journal article·2024-01-02Open access

dECM restores macrophage immune homeostasis and alleviates iron overload to promote DTPI healing

Ju Zhang, Ruijuan Si, Yu Gao, Hui Shan, Qi Su, Zujian Feng, Pingsheng Huang, Deling Kong, Weiwei Wang

Abstract

Abstract Due to its highly insidious and rapid progression, deep tissue pressure injury (DTPI) is a clinical challenge. Our previous study found that DTPI may be a skeletal muscle injury dominated by macrophage immune dysfunction due to excessive iron accumulation. Decellularized extracellular matrix (dECM) hydrogel promotes skeletal muscle injury repair. However, its role in polarizing macrophages and regulating iron metabolism in DTPI remains unclear. Here, porcine dECM hydrogel was prepared, and its therapeutic function and mechanism in repairing DTPI were investigated. The stimulus of dECM hydrogel toward RAW264.7 cells resulted in a significantly higher percentage of CD206+ macrophages and notably decreased intracellular divalent iron levels. In mice DTPI model, dECM hydrogel treatment promoted M1 to M2 macrophage conversion, improved iron metabolism and reduced oxidative stress in the early stage of DTPI. In the remodeling phase, the dECM hydrogel remarkably enhanced revascularization and accelerated skeletal muscle repair. Furthermore, the immunomodulation of dECM hydrogels in vivo was mainly involved in the P13k/Akt signaling pathway, as revealed by GO and KEGG pathway analysis, which may ameliorate the iron deposition and promote the healing of DTPI. Our findings indicate that dECM hydrogel is promising in skeletal muscle repair, inflammation resolution and tissue injury healing by effectively restoring macrophage immune homeostasis and normalizing iron metabolism.
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Research context

OpenAlex topics: Tissue Engineering and Regenerative Medicine · Muscle and Compartmental Disorders · Electrospun Nanofibers in Biomedical Applications

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

Affiliations

Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin 300192 ,

School of Nursing, Qingdao University, Ningde Road, Shinan District, Qingdao, Shandong, 266071,

Cancer Hospital of Tianjin Medical University , North Huanhu West Road , Tianjin,

The Affiliated Hospital of Qingdao University , 16 Jiangsu Road, Shinan District , Qingdao,

Nankai Univerisy , Tianjin, 300071,

Funding

National Natural Science Foundation of China

References (47)

