Lee Chinkyu, Joachimiak Ewa, Maier Wolfgang, Jiang Yu-Yang, Parra Mireya, Lechtreck Karl F, Cole Eric S, Gaertig Jacek
Department of Cellular Biology, University of Georgia, Athens, Georgia, United States of America.
Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland.
PLoS Genet. 2025 Jun 2;21(6):e1011735. doi: 10.1371/journal.pgen.1011735. eCollection 2025 Jun.
In ciliates, cortical organelles, including ciliary arrays, are positioned at precise locations along two polarity axes: anterior-posterior and circumferential (lateral). We explored the poorly understood mechanism of circumferential patterning, which generates left-right asymmetry. The model ciliate Tetrahymena has a single anteriorly-located oral apparatus. During cell division, a single new oral apparatus forms near the equator of the parental cell and along the longitude of the parental organelle. Cells homozygous for hypoangular 1 (hpo1) alleles, assemble multiple oral apparatuses positioned either to the left or right flanking the normal oral longitude. Using comparative next-generation sequencing, we identified HPO1 as a gene encoding an ARMC9-like protein. Hpo1 colocalizes with the ciliary basal bodies, forming a bilateral concentration gradient, with the high point on the cell's right side and a sharp drop-off that marks the longitude at which oral development initiates on the ventral side. A second Hpo1 concentration drop-off is present on the dorsal surface, where it marks the position for development of a cryptic oral apparatus that forms in the janus mutants. Hpo1 acts bilaterally to exclude oral development from the cell's right side. Hpo1 interacts with the Beige-Beach domain protein Bcd1, a cell's left side-enriched factor, whose loss also confers multiple oral apparatuses on the ventral surface. A loss of both Hpo1 and Bcd1 is lethal and profoundly disrupts the positioning, organization and size of the forming oral apparatus (including its internal left-right polarity). We conclude that in ciliates, the circumferential patterning involves gradient-forming factors that are concentrated on either the cell's right or left side and that the two sides of the cortex interact to create boundary effects that induce, position and shape developing cortical organelles.
在纤毛虫中，包括纤毛阵列在内的皮层细胞器沿着前后和周向（横向）两个极性轴定位在精确的位置。我们探究了人们了解较少的周向模式形成机制，该机制会产生左右不对称性。模式纤毛虫嗜热四膜虫有一个位于前部的单一口器。在细胞分裂过程中，一个新的口器在亲代细胞的赤道附近并沿着亲代细胞器的经度形成。hypoangular 1（hpo1）等位基因纯合的细胞会组装多个口器，这些口器位于正常口器经度两侧的左侧或右侧。通过比较下一代测序，我们确定HPO1是一个编码ARMC9样蛋白的基因。Hpo1与纤毛基体共定位，形成一个双侧浓度梯度，细胞右侧为高点，而低点则标志着腹侧口器发育开始的经度。背表面存在第二个Hpo1浓度下降点，它标志着在janus突变体中形成的隐性口器的发育位置。Hpo1在两侧起作用，阻止口器在细胞右侧发育。Hpo1与米色 - 海滩结构域蛋白Bcd1相互作用，Bcd1是一种在细胞左侧富集的因子，其缺失也会使腹侧出现多个口器。Hpo1和Bcd1都缺失是致命的，会严重破坏正在形成的口器的定位、组织和大小（包括其内部的左右极性）。我们得出结论，在纤毛虫中，周向模式形成涉及集中在细胞右侧或左侧的梯度形成因子，并且皮层的两侧相互作用以产生边界效应，从而诱导、定位和塑造发育中的皮层细胞器。
