journal article·2026-10Open access

Bioelectric signals promote diabetic bone regeneration through Piezo1-mediated activation of the efferocytic immune microenvironment

Dilixiati Duolikun, Lei Zhang, Tianlong Wang, Xinhui Wu, Xuran Guo, Waheed Muhammad Zeeshan, Zhiqing Liu, Haijun Zhang, Jinhui Zhao, Longpo Zheng

Abstract

Defective macrophage efferocytosis sustains inflammation and compromises bone repair in diabetic defects, yet strategies that restore efferocytic immune homeostasis remain limited. Here, we engineered an ultrasound-responsive piezoelectric hydrogel (Gel BC@ZnO) by incorporating zinc oxide (ZnO) nanoparticles into a bacterial cellulose (BC)-reinforced gelatin methacryloyl (GelMA) network to provide localized bioelectric cues. Gel BC@ZnO exhibited good cytocompatibility, structural stability, and robust ultrasound-triggered piezoelectric output. Under diabetic-mimicking conditions, ultrasound activation generated bioelectric signals that engaged Piezo1, induced Piezo1-dependent Ca 2+ influx, and rescued macrophage efferocytosis. This efferocytic reactivation attenuated ROS accumulation, shifted macrophages toward a pro-regenerative phenotype, enhanced osteogenic differentiation, and suppressed osteoclast genesis, thereby restoring bone-remodeling homeostasis. In a diabetic femoral condyle defect model, Gel BC@ZnO combined with ultrasound accelerated bone repair, increased local Piezo1 expression, promoted collagen deposition and osteogenic marker expression, and rebuilt a favorable immune microenvironment. These results define a bioelectric signal-Piezo1-Ca 2+ -efferocytosis axis for diabetic bone regeneration and establish a non-invasive, ultrasound-controllable immunomodulatory strategy for compromised bone repair.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Planarian Biology and Electrostimulation · Erythrocyte Function and Pathophysiology · MicroRNA in disease regulation

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (68)

