Department of Molecular and Integrative Physiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
Neuroscience Graduate Program, University of Michigan Medical School, Ann Arbor, MI 48109, USA.
J Cell Sci. 2022 Feb 1;135(3). doi: 10.1242/jcs.259179. Epub 2022 Feb 10.
The adapter protein SH2B1 is recruited to neurotrophin receptors, including TrkB (also known as NTRK2), the receptor for brain-derived neurotrophic factor (BDNF). Herein, we demonstrate that the four alternatively spliced isoforms of SH2B1 (SH2B1α-SH2B1δ) are important determinants of neuronal architecture and neurotrophin-induced gene expression. Primary hippocampal neurons from Sh2b1-/- [knockout (KO)] mice exhibit decreased neurite complexity and length, and BDNF-induced expression of the synapse-related immediate early genes Egr1 and Arc. Reintroduction of each SH2B1 isoform into KO neurons increases neurite complexity; the brain-specific δ isoform also increases total neurite length. Human obesity-associated variants, when expressed in SH2B1δ, alter neurite complexity, suggesting that a decrease or increase in neurite branching may have deleterious effects that contribute to the severe childhood obesity and neurobehavioral abnormalities associated with these variants. Surprisingly, in contrast to SH2B1α, SH2B1β and SH2B1γ, which localize primarily in the cytoplasm and plasma membrane, SH2B1δ resides primarily in nucleoli. Some SH2B1δ is also present in the plasma membrane and nucleus. Nucleolar localization, driven by two highly basic regions unique to SH2B1δ, is required for SH2B1δ to maximally increase neurite complexity and BDNF-induced expression of Egr1, Arc and FosL1.
衔接蛋白 SH2B1 被募集到神经营养因子受体,包括 TrkB(也称为 NTRK2),即脑源性神经营养因子(BDNF)的受体。在此,我们证明 SH2B1 的四个选择性剪接异构体(SH2B1α-SH2B1δ)是神经元结构和神经营养因子诱导基因表达的重要决定因素。Sh2b1-/-(敲除(KO))小鼠的原代海马神经元表现出神经突复杂性和长度降低,以及 BDNF 诱导的突触相关即刻早期基因 Egr1 和 Arc 的表达降低。将每种 SH2B1 异构体重新引入 KO 神经元中会增加神经突复杂性;脑特异性 δ 异构体也会增加总神经突长度。当表达在 SH2B1δ 中的人类肥胖相关变体改变神经突复杂性时,表明神经突分支的减少或增加可能具有有害影响,从而导致与这些变体相关的严重儿童肥胖和神经行为异常。令人惊讶的是,与主要定位于细胞质和质膜中的 SH2B1α、SH2B1β 和 SH2B1γ 相反,SH2B1δ 主要位于核仁中。一些 SH2B1δ 也存在于质膜和核中。由 SH2B1δ 特有的两个高度碱性区域驱动的核仁定位是 SH2B1δ 最大限度地增加神经突复杂性和 BDNF 诱导的 Egr1、Arc 和 FosL1 表达所必需的。