Jearaphunt Miti, Noonin Chadanat, Jiravanichpaisal Pikul, Nakamura Seiko, Tassanakajon Anchalee, Söderhäll Irene, Söderhäll Kenneth
Department of Comparative Physiology, Uppsala University, Uppsala, Sweden.
Department of Comparative Physiology, Uppsala University, Uppsala, Sweden; Aquatic Molecular Genetics and Biotechnology Laboratory, National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency, Pathumthani, Bangkok, Thailand.
PLoS Pathog. 2014 Apr 10;10(4):e1004059. doi: 10.1371/journal.ppat.1004059. eCollection 2014 Apr.
Invertebrates rely on innate immunity to respond to the entry of foreign microorganisms. One of the important innate immune responses in arthropods is the activation of prophenoloxidase (proPO) by a proteolytic cascade finalized by the proPO-activating enzyme (ppA), which leads to melanization and the elimination of pathogens. Proteolytic cascades play a crucial role in innate immune reactions because they can be triggered more quickly than immune responses that require altered gene expression. Caspases are intracellular proteases involved in tightly regulated limited proteolysis of downstream processes and are also involved in inflammatory responses to infections for example by activation of interleukin 1ß. Here we show for the first time a link between caspase cleavage of proPO and release of this protein and the biological function of these fragments in response to bacterial infection in crayfish. Different fragments from the cleavage of proPO were studied to determine their roles in bacterial clearance and antimicrobial activity. These fragments include proPO-ppA, the N-terminal part of proPO cleaved by ppA, and proPO-casp1 and proPO-casp2, the fragments from the N-terminus after cleavage by caspase-1. The recombinant proteins corresponding to all three of these peptide fragments exhibited bacterial clearance activity in vivo, and proPO-ppA had antimicrobial activity, as evidenced by a drastic decrease in the number of Escherichia coli in vitro. The bacteria incubated with the proPO-ppA fragment were agglutinated and their cell morphology was altered. Our findings show an evolutionary conserved role for caspase cleavage in inflammation, and for the first time show a link between caspase induced inflammation and melanization. Further we give a more detailed understanding of how the proPO system is regulated in time and place and a role for the peptide generated by activation of proPO as well as for the peptides resulting from Caspase 1 proteolysis.
无脊椎动物依靠先天免疫来应对外来微生物的侵入。节肢动物重要的先天免疫反应之一是通过由酚氧化酶原激活酶(ppA)完成的蛋白水解级联反应激活酚氧化酶原(proPO),这会导致黑化并清除病原体。蛋白水解级联反应在先天免疫反应中起关键作用,因为它们比需要改变基因表达的免疫反应触发得更快。半胱天冬酶是细胞内蛋白酶,参与对下游过程的严格调控的有限蛋白水解,也参与对感染的炎症反应,例如通过激活白细胞介素1β。在这里,我们首次展示了半胱天冬酶对proPO的切割与该蛋白的释放之间的联系,以及这些片段在小龙虾应对细菌感染时的生物学功能。研究了proPO切割产生的不同片段,以确定它们在细菌清除和抗菌活性中的作用。这些片段包括proPO-ppA,即被ppA切割的proPO的N端部分,以及proPO-casp1和proPO-casp2,即被半胱天冬酶-1切割后N端的片段。与这三个肽片段相对应的重组蛋白在体内均表现出细菌清除活性,proPO-ppA具有抗菌活性,体外实验中大肠杆菌数量的急剧减少证明了这一点。与proPO-ppA片段一起孵育的细菌发生凝集,其细胞形态发生改变。我们的研究结果表明半胱天冬酶切割在炎症中具有进化保守的作用,并且首次展示了半胱天冬酶诱导的炎症与黑化之间的联系。此外,我们更详细地了解了proPO系统如何在时间和空间上受到调控,以及proPO激活产生的肽以及半胱天冬酶1蛋白水解产生的肽所起的作用。