Department of Ophthalmology, University of California, The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, United States of America.
Buck Institute for Research on Aging, Novato, CA, United States of America.
PLoS One. 2021 Oct 26;16(10):e0258872. doi: 10.1371/journal.pone.0258872. eCollection 2021.
Retinal homeostasis relies on intricate coordination of cell death and survival in response to stress and damage. Signaling mechanisms that coordinate this process in the adult retina remain poorly understood. Here we identify Decapentaplegic (Dpp) signaling in Drosophila and its mammalian homologue Transforming Growth Factor-beta (TGFβ) superfamily, that includes TGFβ and Bone Morphogenetic Protein (BMP) signaling arms, as central mediators of retinal neuronal death and tissue survival following acute damage. Using a Drosophila model for UV-induced retinal damage, we show that Dpp released from immune cells promotes tissue loss after UV-induced retinal damage. Interestingly, we find a dynamic response of retinal cells to this signal: in an early phase, Dpp-mediated stimulation of Saxophone/Smox signaling promotes apoptosis, while at a later stage, stimulation of the Thickveins/Mad axis promotes tissue repair and survival. This dual role is conserved in the mammalian retina through the TGFβ/BMP signaling, as supplementation of BMP4 or inhibition of TGFβ using small molecules promotes retinal cell survival, while inhibition of BMP negatively affects cell survival after light-induced photoreceptor damage and NMDA induced inner retinal neuronal damage. Our data identify key evolutionarily conserved mechanisms by which retinal homeostasis is maintained.
视网膜内稳态依赖于细胞死亡和存活在应激和损伤反应中的精细协调。在成年视网膜中协调这一过程的信号机制仍知之甚少。在这里,我们确定了果蝇中的 Decapentaplegic (Dpp) 信号及其哺乳动物同源物 Transforming Growth Factor-beta (TGFβ) 超家族,包括 TGFβ 和 Bone Morphogenetic Protein (BMP) 信号臂,作为急性损伤后视网膜神经元死亡和组织存活的中枢介质。使用一种用于 UV 诱导的视网膜损伤的果蝇模型,我们表明免疫细胞释放的 Dpp 促进了 UV 诱导的视网膜损伤后的组织损失。有趣的是,我们发现视网膜细胞对这种信号有一个动态的反应:在早期阶段,Dpp 介导的 Saxophone/Smox 信号刺激促进细胞凋亡,而在后期,Thickveins/Mad 轴的刺激促进组织修复和存活。这种双重作用在哺乳动物视网膜中通过 TGFβ/BMP 信号得到保守,因为 BMP4 的补充或使用小分子抑制 TGFβ可促进视网膜细胞存活,而抑制 BMP 会对光诱导的光感受器损伤和 NMDA 诱导的内视网膜神经元损伤后的细胞存活产生负面影响。我们的数据确定了维持视网膜内稳态的关键进化保守机制。