Danneels Ellen L, Gerlo Sarah, Heyninck Karen, Van Craenenbroeck Kathleen, De Bosscher Karolien, Haegeman Guy, de Graaf Dirk C
Laboratory of Zoophysiology, Department of Physiology, Ghent University, Gent, Belgium.
VIB Department of Medical Protein Research, Ghent University, Gent, Belgium.
PLoS One. 2014 May 12;9(5):e96825. doi: 10.1371/journal.pone.0096825. eCollection 2014.
With more than 150,000 species, parasitoids are a large group of hymenopteran insects that inject venom into and then lay their eggs in or on other insects, eventually killing the hosts. Their venoms have evolved into different mechanisms for manipulating host immunity, physiology and behavior in such a way that enhance development of the parasitoid young. The venom from the ectoparasitoid Nasonia vitripennis inhibits the immune system in its host organism in order to protect their offspring from elimination. Since the major innate immune pathways in insects, the Toll and Imd pathways, are homologous to the NF-κB pathway in mammals, we were interested in whether a similar immune suppression seen in insects could be elicited in a mammalian cell system. A well characterized NF-κB reporter gene assay in fibrosarcoma cells showed a dose-dependent inhibition of NF-κB signaling caused by the venom. In line with this NF-κB inhibitory action, N. vitripennis venom dampened the expression of IL-6, a prototypical proinflammatory cytokine, from LPS-treated macrophages. The venom also inhibited the expression of two NF-κB target genes, IκBα and A20, that act in a negative feedback loop to prevent excessive NF-κB activity. Surprisingly, we did not detect any effect of the venom on the early events in the canonical NF-κB activation pathway, leading to NF-κB nuclear translocation, which was unaltered in venom-treated cells. The MAP kinases ERK, p38 and JNK are other crucial regulators of immune responses. We observed that venom treatment did not affect p38 and ERK activation, but induced a prolonged JNK activation. In summary, our data indicate that venom from N. vitripennis inhibits NF-κB signaling in mammalian cells. We identify venom-induced up regulation of the glucocorticoid receptor-regulated GILZ as a most likely molecular mediator for this inhibition.
寄生蜂有超过15万种,是膜翅目昆虫中的一大类群,它们会将毒液注入其他昆虫体内,然后在这些昆虫体内或体表产卵,最终杀死宿主。它们的毒液已经进化出不同的机制来操纵宿主的免疫、生理和行为,从而促进寄生蜂幼虫的发育。外寄生蜂丽蝇蛹集金小蜂的毒液会抑制宿主体内的免疫系统,以保护其后代不被清除。由于昆虫体内主要的固有免疫途径——Toll和Imd途径与哺乳动物体内的NF-κB途径同源,我们想了解在昆虫中观察到的类似免疫抑制现象是否能在哺乳动物细胞系统中引发。在纤维肉瘤细胞中进行的一项特征明确的NF-κB报告基因检测显示,毒液会导致NF-κB信号传导呈剂量依赖性抑制。与这种NF-κB抑制作用一致,丽蝇蛹集金小蜂毒液会抑制经脂多糖处理的巨噬细胞中典型促炎细胞因子白细胞介素-6的表达。该毒液还抑制了两个NF-κB靶基因IκBα和A20的表达,这两个基因通过负反馈回路发挥作用,以防止NF-κB活性过度。令人惊讶的是,我们未检测到毒液对经典NF-κB激活途径中导致NF-κB核转位的早期事件有任何影响,在毒液处理的细胞中这一过程未发生改变。丝裂原活化蛋白激酶ERK、p38和JNK是免疫反应的其他关键调节因子。我们观察到毒液处理不影响p38和ERK的激活,但会诱导JNK的长时间激活。总之,我们的数据表明丽蝇蛹集金小蜂的毒液会抑制哺乳动物细胞中的NF-κB信号传导。我们确定毒液诱导的糖皮质激素受体调节的GILZ上调是这种抑制作用最可能的分子介质。