Effect of collagen peptides from walleye pollock skin on bone microstructure of ovariectomized rats_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LIU Lu ¹ , JIN Lixin ² , YANG Jieru ³ , WU Binbin ⁴ , ZHANG Yimeng ³ , HAN Yantao ⁵ , WANG Chunbo ⁵ ,  XING Lifeng ⁴

1. Institute of Integrative Medicine, Qingdao University Medical College, Qingdao Shandong, 266021, P.R.China;
2. Department of Anatomy, Qingdao University Medical College, Qingdao Shandong, 266071, P.R.China;
3. School of Clinical Medicine, Qingdao University Medical College, Qingdao Shandong, 266071, P.R.China;
4. Department of Joint Surgery, Qingdao Haici Medical Group, Qingdao Shandong, 266033, P.R.China;
5. School of Pharmacy, Qingdao University, Qingdao Shandong, 266071, P.R.China;

Corresponding author：

XING Lifeng, Email: xlf329@126.com

Keywords：

Collagen peptides from walleye pollock skin; osteoporosis; calcitonin receptor; interleukin 1; bone microstructure; rat

DOI：

10.7507/1002-1892.201704130

Video：

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Objective To investigate the effect of collagen peptides from walleye pollock skin on the microstructure of osteoporosis model in ovariectomized rats, and to explore the feasibility of preventing and treating oste- oporosis. Methods Sixty adult Wistar female rats, weighing (250±10) g, were randomly divided into 5 groups (12 rats each group): normal group (group A), osteoporosis model group (group B), osteoporosis model+collagen peptides from walleye pollock skin prevention group (group C), osteoporosis model+low concentration of collagen peptides from walleye pollock skin treatment group (group D), and osteoporosis model+high concentration of collagen peptides from walleye pollock skin treatment group (group E). The rats in groups B, C, D, and E were removed bilateral ovarian to establish osteoporosis model. The rats in group C were treated with stomach perfusion of the collagen peptides from walleye pollock skin (1.0 g/kg) from 4 weeks after operation for 6 weeks; and the rats in groups D and E were treated with stomach perfusion of the collagen peptides from walleye pollock skin (0.5, 1.0 g/kg respectively) at 6 weeks after operation for 6 weeks. The rats in groups A and B were given equal volume of normal saline at the same time after operation. At 24 hours after the last administration, the femoral gray value of rats in groups A and B were measured by X-ray film; HE staining was performed on the proximal tibial bone of the left side in 4 groups; the histopathological changes of the bone were observed and the trabecular number (TN), mean trabecular plate thickness (MTPT), mean trabecular plate spacing (MTPS), trabecular bone volume (TBV), mean bone cortical thickness (MBCT) were measured; immunohistochemical staining was performed to observe the expression levels of caltitonin receptor (CTR) and interleukin 1 (IL-1). Results The femoral gray value of group B was significantly lower than that of group A (t=45.130, P=0.000), which indicated that the ovariectomized rat model was successfully prepared. Histological observation showed that TN, MTPS, TBV, and MBCT in groups A, C, and E were significantly different from those in group B (P<0.05). The histological parameters of bone tissue in group C were significantly different from those in groups D and E (P<0.05). TN, MTPS, TBV, and MBCT in group D were significantly different from those in group A (P<0.05); only MTPS in group E was significantly different from that in group A (P<0.05). MTPS, TBV, and MBCT in group E were significantly different from those in group D (P<0.05). The immunohistochemical staining showed that the levels of CTR and IL-1 in groups A, C, D, and E were lower than those in group B, in groups C and E were lower than in group D, showing significant differences (P<0.05). Conclusion Collagen peptides from walleye pollock skin can improve the bone microstructure of osteoporotic rats, and its mechanism may be related to the inhibition of CTR and IL-1 expression in bone tissue, but it has not been found to prevent osteoporosis.

Citation： LIU Lu, JIN Lixin, YANG Jieru, WU Binbin, ZHANG Yimeng, HAN Yantao, WANG Chunbo, XING Lifeng. Effect of collagen peptides from walleye pollock skin on bone microstructure of ovariectomized rats. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(10): 1214-1219. doi: 10.7507/1002-1892.201704130 Copy

