Institute of Neuropathology, University of Duisburg-Essen, Hufelandstr. 55, 45122 Essen, Germany.
Department of Neurology, University of Duisburg-Essen, Hufelandstr. 55, 45122 Essen, Germany.
Brain Pathol. 2018 Nov;28(6):947-964. doi: 10.1111/bpa.12599. Epub 2018 Apr 10.
Women seem to have a higher vulnerability to Alzheimer's disease (AD), but the underlying mechanisms of this sex dichotomy are not well understood. Here, we first determined the influence of sex on various aspects of Alzheimer's pathology in transgenic CRND8 mice. We demonstrate that beta-amyloid (Aβ) plaque burden starts to be more severe around P180 (moderate disease stage) in female transgenics when compared to males and that aging aggravates this sex-specific difference. Furthermore, we show that female transgenics suffer from higher levels of neurovascular dysfunction around P180, resulting in impaired Aβ peptide clearance across the blood-brain-barrier at P360. Female transgenics show also higher levels of diffuse microgliosis and inflammation, but the density of microglial cells surrounding Aβ plaques is less in females. In line with this finding, testosterone compared to estradiol was able to improve microglial viability and Aβ clearance in vitro. The spatial memory of transgenics was in general poorer than in wildtypes and at P360 worse in females irrespective of their genotype. This difference was accompanied by a slightly diminished dendritic complexity in females. While all the above-named sex-differences emerged after the onset of Aβ pathology, kallikrein-8 (KLK8) protease levels were, as an exception, higher in female than in male brains very early when virtually no plaques were detectable. In a second step, we quantified cerebral KLK8 levels in AD patients and healthy controls, and could ascertain, similar to mice, higher KLK8 levels not only in AD-affected but also in healthy brains of women. Accordingly, we could demonstrate that estradiol but not testosterone induces KLK8 synthesis in neuronal and microglial cells. In conclusion, multiple features of AD are more pronounced in females. Here, we show for the first time that this sex-specific difference may be meditated by estrogen-induced KLK8 overproduction long before AD pathology emerges.
女性似乎更容易患阿尔茨海默病(AD),但这种性别差异的潜在机制尚不清楚。在这里,我们首先确定了性别对转基因 CRND8 小鼠阿尔茨海默病病理的各个方面的影响。我们证明,与雄性相比,β-淀粉样蛋白(Aβ)斑块负担在雌性转基因动物中从 P180 左右(中度疾病阶段)开始变得更加严重,并且衰老加剧了这种性别特异性差异。此外,我们表明,雌性转基因动物在 P180 左右遭受更高水平的神经血管功能障碍,导致 P360 时血脑屏障中 Aβ肽清除率受损。雌性转基因动物也显示出更高水平的弥漫性小胶质细胞炎症,但 Aβ斑块周围的小胶质细胞密度较低。与此发现一致,与雌二醇相比,睾丸激素能够提高体外小胶质细胞活力和 Aβ清除率。转基因动物的空间记忆一般比野生型差,而在 P360 时无论其基因型如何,雌性的记忆都更差。这种差异伴随着雌性小胶质细胞的树突复杂性略有降低。虽然所有上述性别差异都出现在 Aβ病理发生后,但激肽释放酶-8(KLK8)蛋白酶水平是一个例外,在几乎检测不到斑块时,雌性的水平高于雄性。在第二步中,我们在 AD 患者和健康对照者中定量了大脑 KLK8 水平,并且可以确定,与小鼠相似,不仅在受 AD 影响的大脑中,而且在健康女性的大脑中,KLK8 水平也更高。因此,我们可以证明雌激素而不是睾丸激素诱导神经元和小胶质细胞中 KLK8 的合成。总之,AD 的多个特征在女性中更为明显。在这里,我们首次表明,这种性别特异性差异可能是由雌激素诱导的 KLK8 过度产生介导的,而这种差异早在 AD 病理出现之前就已经存在。