Xu Jian, Kurup Pradeep, Azkona Garikoitz, Baguley Tyler D, Saavedra Ana, Nairn Angus C, Ellman Jonathan A, Pérez-Navarro Esther, Lombroso Paul J
Yale University School of Medicine, New Haven, Connecticut, USA.
Departament de Biologia Cel·lular, Immunologia i Neurociències, Facultat de Medicina, Universitat de Barcelona, Barcelona, Spain.
J Neurochem. 2016 Jan;136(2):285-94. doi: 10.1111/jnc.13295. Epub 2015 Sep 17.
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.
脑源性神经营养因子(BDNF)调节突触增强和记忆巩固,BDNF表达的改变与多种神经精神疾病和神经退行性疾病有关。BDNF通过激活Fyn和ERK1/2增强N-甲基-D-天冬氨酸受体功能。富含纹状体的蛋白酪氨酸磷酸酶(STEP)也与许多与BDNF相同的疾病有关,但与BDNF相反,STEP会阻碍突触增强的发展。STEP介导的N-甲基-D-天冬氨酸受体亚基GluN2B的去磷酸化促进了含GluN2B的N-甲基-D-天冬氨酸受体的内化,而激酶Fyn、Pyk2和ERK1/2的去磷酸化导致它们失活。因此,STEP和BDNF具有相反的功能。在本研究中,我们证明操纵BDNF表达对STEP61水平有相反的影响。BDNF信号减少会导致BDNF(+/-)小鼠以及皮质培养物中急性敲低BDNF后STEP61水平升高。此外,一种新发现的STEP抑制剂可逆转BDNF(+/-)小鼠的生化和运动异常。相反,用原肌球蛋白受体激酶B激动剂处理后BDNF信号增加会导致STEP61降解,随后培养神经元和小鼠额叶皮质中STEP底物的酪氨酸磷酸化增加。这些发现表明BDNF-原肌球蛋白受体激酶B信号导致STEP61降解,而BDNF表达降低导致STEP61活性增加。更好地理解STEP和BDNF在正常认知功能和神经精神疾病中的相反相互作用有望带来更好的治疗策略。BDNF和STEP61表达的改变与几种神经系统疾病有关。已知BDNF和STEP61调节突触增强,但方向相反。在这里,我们报告BDNF信号减少会导致BDNF(+/-)小鼠以及皮质培养物中急性敲低BDNF后STEP61水平升高。相反,TrkB受体的激活导致STEP61降解,并逆转BDNF(+/-)小鼠的运动亢进。此外,TC-2153对STEP61的抑制足以增强STEP底物的酪氨酸磷酸化,也能逆转BDNF(+/-)小鼠的运动亢进。这些发现让我们更好地理解了BDNF在正常认知功能和神经精神疾病中对STEP61的调节。