloria Blázquez; Rosa López-Hidalgo; Garikoitz Azkona; Jordi Alberch; Eduardo D Martín; Esther Pérez-Navarro
Journal:  Mol Neurobiol       Date:  2018-06-12       Impact factor: 5.590

2.  Disruption of Striatal-Enriched Protein Tyrosine Phosphatase Signaling Might Contribute to Memory Impairment in a Mouse Model of Sepsis-Associated Encephalopathy.

Authors:  Man-Man Zong; Hong-Mei Yuan; Xue He; Zhi-Qiang Zhou; Xiao-Dong Qiu; Jian-Jun Yang; Mu-Huo Ji
Journal:  Neurochem Res       Date:  2019-11-06       Impact factor: 3.996

3.  Synaptic NMDA Receptor Activation Induces Ubiquitination and Degradation of STEP61.

Authors:  Jian Xu; Pradeep Kurup; Angus C Nairn; Paul J Lombroso
Journal:  Mol Neurobiol       Date:  2017-05-02       Impact factor: 5.590

Review 4.  Targeting Tyrosine Phosphatases: Time to End the Stigma.

Authors:  Stephanie M Stanford; Nunzio Bottini
Journal:  Trends Pharmacol Sci       Date:  2017-04-12       Impact factor: 14.819

5.  Inhibition of striatal-enriched protein tyrosine phosphatase (STEP) activity reverses behavioral deficits in a rodent model of autism.

Authors:  Manavi Chatterjee; Priya Singh; Jian Xu; Paul J Lombroso; Pradeep K Kurup
Journal:  Behav Brain Res       Date:  2020-05-24       Impact factor: 3.332

Review 6.  Molecular underpinnings of neurodegenerative disorders: striatal-enriched protein tyrosine phosphatase signaling and synaptic plasticity.

Authors:  Paul J Lombroso; Marilee Ogren; Pradeep Kurup; Angus C Nairn
Journal:  F1000Res       Date:  2016-12-29

7.  Fbxo45-mediated NP-STEP46 degradation via K6-linked ubiquitination sustains ERK activity in lung cancer.

Authors:  Qian Wang; Ci Xu; Renjie Cai; Weishu An; Haihua Yuan; Ming Xu
Journal:  Mol Oncol       Date:  2022-08-05       Impact factor: 7.449

  7 in total

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