McMaster University, Department of Biology, Hamilton, ON, L8S 4K1, Canada
University of Utah, Division of Nephrology and Hypertension, Department of Internal Medicine, Molecular Medicine Program, Salt Lake City, UT 84132, USA.
J Exp Biol. 2019 Jun 3;222(Pt 11):jeb204750. doi: 10.1242/jeb.204750.
The Malpighian tubules (MTs) and hindgut together act as the functional kidney in insects. MTs of caterpillars are notably complex and consist of several regions that display prominent differences in ion transport. The distal ileac plexus (DIP) is a region of MT that is of particular interest because it switches from ion secretion to ion reabsorption in larvae fed on ion-rich diets. The pathways of solute transport in the DIP are not well understood, but one potential route is the paracellular pathway between epithelial cells. This pathway is regulated by the septate junctions (SJs) in invertebrates, and in this study, we found regional and cellular heterogeneity in the expression of several integral SJ proteins. DIP of larvae fed ion-rich diets demonstrated a reduction in paracellular permeability, coupled with alterations in both SJ morphology and the abundance of its molecular components. Similarly, treatment with helicokinin (HK), an antidiuretic hormone identified by previous studies, altered mRNA abundance of many SJ proteins and reduced paracellular permeability. HK was also shown to target a secondary cell-specific SJ protein, Tsp2A. Taken together, our data suggest that dietary ion loading, known to cause ion transport reversal in the DIP of larval , leads to alterations in paracellular permeability, SJ morphology and the abundance of its molecular components. The results suggest that HK is an important endocrine factor that co-regulates ion transport, water transport and paracellular permeability in MTs of larval lepidopterans. We propose that co-regulation of all three components of the MT function in larval lepidopterans allows for safe toggling between ion secretion and reabsorption in the DIP in response to variations in dietary ion availability.
马氏管（MTs）和后肠共同作用，成为昆虫的功能性肾脏。毛毛虫的 MTs 非常复杂，由几个区域组成，这些区域在离子转运方面表现出明显的差异。远端回肠丛（DIP）是 MT 的一个特殊区域，因为它在以富含离子的饮食喂养的幼虫中从离子分泌转变为离子重吸收。DIP 中的溶质转运途径尚未完全了解，但一种潜在的途径是上皮细胞之间的旁细胞途径。该途径在无脊椎动物中受缝隙连接（SJ）调节，在这项研究中，我们发现几个完整 SJ 蛋白的表达存在区域和细胞异质性。以富含离子的饮食喂养的幼虫的 DIP 表现出旁细胞通透性降低，同时 SJ 形态和其分子成分的丰度也发生改变。同样，先前的研究表明，抗利尿激素 helicokinin (HK) 处理也改变了许多 SJ 蛋白的 mRNA 丰度并降低了旁细胞通透性。HK 还被证明靶向一种二次细胞特异性 SJ 蛋白 Tsp2A。总之，我们的数据表明，已知会导致幼虫 DIP 中离子转运逆转的饮食离子负荷会导致旁细胞通透性、SJ 形态和其分子成分丰度发生变化。结果表明，HK 是一种重要的内分泌因子，可共同调节幼虫鳞翅目 MTs 中的离子转运、水转运和旁细胞通透性。我们提出，在幼虫鳞翅目动物中，MT 功能的所有三个组成部分的共同调节允许在 DIP 中根据饮食离子可用性的变化安全地切换离子分泌和重吸收。
