Martín-Estebané María, Navascués Julio, Sierra-Martín Ana, Martín-Guerrero Sandra M, Cuadros Miguel A, Carrasco María-Carmen, Marín-Teva José L
Departamento de Biología Celular, Facultad de Ciencias, Universidad de Granada, Granada, Spain.
Departamento de Biología Celular, Fisiología e Inmunología, Facultad de Biociencias, Universidad Autónoma de Barcelona, Bellaterra, Barcelona, Spain.
PLoS One. 2017 Aug 1;12(8):e0182450. doi: 10.1371/journal.pone.0182450. eCollection 2017.
Microglial cell precursors located in the area of the base of the pecten and the optic nerve head (BP/ONH) start to enter the retina of quail embryos at the 7th day of incubation (E7), subsequently colonizing the entire retina by central-to-peripheral tangential migration, as previously shown by our group. The present study demonstrates a precise chronological coincidence of the onset of microglial cell entry into the retina with a striking increase in death of retinal cells, as revealed by their active caspase-3 expression and TUNEL staining, in regions dorsal to the BP/ONH area, suggesting that dying retinal cells would contribute to the microglial cell inflow into the retina. However, the molecular mechanisms involved in this inflow are currently unclear. Extracellular nucleotides, such as ATP and UDP, have previously been shown to favor migration of microglia towards brain injuries because they are released by apoptotic cells and stimulate both chemotaxis and chemokinesis in microglial cells via signaling through purinergic receptors. Hence, we tested here the hypothesis that ATP and UDP play a role in the entry and migration of microglial precursors into the developing retina. For this purpose, we used an experimental model system based on organotypic cultures of E6.5 quail embryo retina explants, which mimics the entry and migration of microglial precursors in the in situ developing retina. Inhibition of purinergic signaling by treating retina explants with either apyrase, a nucleotide-hydrolyzing enzyme, or suramin, a broad spectrum antagonist of purinergic receptors, significantly prevents the entry of microglial cells into the retina. In addition, treatment of retina explants with either exogenous ATP or UDP results in significantly increased numbers of microglial cells entering the retina. In light of these findings, we conclude that purinergic signaling by extracellular ATP and UDP is necessary for the entry and migration of microglial cells into the embryonic retina by inducing chemokinesis in these cells.
位于栉膜基部和视神经乳头区域(BP/ONH)的小胶质细胞前体细胞在孵化第7天(E7)开始进入鹌鹑胚胎的视网膜,随后如我们小组之前所示,通过从中央到外周的切向迁移定殖于整个视网膜。本研究表明,小胶质细胞进入视网膜的起始时间与视网膜细胞死亡的显著增加在时间上精确吻合,这通过BP/ONH区域背侧区域视网膜细胞的活性半胱天冬酶-3表达和TUNEL染色得以揭示,提示死亡的视网膜细胞会促使小胶质细胞流入视网膜。然而,这种流入所涉及的分子机制目前尚不清楚。细胞外核苷酸,如ATP和UDP,先前已被证明有利于小胶质细胞向脑损伤部位迁移,因为它们由凋亡细胞释放,并通过嘌呤能受体信号传导刺激小胶质细胞的趋化性和化学增活作用。因此,我们在此测试了ATP和UDP在小胶质细胞前体进入和迁移到发育中的视网膜中起作用的假说。为此,我们使用了基于E6.5鹌鹑胚胎视网膜外植体器官型培养的实验模型系统,该系统模拟了小胶质细胞前体在原位发育视网膜中的进入和迁移。用核苷酸水解酶腺苷三磷酸双磷酸酶或嘌呤能受体的广谱拮抗剂苏拉明处理视网膜外植体以抑制嘌呤能信号传导,可显著阻止小胶质细胞进入视网膜。此外,用外源性ATP或UDP处理视网膜外植体导致进入视网膜的小胶质细胞数量显著增加。鉴于这些发现,我们得出结论,细胞外ATP和UDP的嘌呤能信号传导通过诱导小胶质细胞的化学增活作用,对于小胶质细胞进入和迁移到胚胎视网膜是必要的。