A spatiotemporal atlas of senescence-associated secretory phenotype in fracture healing: stage-dependent mechanisms and therapeutic windows

衰老相关分泌表型在骨折愈合中的时空图谱:阶段依赖性机制和治疗窗口

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Abstract

Fracture repair remains a significant clinical challenge in orthopedics, particularly in aging populations. Accumulating evidence indicates that cellular senescence critically modulates the fracture microenvironment via the senescence-associated secretory phenotype (SASP). The SASP constitutes a complex secretory program of senescent cells that releases pro-inflammatory cytokines, growth factors, and matrix-modifying enzymes to reshape the surrounding microenvironment. Rather than being a random collection of molecules, the SASP represents a coordinated signaling network that can either promote tissue repair or drive chronic inflammation depending on its context. In this review, we apply a systematic SASP classification to the canonical four phases of fracture healing to clarify their distinct roles across these stages. During the inflammatory phase, SASP-associated (but non-exclusive) inflammatory cytokines and chemokines potentiate innate immune cell recruitment and early host defense, thereby initiating the repair cascade; in the soft-callus phase, chemotactic and angiogenic SASP components (such as CCL2, PDGF, VEGF) position mesenchymal progenitors and support chondrogenesis and neovascularization; in the hard-callus phase, osteoinductive growth factors and matrix-acting proteases (such as TGF-β, IGFBPs, MMP-9/13) promote cartilage-to-bone conversion and early mineral deposition; and in the remodeling phase, regulated SASP-mediated matrix changes couple osteoclast resorption with osteoblast formation, while sustained pro-inflammatory or profibrotic signals may hinder the fine remodeling of the structure. This stage-resolved framework elucidates the dual nature of SASP, with transient activation facilitating repair and sustained overproduction leading to impaired remodeling. This framework provides a conceptual basis for developing stage-specific interventions to enhance bone repair. Notably, many mediators discussed here overlap with the broader injury-induced inflammatory secretome and are not senescence-exclusive; where possible, we emphasize senescent-cell-enriched contributions and regulatory circuits rather than implying unique cellular origins.

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