Crum Tyler S, Gleixner Amanda M, Posimo Jessica M, Mason Daniel M, Broeren Matthew T, Heinemann Scott D, Wipf Peter, Brodsky Jeffrey L, Leak Rehana K
Graduate School of Pharmaceutical Sciences, Duquesne University, Pittsburgh PA.
Departments of Chemistry and Pharmaceutical Sciences, University of Pittsburgh, Pittsburgh PA.
J Neurochem. 2015 Jun;133(6):780-794. doi: 10.1111/jnc.13041. Epub 2015 Mar 5.
The olfactory bulb is one of the most vulnerable brain regions in age-related proteinopathies. Proteinopathic stress is mitigated by the heat shock protein (Hsp) family of chaperones. Here, we describe age-related decreases in Hsc70 in the olfactory bulb of the female rat and higher levels of Hsp70 and Hsp25 in middle and old age than at 2-4 months. To model proteotoxic and oxidative stress in the olfactory bulb, primary olfactory bulb cultures were treated with the proteasome inhibitors lactacystin and MG132 or the pro-oxidant paraquat. Toxin-induced increases were observed in Hsp70, Hsp25, and Hsp32. To determine the functional consequences of the increase in Hsp70, we attenuated Hsp70 activity with two mechanistically distinct inhibitors. The Hsp70 inhibitors greatly potentiated the toxicity of sublethal lactacystin or MG132 but not of paraquat. Although ubiquitinated protein levels were unchanged with aging in vivo or with sublethal MG132 in vitro, there was a large, synergistic increase in ubiquitinated proteins when proteasome and Hsp70 functions were simultaneously inhibited. Our study suggests that olfactory bulb cells rely heavily on Hsp70 chaperones to maintain homeostasis during mild proteotoxic, but not oxidative insults, and that Hsp70 prevents the accrual of ubiquitinated proteins in these cells. The olfactory bulb is affected in the early phases of many age-related neurodegenerative disorders. Here, we described the impact of aging on multiple heat shock proteins (Hsps), such as Hsp70, in the female rat olfactory bulb in vivo. Using multiple proteasome and Hsp70 inhibitors (see schematic), we found that proteotoxicity elicited a compensatory increase in Hsp70 in primary olfactory bulb cells in vitro. Hsp70 then reduced the proteotoxic buildup of ubiquitinated proteins and robustly protected against cell death according to three independent viability assays. Thus, olfactory bulb neurons can mount impressive natural adaptations to proteotoxic injury, perhaps explaining why neurodegenerative disorders are so delayed in onset and so slow to progress.
嗅球是与年龄相关的蛋白质病中最易受损的脑区之一。伴侣蛋白热休克蛋白(Hsp)家族可减轻蛋白质病应激。在此,我们描述了雌性大鼠嗅球中Hsc70随年龄增长而减少,以及中年和老年时Hsp70和Hsp25水平高于2 - 4个月龄时的情况。为模拟嗅球中的蛋白毒性和氧化应激,原代嗅球培养物用蛋白酶体抑制剂乳胞素和MG132或促氧化剂百草枯处理。观察到毒素诱导Hsp70、Hsp25和Hsp32增加。为确定Hsp70增加的功能后果,我们用两种机制不同的抑制剂减弱Hsp70活性。Hsp70抑制剂极大地增强了亚致死剂量乳胞素或MG132的毒性,但未增强百草枯的毒性。尽管体内衰老或体外亚致死剂量MG132处理时泛素化蛋白水平未改变,但当蛋白酶体和Hsp70功能同时受到抑制时,泛素化蛋白有大幅协同增加。我们的研究表明,嗅球细胞在轻度蛋白毒性而非氧化损伤期间严重依赖Hsp70伴侣蛋白来维持内环境稳定,且Hsp70可防止这些细胞中泛素化蛋白的积累。嗅球在许多与年龄相关的神经退行性疾病早期会受到影响。在此,我们描述了衰老对雌性大鼠体内嗅球中多种热休克蛋白(如Hsp70)的影响。使用多种蛋白酶体和Hsp70抑制剂(见图),我们发现蛋白毒性在体外原代嗅球细胞中引发了Hsp70的代偿性增加。然后,Hsp70减少了泛素化蛋白的蛋白毒性积累,并根据三种独立的活力测定法有力地保护细胞免受死亡。因此,嗅球神经元能够对蛋白毒性损伤产生显著的自然适应,这或许可以解释为什么神经退行性疾病发病如此延迟且进展如此缓慢。