O'Donoghue Anthony J, Knudsen Giselle M, Beekman Chapman, Perry Jenna A, Johnson Alexander D, DeRisi Joseph L, Craik Charles S, Bennett Richard J
Department of Pharmaceutical Chemistry.
Department of Microbiology and Immunology, Brown University, Providence, RI 02912.
Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):7478-83. doi: 10.1073/pnas.1507082112. Epub 2015 May 5.
Pseudogymnoascus destructans is the causative agent of white-nose syndrome, a disease that has caused the deaths of millions of bats in North America. This psychrophilic fungus proliferates at low temperatures and targets hibernating bats, resulting in their premature arousal from stupor with catastrophic consequences. Despite the impact of white-nose syndrome, little is known about the fungus itself or how it infects its mammalian host. P. destructans is not amenable to genetic manipulation, and therefore understanding the proteins involved in infection requires alternative approaches. Here, we identify hydrolytic enzymes secreted by P. destructans, and use a novel and unbiased substrate profiling technique to define active peptidases. These experiments revealed that endopeptidases are the major proteolytic activities secreted by P. destructans, and that collagen, the major structural protein in mammals, is actively degraded by the secretome. A serine endopeptidase, hereby-named Destructin-1, was subsequently identified, and a recombinant form overexpressed and purified. Biochemical analysis of Destructin-1 showed that it mediated collagen degradation, and a potent inhibitor of peptidase activity was identified. Treatment of P. destructans-conditioned media with this antagonist blocked collagen degradation and facilitated the detection of additional secreted proteolytic activities, including aminopeptidases and carboxypeptidases. These results provide molecular insights into the secretome of P. destructans, and identify serine endopeptidases that have the clear potential to facilitate tissue invasion and pathogenesis in the mammalian host.
毁灭柱孢菌是白鼻综合征的病原体,这种疾病已导致北美数百万只蝙蝠死亡。这种嗜冷真菌在低温下增殖,并以冬眠的蝙蝠为目标,导致它们从昏迷中过早苏醒,产生灾难性后果。尽管白鼻综合征影响巨大,但对这种真菌本身或其如何感染哺乳动物宿主却知之甚少。毁灭柱孢菌不易进行基因操作,因此了解参与感染的蛋白质需要采用其他方法。在这里,我们鉴定了毁灭柱孢菌分泌的水解酶,并使用一种新颖且无偏差的底物谱分析技术来确定活性肽酶。这些实验表明,内肽酶是毁灭柱孢菌分泌的主要蛋白水解活性物质,并且哺乳动物中的主要结构蛋白胶原蛋白会被分泌组积极降解。随后鉴定出一种丝氨酸内肽酶,命名为Destructin-1,并对其重组形式进行了过表达和纯化。对Destructin-1的生化分析表明它介导胶原蛋白降解,并鉴定出一种有效的肽酶活性抑制剂。用这种拮抗剂处理毁灭柱孢菌条件培养基可阻止胶原蛋白降解,并有助于检测其他分泌的蛋白水解活性,包括氨肽酶和羧肽酶。这些结果为毁灭柱孢菌的分泌组提供了分子层面的见解,并鉴定出具有明显潜力促进在哺乳动物宿主中组织侵袭和发病机制的丝氨酸内肽酶。