Age-related functional deterioration of medullary bone is linked with senescent bone marrow microenvironment in laying hens

doi:10.1016/j.jia.2025.10.016

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Xujie Liao¹, Aoze Wang¹, Shutong Wang¹, Wanting Zhao¹, Jionghao Chen¹, Nan Wang², Menglin Wang², Jiakun Yan¹, Yanli Liu¹, Xin Yang¹, Xiaojun Yang^1#, Zhouzheng Ren^1#

¹ College of Animal Science and Technology, Northwest A&F University, Yangling 712100, China

2 Xinjiang Tiankang Feed Co., Ltd., Urumqi, Xinjiang, China 831300

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摘要

产蛋后期破蛋问题是蛋鸡产业共性难题。髓质骨是蛋壳形成的重要“钙库”，老龄蛋鸡髓质骨成骨机能减退，导致“钙库”功能下降，是破蛋问题的生理根源。解析老龄蛋鸡髓质骨功能的变化特征及其内在原因，对于优化产蛋后期蛋壳品质，延长蛋鸡生产周期，具有重要意义。选取48、61、74和87周龄海兰褐产蛋鸡各12只，记录蛋壳质量并屠宰采集血清和股骨样本，重点围绕髓质骨矿化参数、髓质骨“动员-重塑”机能、骨髓腔微环境衰老特征、骨髓腔脂肪沉积等层面揭示周龄增长过程中蛋鸡“钙库”的功能变化情况。结果表明：（1）与48和61周龄蛋鸡相比，74和87周龄蛋鸡的蛋壳质量（蛋壳厚度、蛋壳强度、蛋比重和蛋壳指数）显著降低（P<0.05）。（2）微计算机断层扫描（Micro-CT）显示，随周龄增长，蛋鸡股骨矿化参数逐渐恶化（P<0.05）。（3）与48周龄蛋鸡相比，61、74和87周龄蛋鸡的髓质骨成骨机能显著降低；主要表现为，血清碱性磷酸酶水平显著降低（P<0.05），髓质骨成骨相关标志物（RUNX2、OPN、ALPL）的蛋白表达显著降低（P<0.05）。（4）与48和74周龄蛋鸡相比，87周龄蛋鸡破骨相关标志物（TRAP）的蛋白表达显著增加（P<0.05）。（5）与其他周龄蛋鸡相比，87周龄蛋鸡股骨表现出更高的衰老相关分泌表型（SASP）的基因表达（P<0.05）。（6）与48和61周龄蛋鸡相比，74和87周龄蛋鸡股骨表现出明显的衰老特征，主要表现为股骨衰老标志物的蛋白表达（γ-H2A.X、GLB1和p53）显著增加（P<0.05）。（7）与48周龄蛋鸡相比，61、74和87周龄蛋鸡股骨具有更多的脂肪沉积（P<0.05）；进一步支持骨髓间充质干细胞趋向于成脂分化而非成骨分化。本研究系统揭示了周龄增长过程中老龄蛋鸡髓质骨矿化机能和骨髓腔微环境的变化特征及其相互关联，发现老龄蛋鸡骨髓腔微环境衰老可能是导致髓质骨矿化功能衰退及蛋壳品质下降的重要因素，为蛋鸡周龄增长过程中影响其蛋壳质量的关键年龄段与生理指标的确定提供了理论依据。

Abstract

Medullary bone is a labile calcium store for eggshell deposition. The dysfunctional mineralization function of medullary bone in aged laying hens leads to decreased eggshell mineralization and increased egg breakage. Understanding the mechanisms underlying age-related decline in medullary bone mineralization function is critical for developing novel strategies to improve eggshell quality in aged laying hens. Hy-Line Brown laying hens were sampled at different ages (48, 61, 74, and 87 wk of age; n=12 at each age). Analyses were conducted to determine the effect of aging on eggshell mineralization, medullary bone remodeling, and physiological and molecular biological parameters for bone marrow microenvironment senescence. The results showed that: (1) compared with 48- and 61-wk-old la`ying hens, 74- and 87-wk-old laying hens had decreased (P<0.05) eggshell quality; (2) micro computed tomography scans illustrated a progressive decrease (P<0.05) with age in femoral mineralization; (3) compared with 48-wk-old laying hens, 61-, 74- and 87-wk-old laying hens had decreased (P<0.05) osteoblastic function, characterized by decreased serum alkaline phosphatase levels and decreased protein expression of osteogenic markers (runt-related transcription factor 2, osteopontin and alkaline phosphatase) of femoral medullary bone; (4) compared with 48- and 74-wk-old laying hens, 87-wk-old laying hens had increased (P<0.05) protein expression of osteoclastic marker (tartrate resistant acid phosphatase) of femoral medullary bone; (5) compared with other ages, 87-wk-old laying hens had increased (P<0.05) mRNA expression of senescence-associated secretory phenotype in the femoral marrow microenvironment; (6) compared with 48- and 61-wk-old laying hens, 74- and 87-wk-old laying hens had increased (P<0.05) protein expression of senescence biomarkers (gamma H2A.X, galactosidase beta 1 and tumor suppressor protein 53) in the femoral marrow microenvironment; (7) compared with 48-wk-old laying hens, 61-, 74- and 87-wk-old laying hens had increased (P<0.05) femoral adipose deposition. Age-related decline in mineralization function of medullary bone was accompanied by an uncoupling of medullary bone osteoblastic and osteoclastic functions, which may link to a senescent femoral marrow microenvironment in aged laying hens. Methods are needed to monitor and manage the bone marrow microenvironment in the later laying periods.

Keywords: aged laying hens eggshell quality bone marrow microenvironment medullary bone senescence

Online: 01 November 2025

Fund:

This study was financially supported by National Natural Science Foundation of China (32172759), Wujiaqu Science and Technology Bureau (2023-2319), Xianyang Science and Technology Bureau, China (L2024-ZDKJ-ZDCGZH-0007), and Shaanxi Provincial Department of Science and Technology, China (2023KXJ-243).

About author: Xujie Liao, E-mail: liaoxujie2000@163.com; Correspondence Zhouzheng Ren, Tel: +86-029-87092164, E-mail: poultryren@nwafu.edu.cn; Xiaojun Yang, Tel: +86-029-87080018, E-mail: yangxj@nwsuaf.edu.cn

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Xujie Liao, Aoze Wang, Shutong Wang, Wanting Zhao, Jionghao Chen, Nan Wang, Menglin Wang, Jiakun Yan, Yanli Liu, Xin Yang, Xiaojun Yang, Zhouzheng Ren. 2025. Age-related functional deterioration of medullary bone is linked with senescent bone marrow microenvironment in laying hens. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.10.016

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