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Manganese-Based Biofunctional 2D Nanosheets Enabled In Situ Macrophage Engineering for Precise Eradication of
Shengchang Zhang1, Huaijuan Zhou2, Bowen Chi3
1School of Medical Technology, Beijing Institute of Technology, Beijing, 100081, China.
Abstract:
Efficient treatment of osteomyelitis caused by Staphylococcus aureus is a great clinical challenge due to bacterial resistance and immune evasion issues. Macrophages play a crucial role in the fight against S. aureus but suffer from deficiencies in function in the infectious milieu leading to persistent infection. Here, a strategy of exploiting aged neutrophil membrane (aNM) is developed to camouflage 2D MnPSe3 nanosheets (MPS NSs), denoted as aNM@MPS, to mediate in situ macrophage engineering, thereby potentiating macrophages to eradicate refractory osteomyelitis. When administered systematically, the biofunctional aNM@MPS ensures selectivity for osteomyelitis lesions, enhanced bone marrow retention, and subsequent phagocytosis by macrophages. In the mouse model of osteomyelitis, the aNM@MPS enables dysfunctional macrophages to digest intracellular bacteria by generating highly toxic hydroxyl radicals and sequentially reprogramming bactericidal immunity through manganese ion-mediated immune activation, which synergistically terminates persistent infection-initiated pathological cascades and subsequently reestablish host-directed bactericidal potency, thereby conferring a satisfactory osteoprotective effect. These findings demonstrate that macrophages in the skeletal infectious milieu can be precisely remodeled via the lesion-macrophage dual-targeting metalloimmunotherapy strategy, which holds potential for osteomyelitis treatment.
Insights
This study engineered macrophages using aged neutrophil membrane-camouflaged nanosheets to treat Staphylococcus aureus osteomyelitis. This metalloimmunotherapy strategy effectively eradicated bacteria and protected bone in mice.
Area of Science:
- Biomaterials Science
- Immunology
- Nanomedicine
Background:
- Osteomyelitis caused by Staphylococcus aureus presents treatment challenges due to antibiotic resistance and bacterial immune evasion.
- Macrophages are critical in combating S. aureus but are functionally impaired in the infectious environment, leading to persistent infections.
Purpose of the Study:
- To develop a novel strategy for in situ macrophage engineering to enhance osteomyelitis treatment.
- To potentiate macrophages to eradicate refractory Staphylococcus aureus infections using a biomimetic nanosheet system.
Main Methods:
- Aged neutrophil membrane (aNM) was used to camouflage 2D MnPSe3 nanosheets (MPS NSs), creating aNM@MPS nanoparticles.
- Systemic administration of aNM@MPS targeted osteomyelitis lesions and was phagocytosed by macrophages.
- The in vivo efficacy was evaluated in a mouse model of osteomyelitis.
Main Results:
- aNM@MPS nanoparticles were selectively delivered to osteomyelitis lesions and enhanced macrophage retention.
- Macrophages treated with aNM@MPS generated hydroxyl radicals to digest intracellular bacteria.
- Manganese ion-mediated immune activation reprogrammed macrophage bactericidal immunity, synergistically terminating infection and promoting bone protection.
Conclusions:
- Macrophage engineering via lesion-macrophage dual-targeting metalloimmunotherapy is a promising strategy for treating refractory osteomyelitis.
- This approach remodels macrophages in the skeletal infectious milieu to restore host-directed bactericidal potency.
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