Tavignot Raphael, Chaduli Delphine, Djitte Fatoumata, Charroux Bernard, Royet Julien
Aix Marseille Univ, CNRS, IBDM, Marseille, France.
PLoS Genet. 2017 Jan 13;13(1):e1006569. doi: 10.1371/journal.pgen.1006569. eCollection 2017 Jan.
NF-κB pathways are key signaling cascades of the Drosophila innate immune response. One of them, the Immune Deficiency (IMD) pathway, is under a very tight negative control. Although molecular brakes exist at each step of this signaling module from ligand availability to transcriptional regulation, it remains unknown whether repressors act in the same cells or tissues and if not, what is rationale behind this spatial specificity. We show here that the negative regulator of IMD pathway PGRP-LF is epressed in ectodermal derivatives. We provide evidence that, in the absence of any immune elicitor, PGRP-LF loss-of-function mutants, display a constitutive NF-κB/IMD activation specifically in ectodermal tissues leading to genitalia and tergite malformations. In agreement with previous data showing that proper development of these structures requires induction of apoptosis, we show that ectopic activation of NF-κB/IMD signaling leads to apoptosis inhibition in both genitalia and tergite primordia. We demonstrate that NF-κB/IMD signaling antagonizes apoptosis by up-regulating expression of the anti-apoptotic protein Diap1. Altogether these results show that, in the complete absence of infection, the negative regulation of NF-κB/IMD pathway by PGRP-LF is crucial to ensure proper induction of apoptosis and consequently normal fly development. These results highlight that IMD pathway regulation is controlled independently in different tissues, probably reflecting the different roles of this signaling cascade in both developmental and immune processes.
NF-κB信号通路是果蝇先天免疫反应的关键信号级联。其中一条通路,即免疫缺陷(IMD)通路,受到非常严格的负调控。尽管从配体可用性到转录调控的这个信号模块的每一步都存在分子制动,但仍不清楚抑制因子是否在相同的细胞或组织中起作用,如果不是,这种空间特异性背后的原理是什么。我们在此表明,IMD通路的负调控因子PGRP-LF在外胚层衍生物中表达。我们提供的证据表明,在没有任何免疫激发子的情况下,PGRP-LF功能丧失突变体在表皮组织中特异性地表现出组成型NF-κB/IMD激活,导致生殖器和背板畸形。与先前的数据一致,这些结构的正常发育需要诱导细胞凋亡,我们表明NF-κB/IMD信号的异位激活导致生殖器和背板原基中的细胞凋亡抑制。我们证明NF-κB/IMD信号通过上调抗凋亡蛋白Diap1的表达来拮抗细胞凋亡。总之,这些结果表明,在完全没有感染的情况下,PGRP-LF对NF-κB/IMD通路的负调控对于确保细胞凋亡的正确诱导以及因此正常的果蝇发育至关重要。这些结果突出表明,IMD通路的调控在不同组织中是独立控制的,这可能反映了该信号级联在发育和免疫过程中的不同作用。