Ben Haim Lucile, Ceyzériat Kelly, Carrillo-de Sauvage Maria Angeles, Aubry Fabien, Auregan Gwennaëlle, Guillermier Martine, Ruiz Marta, Petit Fanny, Houitte Diane, Faivre Emilie, Vandesquille Matthias, Aron-Badin Romina, Dhenain Marc, Déglon Nicole, Hantraye Philippe, Brouillet Emmanuel, Bonvento Gilles, Escartin Carole
Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Département des Sciences du Vivant (DSV), Institut d'Imagerie Biomédicale (I2BM), Molecular Imaging Research Center (MIRCen), F-92260 Fontenay-aux-Roses, France, and Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud, UMR 9199, Neurodegenerative Diseases Laboratory, F-92260 Fontenay-aux-Roses, France.
Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Département des Sciences du Vivant (DSV), Institut d'Imagerie Biomédicale (I2BM), Molecular Imaging Research Center (MIRCen), F-92260 Fontenay-aux-Roses, France, and Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud, UMR 9199, Neurodegenerative Diseases Laboratory, F-92260 Fontenay-aux-Roses, France
J Neurosci. 2015 Feb 11;35(6):2817-29. doi: 10.1523/JNEUROSCI.3516-14.2015.
Astrocyte reactivity is a hallmark of neurodegenerative diseases (ND), but its effects on disease outcomes remain highly debated. Elucidation of the signaling cascades inducing reactivity in astrocytes during ND would help characterize the function of these cells and identify novel molecular targets to modulate disease progression. The Janus kinase/signal transducer and activator of transcription 3 (JAK/STAT3) pathway is associated with reactive astrocytes in models of acute injury, but it is unknown whether this pathway is directly responsible for astrocyte reactivity in progressive pathological conditions such as ND. In this study, we examined whether the JAK/STAT3 pathway promotes astrocyte reactivity in several animal models of ND. The JAK/STAT3 pathway was activated in reactive astrocytes in two transgenic mouse models of Alzheimer's disease and in a mouse and a nonhuman primate lentiviral vector-based model of Huntington's disease (HD). To determine whether this cascade was instrumental for astrocyte reactivity, we used a lentiviral vector that specifically targets astrocytes in vivo to overexpress the endogenous inhibitor of the JAK/STAT3 pathway [suppressor of cytokine signaling 3 (SOCS3)]. SOCS3 significantly inhibited this pathway in astrocytes, prevented astrocyte reactivity, and decreased microglial activation in models of both diseases. Inhibition of the JAK/STAT3 pathway within reactive astrocytes also increased the number of huntingtin aggregates, a neuropathological hallmark of HD, but did not influence neuronal death. Our data demonstrate that the JAK/STAT3 pathway is a common mediator of astrocyte reactivity that is highly conserved between disease states, species, and brain regions. This universal signaling cascade represents a potent target to study the role of reactive astrocytes in ND.
星形胶质细胞反应性是神经退行性疾病(ND)的一个标志,但其对疾病转归的影响仍存在激烈争论。阐明在ND期间诱导星形胶质细胞反应性的信号级联反应,将有助于明确这些细胞的功能,并识别调控疾病进展的新分子靶点。在急性损伤模型中,Janus激酶/信号转导子和转录激活子3(JAK/STAT3)通路与反应性星形胶质细胞相关,但在诸如ND等进行性病理状况下,该通路是否直接导致星形胶质细胞反应性尚不清楚。在本研究中,我们检测了JAK/STAT3通路在几种ND动物模型中是否促进星形胶质细胞反应性。在两种阿尔茨海默病转基因小鼠模型以及一种基于慢病毒载体的小鼠和非人类灵长类亨廷顿舞蹈病(HD)模型的反应性星形胶质细胞中,JAK/STAT3通路被激活。为了确定该级联反应是否对星形胶质细胞反应性起作用,我们使用了一种在体内特异性靶向星形胶质细胞的慢病毒载体,以过表达JAK/STAT3通路的内源性抑制剂[细胞因子信号传导抑制因子3(SOCS3)]。在两种疾病模型中,SOCS3均显著抑制星形胶质细胞中的该通路,阻止星形胶质细胞反应性,并减少小胶质细胞激活。抑制反应性星形胶质细胞内的JAK/STAT3通路也增加了亨廷顿蛋白聚集体的数量,这是HD的一种神经病理学标志,但不影响神经元死亡。我们的数据表明,JAK/STAT3通路是星形胶质细胞反应性的一个常见介质,在疾病状态、物种和脑区之间高度保守。这种通用的信号级联反应代表了一个研究反应性星形胶质细胞在ND中作用的有力靶点。