Metzger Corinne E, Tak Landon Y, Scholz Samantha, Allen Matthew R
Department of Anatomy, Cell Biology and Physiology, Indiana University School of Medicine, Indianapolis, Indiana, United States of America.
Office for Research Compliance, Indiana University, Bloomington, Indiana, United States of America.
PLoS One. 2025 May 23;20(5):e0324628. doi: 10.1371/journal.pone.0324628. eCollection 2025.
High circulating parathyroid hormone (PTH) leading to secondary hyperparathyroidism is proposed to be a key driver of the skeletal phenotype of chronic kidney disease-mineral bone disorder (CKD-MBD) leading to high bone turnover and cortical bone deterioration. The association between high PTH and the skeletal phenotype is typically clearly demonstrated in preclinical models of CKD; however, clinical studies show the relationship between PTH and skeletal outcomes is not as clear. The clinical data have led to a proposed hyporesponsiveness to PTH in the CKD setting with unclear causes. In the current study, we assessed skeletally mature male C57BL/6J mice at 12-weeks and 21-weeks of adenine-induced CKD (Ad) with the second timepoint seven weeks longer than we have previously assessed. We found that serum BUN was high in Ad mice in both groups indicating the presence of kidney disease while PTH was higher in 21-wk Ad vs. 12-wk Ad. Despite the higher PTH, bone formation rate in 21-wk Ad mice was lower than 21-wk Ad mice. Additionally, immunohistochemical assessment of the PTH receptor, PTHR1, and RANKL, a key factor upregulated by PTH, showed a lower percentage of osteocytes positive for the proteins in 21-wk Ad vs. 12-wk Ad. Furthermore, regression analyses demonstrated a positive relationship between serum PTH and PTHR1 and RANKL at 12-weeks, but this relationship was lost by 21-weeks. Overall, these data indicate that prolonged exposure to continuously elevated PTH in adenine-induced CKD mice eventually led to an altered skeletal response indicating lower responsiveness of bone, particularly osteocytes, to the chronic PTH signal. This has implications for using PTH as a surrogate marker of bone outcomes in CKD as well as pointing to the need to better understand the time-based relationship between PTH and skeletal outcomes in CKD.
循环甲状旁腺激素(PTH)水平升高导致继发性甲状旁腺功能亢进,被认为是慢性肾脏病-矿物质和骨异常(CKD-MBD)骨骼表型的关键驱动因素,可导致高骨转换和皮质骨恶化。高PTH与骨骼表型之间的关联在CKD临床前模型中通常得到明确证实;然而,临床研究表明PTH与骨骼结局之间的关系并不那么清晰。临床数据提示在CKD环境中对PTH存在反应低下,原因尚不清楚。在本研究中,我们评估了12周龄和21周龄经腺嘌呤诱导的CKD(Ad)骨骼成熟的雄性C57BL/6J小鼠,第二个时间点比我们之前评估的时间长7周。我们发现两组Ad小鼠的血清尿素氮均较高,表明存在肾脏疾病,而21周龄Ad小鼠的PTH高于12周龄Ad小鼠。尽管PTH较高,但21周龄Ad小鼠的骨形成率低于12周龄Ad小鼠。此外,对PTH受体PTHR1和RANKL(一种由PTH上调的关键因子)的免疫组织化学评估显示,21周龄Ad小鼠中对这些蛋白呈阳性的骨细胞百分比低于12周龄Ad小鼠。此外,回归分析显示12周时血清PTH与PTHR1和RANKL之间呈正相关,但到21周时这种关系消失了。总体而言,这些数据表明,在腺嘌呤诱导的CKD小鼠中,长时间暴露于持续升高的PTH最终导致骨骼反应改变,表明骨骼尤其是骨细胞对慢性PTH信号的反应性降低。这对于将PTH用作CKD中骨骼结局的替代标志物具有启示意义,同时也指出需要更好地理解CKD中PTH与骨骼结局之间基于时间的关系。