Corvino Valentina, Marchese Elisa, Podda Maria Vittoria, Lattanzi Wanda, Giannetti Stefano, Di Maria Valentina, Cocco Sara, Grassi Claudio, Michetti Fabrizio, Geloso Maria Concetta
Institute of Anatomy and Cell Biology - Università Cattolica del Sacro Cuore, Rome, Italy.
Institute of Human Physiology - Università Cattolica del Sacro Cuore, Rome, Italy.
PLoS One. 2014 Feb 7;9(2):e88294. doi: 10.1371/journal.pone.0088294. eCollection 2014.
Modulation of endogenous neurogenesis is regarded as a promising challenge in neuroprotection. In the rat model of hippocampal neurodegeneration obtained by Trimethyltin (TMT) administration (8 mg/kg), characterised by selective pyramidal cell loss, enhanced neurogenesis, seizures and cognitive impairment, we previously demonstrated a proliferative role of exogenous neuropeptide Y (NPY), on dentate progenitors in the early phases of neurodegeneration. To investigate the functional integration of newly-born neurons, here we studied in adult rats the long-term effects of intracerebroventricular administration of NPY (2 µg/2 µl, 4 days after TMT-treatment), which plays an adjuvant role in neurodegeneration and epilepsy. Our results indicate that 30 days after NPY administration the number of new neurons was still higher in TMT+NPY-treated rats than in control+saline group. As a functional correlate of the integration of new neurons into the hippocampal network, long-term potentiation recorded in Dentate Gyrus (DG) in the absence of GABAA receptor blockade was higher in the TMT+NPY-treated group than in all other groups. Furthermore, qPCR analysis of Kruppel-like factor 9, a transcription factor essential for late-phase maturation of neurons in the DG, and of the cyclin-dependent kinase 5, critically involved in the maturation and dendrite extension of newly-born neurons, revealed a significant up-regulation of both genes in TMT+NPY-treated rats compared with all other groups. To explore the early molecular events activated by NPY administration, the Sonic Hedgehog (Shh) signalling pathway, which participates in the maintenance of the neurogenic hippocampal niche, was evaluated by qPCR 1, 3 and 5 days after NPY-treatment. An early significant up-regulation of Shh expression was detected in TMT+NPY-treated rats compared with all other groups, associated with a modulation of downstream genes. Our data indicate that the neurogenic effect of NPY administration during TMT-induced neurodegeneration involves early Shh pathway activation and results in a functional integration of newly-generated neurons into the local circuit.
内源性神经发生的调节被视为神经保护领域一项具有前景的挑战。在通过给予三甲基锡(TMT,8毫克/千克)建立的海马神经退行性变大鼠模型中,其特征为选择性锥体细胞丢失、神经发生增强、癫痫发作和认知障碍,我们之前已证明外源性神经肽Y(NPY)在神经退行性变早期阶段对齿状祖细胞具有增殖作用。为了研究新生神经元的功能整合,在此我们对成年大鼠进行了脑室内注射NPY(2微克/2微升,TMT治疗后4天)的长期影响研究,NPY在神经退行性变和癫痫中起辅助作用。我们的结果表明,在给予NPY 30天后,TMT + NPY处理组大鼠的新生神经元数量仍高于对照组 + 生理盐水组。作为新生神经元整合到海马网络中的功能关联指标,在未阻断GABAA受体的情况下,TMT + NPY处理组齿状回(DG)记录的长时程增强比所有其他组更高。此外,对DG中神经元晚期成熟所必需的转录因子Kruppel样因子9以及对新生神经元成熟和树突延伸至关重要的细胞周期蛋白依赖性激酶5进行qPCR分析,结果显示与所有其他组相比,TMT + NPY处理组大鼠中这两个基因均有显著上调。为了探究NPY给药激活的早期分子事件,在NPY治疗后1、3和5天通过qPCR评估了参与神经源性海马生态位维持的音猬因子(Shh)信号通路。与所有其他组相比,在TMT + NPY处理组大鼠中检测到Shh表达早期显著上调,并伴有下游基因的调节。我们的数据表明,在TMT诱导的神经退行性变期间给予NPY的神经源性作用涉及早期Shh信号通路激活,并导致新生神经元功能性整合到局部回路中。