Show source-provided references
1. Challenges and new therapeutic approaches in managing chronic wounds10.2174/1389450121666200623131200 ↗
2. Chronic wounds: evaluation and management
4. Deep tissue pressure injury: a clinical review10.1097/01.NAJ.0000516273.66604.c7 ↗
5. Deep tissue injury: what is it?10.1097/01.ASW.0000426712.72787.f3 ↗
6. Ischemia/reperfusion injury following acute myocardial infarction: a critical issue for clinicians and forensic pathologists10.1155/2017/7018393 ↗
7. Understanding the connection between common stroke comorbidities, their associated inflammation, and the course of the cerebral ischemia/reperfusion Cascade10.3389/fimmu.2021.782569 ↗
8. Disulfiram ameliorates ischemia/reperfusion-induced acute kidney injury by suppressing the caspase-11-GSDMD pathway10.1080/0886022X.2022.2098764 ↗
9. Ferroptosis: a novel therapeutic target for ischemia-reperfusion injury10.3389/fcell.2021.688605 ↗
10. Deferoxamine inhibits oxidative stress response to promote wound healing of deep tissue pressure injury in mice
11. More than a duologue: in-depth insights into epi transcriptomics and ferroptosis10.3389/fcell.2022.982606 ↗
12. Regulation of tissue iron homeostasis: the macrophage “ferrostat”10.1172/jci.insight.132964 ↗
13. Polarization dictates iron handling by inflammatory and alternatively activated macrophages10.3324/haematol.2010.023879 ↗
14. A precious metal: iron, an essential nutrient for all cells10.1007/BF02829934 ↗
15. Iron levels in polarized macrophages: regulation of immunity and autoimmunity10.1016/j.autrev.2012.03.003 ↗
16. An unrestrained pro-inflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice10.1172/JCI44490 ↗
17. Extracellular matrix-based strategies for immunomodulatory biomaterials engineering10.1002/adhm.201801578 ↗
18. Decellularized extracellular matrix materials for cardiac repair and regeneration10.1002/adhm.201801217 ↗
19. Injectable skeletal muscle matrix hydrogel promotes neovascularization and muscle cell infiltration in a hindlimb ischemia model10.22203/eCM.v023a31 ↗
20. Dose optimization of decellularized skeletal muscle extracellular matrix hydrogels for improving perfusion and subsequent validation in an aged hindlimb ischemia model10.1039/C9BM01963D ↗
21. Injectable extracellular matrix hydrogels as scaffolds for spinal cord injury repair10.1089/ten.tea.2015.0422 ↗
22. Intramuscular injection of skeletal muscle derived extracellular matrix mitigates denervation atrophy after sciatic nerve transection10.1177/20417314211032491 ↗
23. Development of a simple, noninvasive, clinically relevant model of pressure ulcers in the mouse10.1080/08941930490472046 ↗
24. The role of iron in the skin and cutaneous wound healing10.3389/fphar.2014.00156 ↗
25. Pathophysiology of venous ulceration10.1016/j.jvsv.2017.03.015 ↗
26. Heme-scavenging role of alpha1-microglobulin in chronic ulcers10.1046/j.1523-1747.2003.12409.x ↗
27. Does localized iron loss in venous disease lead to systemic iron deficiency? A descriptive pilot study10.1111/wrr.12769 ↗
28. Dermal extracellular matrix-derived hydrogels as an in vitro substrate to study mast cell maturation10.1089/ten.tea.2020.0142 ↗
29. Extracellular matrix hydrogel derived from bovine bone is biocompatible in vitro and in vivo
30. Periosteal matrix-derived hydrogel promotes bone repair through an early immune regulation coupled with enhanced angio- and osteogenesis10.1016/j.biomaterials.2019.119552 ↗
31. Macrophage involvement in aging-associated skeletal muscle regeneration10.3390/cells12091214 ↗
32. Integrin-mediated interactions control macrophage polarization in 3D hydrogels10.1002/adhm.201700289 ↗
33. Laminin therapy for the promotion of muscle regeneration10.1016/j.febslet.2015.10.004 ↗
34. Macrophage and fibroblast interactions in biomaterial-mediated fibrosis10.1002/adhm.201801451 ↗
35. IL-1 beta-mediated macrophage-hepatocyte crosstalk upregulates hepcidin under physiological low oxygen levels10.1016/j.redox.2019.101209 ↗
36. Role of the PI3K/AKT (mTOR and GSK3β) signalling pathway and photobiomodulation in diabetic wound healing10.1016/j.cytogfr.2019.03.001 ↗
37. Overexpression of the miR-141/200c cluster promotes the migratory and invasive ability of triple-negative breast cancer cells through the activation of the FAK and PI3K/AKT signaling pathways by secreting VEGF-A10.1186/s12885-016-2620-7 ↗
38. Transforming growth factor β (TGF-β) receptor signaling regulates kinase networks and phosphatidylinositol metabolism during T-cell activation10.1074/jbc.RA120.012572 ↗
39. AKT as a therapeutic target for cancer10.1158/0008-5472.CAN-18-2738 ↗
40. Arctigenin inhibits glioblastoma proliferation through the AKT/mTOR pathway and induces autophagy10.1155/2020/3542613 ↗
41. Cellular and molecular mechanisms of fibrosis10.1002/path.2277 ↗
42. Targeting PI3K/AKT/mTOR-mediated autophagy for tumor therapy10.1007/s00253-019-10257-8 ↗
43. Cross talk between autophagy and apoptosis contributes to ZnO nanoparticle-induced human osteosarcoma cell death10.1002/adhm.201800332 ↗
44. Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways10.1080/15548627.2015.1023981 ↗
45. m(6)A reader YTHDC1 modulates autophagy by targeting SQSTM1 in diabetic skin10.1080/15548627.2021.1974175 ↗
46. AGEs induced autophagy impairs cutaneous wound healing via stimulating macrophage polarization to M1 in diabetes10.1038/srep36416 ↗
47. Diabetic sarcopenia: metabolic and molecular appraisal10.1007/s00592-022-01883-2 ↗