Defect patterns on the curved surface of fish retinae suggest a mechanism of cone mosaic formation.
Defect patterns on the curved surface of fish retinae suggest a mechanism of cone mosaic formation.
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DOI：
10.1371/journal.pcbi.1008437
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发表时间：
2020-12
影响因子：
4.3
通讯作者：
Lubensky DK
中科院分区：
文献类型：
--
作者：
Nunley H;Nagashima M;Martin K;Lorenzo Gonzalez A;Suzuki SC;Norton DA;Wong ROL;Raymond PA;Lubensky DK
斑马鱼视网膜的外上皮层含有锥形感光细胞的晶体阵列，称为锥形马赛克。当这种马赛克通过在半球视网膜边缘有丝分裂地增加新的光感受器而生长时，称为“Y-连接”的拓扑缺陷形成，以保持大致恒定的细胞间距。由于在曲面上生长而产生的拓扑缺陷是锥形马赛克的一个明显特征，这在其他研究得很好的生物模式中是没有的，比如果蝇复眼的R8光感受器阵列。由于缺陷可以提供对图案形成负责的细胞-细胞相互作用的洞察，在这里，我们描述了单个Y-连接核心中锥体的排列以及整个视网膜中Y-连接的空间分布。我们发现，对于单个的Y结，靠近核心的锥体的分布与在物理晶体中观察到的结构密切对应。此外，Y形连接从视网膜中心到外围被组织成称为颗粒边界的线条。在物理晶体中，无论缺陷的初始分布如何，缺陷都可以通过单个粒子的迁移性结合成晶界。通过对活体鱼类的成像，我们证明了锥形马赛克中的晶界在初始马赛克形成期间出现，而不需要缺陷运动。在这一观察的激励下，我们证明了细胞-细胞相互作用的计算模型产生了带有晶界的马赛克。与大多静止的细胞包装中命运指定的范例模型不同，这一发现强调了细胞运动在形成生物晶体中的作用，该作用由分化过程中的细胞间相互作用引导。这种形成规则图案的途径在某些情况下可能特别有价值，比如在曲面上生长，在这种情况下，缺陷之间产生的远程、弹性、有效的相互作用可以帮助将它们组合成晶界。从哺乳动物内耳的毛细胞到苍蝇背上的刷毛，感觉细胞通常形成精确的阵列，确保这些细胞均匀地分布在组织的表面。这里我们考虑斑马鱼的视锥马赛克，这是位于视网膜外层的视锥感光细胞的晶体。由于视锥马赛克从弯曲的视网膜表面的边缘生长，所以插入新的视锥(即缺陷)以保持感觉细胞之间的恒定间距。我们研究了这些缺陷的空间分布，以深入了解锥形图案的形成。通过对活鱼的视网膜进行成像，我们发现，随着分化的锥体被合并到马赛克中，缺陷形成了线(晶界)，这些线(晶界)分隔了大部分无缺陷的区域。然后，我们证明了一个基于移动细胞之间的排斥力的计算模型在它们并入马赛克的过程中产生了类似的晶界。因此，这项研究表明，由排斥细胞-细胞相互作用控制的细胞运动在建立生命系统中的规律模式方面发挥着重要作用。
The outer epithelial layer of zebrafish retinae contains a crystalline array of cone photoreceptors, called the cone mosaic. As this mosaic grows by mitotic addition of new photoreceptors at the rim of the hemispheric retina, topological defects, called “Y-Junctions”, form to maintain approximately constant cell spacing. The generation of topological defects due to growth on a curved surface is a distinct feature of the cone mosaic not seen in other well-studied biological patterns like the R8 photoreceptor array in the Drosophila compound eye. Since defects can provide insight into cell-cell interactions responsible for pattern formation, here we characterize the arrangement of cones in individual Y-Junction cores as well as the spatial distribution of Y-junctions across entire retinae. We find that for individual Y-junctions, the distribution of cones near the core corresponds closely to structures observed in physical crystals. In addition, Y-Junctions are organized into lines, called grain boundaries, from the retinal center to the periphery. In physical crystals, regardless of the initial distribution of defects, defects can coalesce into grain boundaries via the mobility of individual particles. By imaging in live fish, we demonstrate that grain boundaries in the cone mosaic instead appear during initial mosaic formation, without requiring defect motion. Motivated by this observation, we show that a computational model of repulsive cell-cell interactions generates a mosaic with grain boundaries. In contrast to paradigmatic models of fate specification in mostly motionless cell packings, this finding emphasizes the role of cell motion, guided by cell-cell interactions during differentiation, in forming biological crystals. Such a route to the formation of regular patterns may be especially valuable in situations, like growth on a curved surface, where the resulting long-ranged, elastic, effective interactions between defects can help to group them into grain boundaries. From hair cells in the mammalian inner ear to the bristles on a fly’s back, sensory cells often form precise arrays, ensuring that these cells are evenly spread out on the tissue’s surface. Here we consider the zebrafish cone mosaic, a crystal of cone photoreceptors in the outer retinal layer. Because the cone mosaic grows from the rim of the curved retinal surface, new rows of cones (i.e., defects) are inserted to maintain constant spacing between sensory cells. We study the spatial distribution of these defects to gain insight into how the cone pattern forms. By imaging retinae in live fish, we find that as differentiating cones are incorporated into the mosaic, defects form lines (grain boundaries) that separate mostly defect-free domains. Then, we show that a computational model based on repulsion between mobile cells during their incorporation into the mosaic generates similar grain boundaries. This study thus suggests that cell motion governed by repulsive cell-cell interactions can play an important role in establishing regular patterns in living systems.
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