Show source-provided references
1. IDF Diabetes Atlas: global, regional and country-level diabetes prevalence estimates for 2021 and projections for 204510.1016/j.diabres.2021.109119 ↗
2. Update on the pathogenesis and treatment of skeletal fragility in type 2 diabetes mellitus, Nature reviews
3. Mechanisms of diabetes mellitus-induced bone fragility, Nature reviews
4. The effects of type 1 and type 2 diabetes mellitus on bone health in chronic kidney disease, Nature reviews
5. Human blood vessel organoids as a model of diabetic vasculopathy10.1038/s41586-018-0858-8 ↗
6. Targeting innate immune mediators in type 1 and type 2 diabetes10.1038/s41577-019-0213-9 ↗
7. Macrophage-Targeted efferocytosis therapy promotes diabetic wound healing via cellular level debridement
8. The clearance of dead cells by efferocytosis10.1038/s41580-020-0232-1 ↗
9. Efferocytosis induces a novel SLC program to promote glucose uptake and lactate release10.1038/s41586-018-0735-5 ↗
10. Efferocytosis induces macrophage proliferation to help resolve tissue injury10.1016/j.cmet.2021.10.015 ↗
11. Efferocytosis drives a tryptophan metabolism pathway in macrophages to promote tissue resolution10.1038/s42255-024-01115-7 ↗
12. Hyperglycemia exacerbates osteoarthritis by impairing macrophage efferocytosis through modulation of CD11b lactylation
13. Efferocytosis in inflammatory bone disorders10.1016/j.tips.2025.04.001 ↗
14. Microenvironment-based diabetic foot ulcer nanomedicine10.1002/advs.202203308 ↗
15. Manganese-based polyoxometalate nanozyme-metformin Co-functionalized Hydrogel promotes diabetic wound regeneration by enhancing phagocyte efferocytosis10.34133/research.0964 ↗
16. Turmeric-derived nanoparticles functionalized aerogel regulates multicellular networks to promote diabetic wound healing10.1002/advs.202307630 ↗
17. The mechanosensitive Piezo1 channel is required for bone formation10.7554/eLife.47454 ↗
18. A novel Piezo1 agonist promoting mesenchymal stem cell proliferation and osteogenesis to attenuate disuse osteoporosis
19. Three-dimensionally printed Ti2448 with low stiffness enhanced angiogenesis and osteogenesis by regulating macrophage polarization via Piezo1/YAP signaling axis10.3389/fcell.2021.750948 ↗
20. Piezo1 inactivation in chondrocytes impairs trabecular bone formation10.1002/jbmr.4198 ↗
21. Mechanosensitive channel Piezo1 is an essential regulator in cell cycle progression of optic nerve head astrocytes10.1002/glia.24334 ↗
22. Piezo1-mediated mechanotransduction regulates diabetic osteoporosis and hyperglycemia via low-intensity pulsed ultrasound10.1016/j.bone.2025.117664 ↗
23. Mechanical sensing protein PIEZO1 regulates bone homeostasis via osteoblast-osteoclast crosstalk10.1038/s41467-019-14146-6 ↗
24. Rehabilitation exercise-driven symbiotic electrical stimulation system accelerating bone regeneration10.1126/sciadv.adi6799 ↗
25. Exercise-induced piezoelectric stimulation for cartilage regeneration in rabbits10.1126/scitranslmed.abi7282 ↗
26. Piezoelectric hydrogel with self-powered biomechanical stimulation enhances bone regeneration10.1016/j.actbio.2025.02.016 ↗
27. Review of zinc oxide piezoelectric nanogenerators: piezoelectric properties, composite structures and power output10.3390/s23083859 ↗
28. 3D-printed zinc oxide nanoparticles modified barium titanate/hydroxyapatite ultrasound-responsive piezoelectric ceramic composite scaffold for treating infected bone defects
29. NanoZnO-modified titanium implants for enhanced anti-bacterial activity, osteogenesis and corrosion resistance10.1186/s12951-021-01099-6 ↗
30. Fiber reinforced GelMA hydrogel to induce the regeneration of corneal stroma10.1038/s41467-020-14887-9 ↗
31. Extracellular vesicles secreted by LRP1(+) ligament-derived stem cells promote tendon-bone healing after ACL reconstruction via miR-708-5p/Bambi axis10.1016/j.biomaterials.2026.123977 ↗
32. Reinforcing gelatin hydrogels via in situ phase separation and enhanced interphase bonding for advanced 3D fabrication10.1002/adma.202416432 ↗
33. Bio-orthogonal functionalization of bacterial cellulose combining metabolic glycoengineering and click chemistry
34. Unraveling the biosynthesis and regulation mechanism of bacterial cellulose: challenges and strategies toward industrial production10.1016/j.carbpol.2026.124891 ↗
35. Cartilage structure-inspired nanofiber-hydrogel composite with robust proliferation and stable chondral lineage-specific differentiation function to orchestrate cartilage regeneration for artificial tracheal construction
