Neupane Sanjiv, Janowicz Isabella A, Godwin Alan R F, Donnelly Kaitlyn E, Grady Richard C, Haltiwanger Robert S, Baldock Clair, Holdener Bernadette C
Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, NY, USA.
Manchester Cell-Matrix Centre, Division of Cell-Matrix Biology and Regenerative Medicine, University of Manchester, Manchester Academic Health Science Centre, Manchester, M13 9PT, UK.
Dev Biol. 2025 Nov;527:147-164. doi: 10.1016/j.ydbio.2025.08.004. Epub 2025 Aug 8.
The separation of individual digits is dependent on establishment of digit-interdigit periodicity, remodeling of the interdigital mesenchyme, and invagination of interdigital epithelial tongues. In Protein O-glucosyltransferase 2 and 3 double knockout (Poglut2/3 DKO) mice, digits 2 and 3 are fused, suggesting a defect in one or more processes. POGLUT2/3 add O-linked glucose to epidermal growth factor-like (EGF) repeats. Syndactyly is also observed when genes encoding the POGLUT2/3 substrates fibrillin 2 (FBN2) or both Nidogen 1 and 2 (NID1/2) are knocked out, suggesting that O-glucosylation is important for their function or localization. In this study, we evaluated the distribution of these substrates during digit separation and the effects of the Poglut2/3 DKO on their localization and cell behavior. During digit separation, the FBNs underwent a dramatic reorganization. Aberrant levels and distribution of the FBNs were observed in the Poglut2/3 DKO and microfibrils isolated from Poglut2/3 DKO skin showed altered periodicity in Fibrillin microfibrils. In contrast, the Poglut2/3 DKO had no effect on the levels or localization of NID1. In Poglut2/3 DKOs, bone morphogenetic protein (BMP) signaling was reduced during digit development, especially in the anterior autopod. Early anterior reduction of BMP signaling could potentially affect spacing of digits 2 & 3. While later reduction of BMP signaling in the Poglut2/3 DKO in the digit 2-3 region was likely responsible for defects in clearance of interdigital mesenchyme and interdigital tongue morphogenesis. These results highlight the importance of POGLUT2/3 mediated O-glucosylation for FBN microfibril organization and raise the possibility that O-glucose modulates the biological or physical properties of the FBN microfibril network.
单个手指的分离依赖于指-指间周期性的建立、指间间充质的重塑以及指间上皮舌的内陷。在蛋白质O-葡萄糖基转移酶2和3双敲除(Poglut2/3 DKO)小鼠中,第2和第3指融合,提示一个或多个过程存在缺陷。POGLUT2/3将O-连接的葡萄糖添加到表皮生长因子样(EGF)重复序列上。当编码POGLUT2/3底物原纤蛋白2(FBN2)或Nidogen 1和2(NID1/2)的基因被敲除时,也会观察到并指现象,这表明O-葡萄糖基化对它们的功能或定位很重要。在本研究中,我们评估了这些底物在手指分离过程中的分布以及Poglut2/3 DKO对它们定位和细胞行为的影响。在手指分离过程中,FBNs经历了剧烈的重组。在Poglut2/3 DKO中观察到FBNs水平和分布异常,并且从Poglut2/3 DKO皮肤分离的微原纤维显示原纤蛋白微原纤维的周期性改变。相比之下,Poglut2/3 DKO对NID1的水平或定位没有影响。在Poglut2/3 DKO小鼠中,手指发育过程中骨形态发生蛋白(BMP)信号减弱,尤其是在前肢末端。早期前肢BMP信号减弱可能会影响第2和第3指的间距。而后期Poglut2/3 DKO中第2-3指区域BMP信号减弱可能是指间间充质清除缺陷和指间舌形态发生缺陷的原因。这些结果突出了POGLUT2/3介导的O-葡萄糖基化对FBN微原纤维组织的重要性,并增加了O-葡萄糖调节FBN微原纤维网络生物学或物理特性的可能性。