Research Paper Volume 14, Issue 21 pp 8856—8875

Polydatin administration attenuates the severe sublesional bone loss in mice with chronic spinal cord injury

Jiheng Zhan1,2,3,4,5, *, , Dan Luo1,3, *, , Bingde Zhao1, *, , Shudong Chen1,3, , Jiyao Luan6, , Junhua Luo5, , Yu Hou1,3,5, , Yonghui Hou1,3, *, , Wenke Xu1,5, , Wanying Yan7, , Ji Qi1,2,4,5, , Xing Li1,3, , Qing Zhang4,8, , Dingkun Lin1,2,3,5, &, ,

  • 1 Department of Orthopaedics, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510120, China
  • 2 Postdoctoral Workstation, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou 510120, China
  • 3 Research Team on the Prevention and Treatment of Spinal Degenerative Disease, Guangdong Provincial Academy of Chinese Medical Sciences, Guangzhou 510006, China
  • 4 Postdoctoral Research Station, Chinese Academy of Chinese Medical Sciences, Beijing 100700, China
  • 5 Second Clinical College, Guangzhou University of Chinese Medicine, Guangzhou 510405, China
  • 6 Luoyang Orthopedic-Traumatological Hospital of Henan Province (Henan Provincial Orthopedic Hospital), Zhengzhou 450046, China
  • 7 National Quality Testing Center for Processed Food, Guangzhou Inspection and Testing Certification Group Company Limited, Guangzhou 511447, China
  • 8 Department of Spine, Wangjing Hospital of Chinese Academy of Chinese Medical Sciences, Beijing 100102, China
* Equal contribution

Received: April 20, 2022       Accepted: October 27, 2022       Published: November 15, 2022      

https://doi.org/10.18632/aging.204382
How to Cite

Copyright: © 2022 Zhan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Background: Spinal cord injury (SCI) is often accompanied by rapid and extensive bone mineral loss below the lesion level, and there is currently no gold standard for treatment. Evidence suggests that polydatin (PLD) may help promote osteogenic differentiation and exhibit anti-osteoporotic activity. However, whether PLD could reverse substantial bone loss in SCI patients, especially those with protracted injury, and the underlying regulatory mechanism have not been investigated.

Study design: Male C57BL/6J mice were subjected to either contusion SCI or laminectomy at the T8-9 level. Eight weeks after SCI, PLD (40 mg/kg/day) or vehicle was administrated to the mice via the intragastric route for consecutive eight weeks. Blood was collected after the treatment regimen, and the tibiae and femora were removed. Bone marrow stromal cells were isolated from the long bones for ex vivo osteoblastogenesis and osteoclastogenesis assays.

Results: Chronic SCI led to a rapid and significant decrease in bone mineral density (BMD) of the distal femur and proximal tibia, resulting in structural deterioration of the bone tissues. Treatment with PLD largely restored BMD and bone structure. In addition, static histo-morphometric analysis revealed that PLD enhanced bone formation and inhibited bone resorption in vivo. PLD also promoted osteoblastogenesis and inhibited osteoclastogenesis ex vivo, which was accompanied by increased OPG/RANKL ratio, and reduced expression levels of CTR, TRAP, NFATc1 and c-Fos. However, PLD had no marked effect on serum 25(OH)D levels and VDR protein expression, although it did significantly lower serum and femoral malondialdehyde levels, inhibited expression level of matrix metallopeptidase 9 (MMP9), upregulated skeletal Wnt3a, Lrp5 and ctnnb1 mRNAs, and increased β-catenin protein expression.

Conclusions: PLD protected mice with chronic SCI against sublesional bone loss by modulating genes involved the differentiation and activity of osteoclasts and osteoblasts, abating oxidative stress and MMP activity, and restoring the Wnt/β-catenin signaling pathway.

Abbreviations

SCI: spinal cord injury; PLD: polydatin; 25(OH)D: 25-hydroxyvitamin D; OCN: osteocalcin; OPN: osteopontin; RUNX2: runt-related transcription factor 2; OPG: osteoprotegerin; RANKL: receptor-activator of nuclear factor κ-B ligand; CTR: calcitonin receptor; Wnt3a: wingless-related MMTV integration site 3A; SOST: sclerostin; Lrp5: lipoprotein receptor-related protein 5; CTX-1: C-terminal telopeptide of type I collagen; DPD: deoxypyridinoline; VDR: vitamin D receptor; BMD: bone mineral density; DEXA: dual-energy X-ray absorptiometry; μCT: micro-computed tomography; TRAP: tartrate-resistant acid phosphatase; NFATc1: nuclear factor of activated T cells 1; ALP: alkaline phosphatase; PCR: polymerase chain reaction; MDA: malondialdehyde; MMP-9: matrix-metalloproteinase-9.