36. 0D/1D heterojunction implant with electro-mechanobiological coupling cues promotes osteogenesis
37. Mineralized enzyme-based biomaterials with superior bioactivities for bone regeneration10.1021/acsami.2c05794 ↗
38. Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels10.1016/j.biomaterials.2015.08.045 ↗
39. A high performance nanocellulose-PVDF based piezoelectric nanogenerator based on the highly active CNF@ZnO via electrospinning technology10.1016/j.nanoen.2024.109741 ↗
40. Ultrasound-driven electrical stimulation based on 3D hierarchical porous piezoelectric nanofiber-aerogel scaffold promotes bone defect repair10.1016/j.cej.2023.144305 ↗
41. Hypoxia-mimicking 3D bioglass-nanoclay scaffolds promote endogenous bone regeneration
42. Stimulation of Piezo1 by mechanical signals promotes bone anabolism10.7554/eLife.49631 ↗
43. Multiscale profiling of tyrosine kinase inhibitor cardiotoxicity reveals mechanosensitive ion channel PIEZO1 as cardioprotective10.1126/scitranslmed.adv9403 ↗
44. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity10.1038/s41586-019-1485-8 ↗
45. Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing10.1038/s41467-021-23482-5 ↗
46. An ultrasound-driven PLGA/Zn-KNN hybrid piezoelectric scaffold with direct and immunoregulatory antibacterial activity for bone infection
47. Piezo1 channel activation in response to mechanobiological acoustic radiation force in osteoblastic cells10.1038/s41413-020-00124-y ↗
48. The Sirt1-Piezo1 axis promotes bone formation and repair in mice10.1002/advs.202510103 ↗
49. Mechanosensitive ion channels as novel targets in osteoporosis
50. Nano-zinc oxide (nZnO) targets the AMPK-ULK1 pathway to promote bone regeneration10.1186/s13287-025-04322-5 ↗
51. Sustained zinc release in cooperation with CaP scaffold promoted bone regeneration via directing stem cell fate and triggering a pro-healing immune stimuli10.1186/s12951-021-00956-8 ↗
52. Specialized roles for actin in osteoclasts: unanswered questions and therapeutic opportunities10.3390/biom9010017 ↗
53. Zinc stimulates osteoblastogenesis and suppresses osteoclastogenesis by antagonizing NF-κB activation10.1007/s11010-011-0852-z ↗
54. Zinc inhibits osteoclast differentiation by suppression of Ca2+-Calcineurin-NFATc1 signaling pathway10.1186/1478-811X-11-74 ↗
55. Ultrasound-responsive piezoelectric membrane promotes osteoporotic bone regeneration via the "Two-Way Regulation" bone homeostasis strategy10.1002/advs.202504293 ↗
56. Mild hyperthermia accelerates bone repair by dynamically regulating iNOS/Arg1 balance in the early stage10.1002/advs.202409882 ↗
57. Enhanced corrosion resistance of zinc-containing nanowires-modified titanium surface under exposure to oxidizing microenvironment10.1186/s12951-019-0488-9 ↗
58. PFKFB2-mediated glycolysis promotes lactate-driven continual efferocytosis by macrophages10.1038/s42255-023-00736-8 ↗
59. The multifaceted roles of macrophages in bone regeneration: a story of polarization, activation and time10.1016/j.actbio.2021.04.052 ↗
60. Activating macrophage continual efferocytosis via microenvironment biomimetic short fibers for reversing inflammation in bone repair10.1002/adma.202402968 ↗
61. Mild photothermal-stimulation based on injectable and photocurable hydrogels orchestrates immunomodulation and osteogenesis for high-performance bone regeneration10.1002/smll.202300111 ↗
62. Smart-responsive multifunctional therapeutic system for improved regenerative microenvironment and accelerated bone regeneration via mild photothermal therapy10.1002/advs.202304641 ↗
63. Bioinspired soft-hard combined system with mild photothermal therapeutic activity promotes diabetic bone defect healing via synergetic effects of immune activation and angiogenesis10.7150/thno.97335 ↗
64. Multifunctional injectable hydrogel system as a mild photothermal-assisted therapeutic platform for programmed regulation of inflammation and osteo-microenvironment for enhanced healing of diabetic bone defects in situ10.7150/thno.102779 ↗
65. Polyphenol-derived Nanoarmor-Functionalized photothermal hydrogel platform for programmed modulation of the regenerative microenvironment and bone defect healing10.1002/smll.202510733 ↗
66. Biomaterials for diabetic bone repair: influencing mechanisms, multi-aspect progress and future prospects10.1016/j.compositesb.2024.111282 ↗
67. A review of the clinical side effects of bone morphogenetic Protein-2, tissue engineering
68. Injectable short-fiber hydrogel with fatigue resistance and antibacterial properties for synergistic periodontitis therapy10.1016/j.cej.2025.166298 ↗