3D printed scaffolds regulated by neural-bone metabolic coupling promote bone unit regeneration.

Zhang, Pengrui; Li, Linfeng; Yan, Caiping; Cao, Xinna; Lai, Neng; Lei, Yefei; Jiang, Ke; Yang, Hanfeng et al. · Bioact Mater · 2026

basic_science · Level V

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Abstract

The bone unit (BU) is a multicellular functional unit composed of neuromodulatory networks, bone tissue, and functional blood vessels. As a functional extension of bone regeneration, the BU coordinates neural signal, regeneration of the circulatory network and remodeling of the bone matrix through the neural-bone metabolic coupling mechanism. Currently, effective strategies are lacking to remodel the homeostasis of the neural-bone metabolic coupling, which in turn leads to impaired BU regeneration. Here, we constructed a 3D-printed biomimetic hydrogel scaffold, GGMN-GSE, to synergistically couple nerve-bone metabolism and restore BU regeneration through electrophysiological microenvironment reconstruction and functional cell recruitment. The GGMN layer (Grooved GelMA@MXene@NGF) incorporates conductive MXene to emulate periosteal electrophysiology and features biomimetic microgrooves to guide neural orientation, collectively modulating neural-bone metabolic coupling. The GSE layer (GelMA@SVVYGLR-E7), engineered with a dual-targeting peptide, recruits BMSCs/EPCs to supply functional cells while remodeling the vasculo-osseous regenerative niche, synergistically driving osteogenic regeneration. In vitro, the GGMN-GSE scaffold promoted nerve fiber regeneration and induced secretion of neuropeptides such as CGRP, GHRH, and VIP, and activated <i>Calcrl, Ghr, Vipr</i>, and other receptors on the surface of BMSCs, driving BU regeneration. This effect was mediated by neural-bone metabolic coupling through the PI3K-Akt/STAT5 signaling axis. In vivo, compared with the control group, the density of CGRP<sup>+</sup> nerves in the GGMN-GSE group increased by 2.9-fold, the density of CD31<sup>+</sup> blood vessels in the GGMN-GSE group increased by 1.8-fold, the area of the neogenetic bone matrix expanded by 3.6-fold, and the BV/TV reached 97.1 % in the CT. Confocal analysis of rat calvarial defects established that GGMN-GSE scaffolds exclusively promoted synergistic 3D co-localization of neural networks, functionalized vasculature, and osseous tissue, which drove multi-scale BU regeneration. The 3D-printed scaffolds fabricated in this study effectively remodel neural-bone metabolic coupling homeostasis to treat critical bone defects.