The Bloomfield Center for Research in Aging, Lady Davis Institute for Medical Research, Jewish General Hospital, Montreal, Quebec, Canada.
The Bloomfield Center for Research in Aging, Lady Davis Institute for Medical Research, Jewish General Hospital, Montreal, Quebec, Canada ; Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada.
PLoS One. 2013 Dec 19;8(12):e84615. doi: 10.1371/journal.pone.0084615. eCollection 2013.
b-Amyloid peptide accumulation, tau hyperphosphorylation, and synapse loss are characteristic neuropathological symptoms of Alzheimer's disease (AD). Tau hyperphosphorylation is suggested to inhibit the association of tau with microtubules, making microtubules unstable and causing neurodegeneration. The mechanism of tau phosphorylation in AD brain, therefore, is of considerable significance. Although PHF-tau is phosphorylated at over 40 Ser/Thr sites, Ser(262) phosphorylation was shown to mediate b-amyloid neurotoxicity and formation of toxic tau lesions in the brain. In vitro, PKA is one of the kinases that phosphorylates tau at Ser(262), but the mechanism by which it phosphorylates tau in AD brain is not very clear. 14-3-3z is associated with neurofibrillary tangles and is upregulated in AD brain. In this study, we show that 14-3-3z promotes tau phosphorylation at Ser(262) by PKA in differentiating neurons. When overexpressed in rat hippocampal primary neurons, 14-3-3z causes an increase in Ser(262) phosphorylation, a decrease in the amount of microtubule-bound tau, a reduction in the amount of polymerized microtubules, as well as microtubule instability. More importantly, the level of pre-synaptic protein synaptophysin was significantly reduced. Downregulation of synaptophysin in 14-3-3z overexpressing neurons was mitigated by inhibiting the proteosome, indicating that 14-3-3z promotes proteosomal degradation of synaptophysin. When 14-3-3z overexpressing neurons were treated with the microtubule stabilizing drug taxol, tau Ser(262) phosphorylation decreased and synaptophysin level was restored. Our data demonstrate that overexpression of 14-3-3z accelerates proteosomal turnover of synaptophysin by promoting the destabilization of microtubules. Synaptophysin is involved in synapse formation and neurotransmitter release. Our results suggest that 14-3-3z may cause synaptic pathology by reducing synaptophysin levels in the brains of patients suffering from AD.
β-淀粉样肽积累、tau 过度磷酸化和突触丧失是阿尔茨海默病(AD)的特征性神经病理学症状。tau 过度磷酸化被认为会抑制 tau 与微管的结合,使微管不稳定并导致神经退行性变。因此,AD 脑中 tau 磷酸化的机制具有重要意义。尽管 PHF-tau 在超过 40 个 Ser/Thr 位点被磷酸化,但 Ser(262)磷酸化被证明介导了 b-淀粉样蛋白的神经毒性,并在大脑中形成有毒的 tau 病变。在体外,PKA 是磷酸化 tau 于 Ser(262)的激酶之一,但它在 AD 脑中磷酸化 tau 的机制尚不清楚。14-3-3z 与神经原纤维缠结有关,在 AD 脑中上调。在这项研究中,我们表明 14-3-3z 通过 PKA 在分化神经元中促进 tau 于 Ser(262)的磷酸化。当在大鼠海马原代神经元中过表达时,14-3-3z 导致 Ser(262)磷酸化增加,微管结合 tau 减少,聚合微管减少,微管不稳定。更重要的是,突触前蛋白突触小泡蛋白的水平显著降低。14-3-3z 过表达神经元中的突触小泡蛋白下调通过抑制蛋白酶体得到缓解,表明 14-3-3z 促进了突触小泡蛋白的蛋白酶体降解。当用微管稳定药物紫杉醇处理 14-3-3z 过表达神经元时,tau Ser(262)磷酸化减少,突触小泡蛋白水平恢复。我们的数据表明,通过促进微管的不稳定性,14-3-3z 的过表达加速了突触小泡蛋白的蛋白酶体周转率。突触小泡蛋白参与突触形成和神经递质释放。我们的结果表明,14-3-3z 通过降低 AD 患者大脑中的突触小泡蛋白水平可能导致突触病理学。