1.	Pallagatti S, Parnami P, Sheikh S, et al. Efficacy of Panoramic Radiography in the Detection of Osteoporosis in Post-Menopausal Women When Compared to Dual Energy X-Ray Absorptiometry. Open Dent J, 2017, 11: 350-359.
2.	Kavitha MS, An SY, An CH, et al. Texture analysis of mandibular cortical bone on digital dental panoramic radiographs for the diagnosis of osteoporosis in Korean women. Oral Surg Oral Med Oral Pathol Oral Radiol, 2015, 119(3): 346-356.
3.	Shang DP, Lian HY, Fu DP, et al. Relationship between estrogen receptor 1 gene polymorphisms and postmenopausal osteoporosis of the spine in Chinese women. Genet Mol Res, 2016, 15(2): 1-6.
4.	吴彬, 张勇, 陈明亮, 等. 雌马酚对去卵巢后大鼠骨质疏松症的影响. 第三军医大学学报, 2015, 37(3): 256-260.0.
5.	周建烈, 陈悦. 水解胶原蛋白的骨骼和关节效应研究进展. 中国骨质疏松杂志, 2010, 16(10): 798-801.0.
6.	Li X, Shi F, Gong L, et al. Species-specific identification of collagen components in Colla corii asini using a nano-liquid chromatography tandem mass spectrometry proteomics approach. Int J Nanomedicine, 2017, 12: 4443-4454.
7.	Wu H, Ren C, Yang F, et al. Extraction and identification of collagen-derived peptides with hematopoietic activity from Colla Corii Asini. J Ethnopharmacol, 2016, 182: 129-136.
8.	Wang D, Ru W, Xu Y, et al. Chemical constituents and bioactivities of Colla corii asini. Drug Discov Ther, 2014, 8(5): 201-207.
9.	张鹤, 赵雨, 徐云凤, 等. 鹿骨胶原蛋白对去卵巢所致骨质疏松大鼠的治疗作用. 中药药理与临床, 2011, 27(5): 76-79.0.
10.	樊洁, 张德岩, 苗德深, 等. 狭鳕鱼皮胶原多肽理化性质研究. 青岛大学医学院学报, 2013, 49(6): 479-481.0.
11.	薛玲芳, 陈雪红, 徐宏伟, 等. 狭鳕鱼皮胶原肽对过氧化氢诱导的人成骨细胞氧化损伤作用. 安徽农业科学, 2016, 44(25): 142-145.0.
12.	卢玉坤. 鳕鱼皮胶原蛋白肽的促钙吸收作用研究. 青岛: 中国海洋大学, 2013.
13.	Guo L, Harnedy PA, Zhang L, et al. In vitro assessment of the multifunctional bioactive potential of Alaska pollock skin collagen following simulated gastrointestinal digestion. J Sci Food Agric, 2015, 95(7): 1514-1520.
14.	Beaudreuil J, Taboulet J, Orcel P, et al. Calcitonin receptor mRNA in mononuclear leucocytes from postmenopausal women: decrease during osteoporosis and link to bone markers with specific isoform involvement. Bone, 2000, 27(1): 161-168.
15.	Lin CC, Li TC, Liu CS, et al. Associations of TNF-α and IL-6 polymorphisms with osteoporosis through joint effects and interactions with LEPR gene in Taiwan: Taichung Community Health Study for Elders (TCHS-E). Mol Biol Rep, 2016, 43(10): 1179-1191.
16.	Xu J, Gao Y, Yin J, et al. Calcitonin receptor gene polymorphism in cCinese Xinjiang Han and Uygur women with primary osteoporosis. J Nutr Health Aging, 2014, 18(2): 204-208.
17.	Ito A, Yoshimura M. Mechanisms of the analgesic effect of calcitonin on chronic pain by alteration of receptor or channel expression. Mol Pain, 2017, 13: 1744806917720316.
18.	柴建胜, 邓高荣, 黄巍. 降钙素受体在去势大鼠骨质疏松模型组织中的分布. 医学信息, 2013, 26(10 上): 141.0.
19.	Gardner CR. Morphological analysis of osteoclastogenesis induced by RANKL in mouse bone marrow cell cultures. Cell Biol Int, 2007, 31(7): 672-682.
20.	Mancini L, Paul-Clark MJ, Rosignoli G, et al. Calcitonin and prednisolone display antagonistic actions on bone and have synergistic effects in experimental arthritis. Am J Pathol, 2007, 170(3): 1018-1027.
21.	Brandström H, Jonsson KB, Ohlsson C, et al. Regulation of osteoprotegerin mRNA levels by prostaglandin E2 in human bone marrow stroma cells. Biochem Biophys Res Commun, 1998, 247(2): 338-341.
22.	Li H, Cuartas E, Cui W, et al. IL-1 receptor-associated kinase M is a central regulator of osteoclast differentiation and activation. J Exp Med, 2005, 201(7): 1169-1177.
23.	李晓红, 司红羚, 刘啸晨. 雌激素对骨质疏松大鼠牙槽骨改建过程中 IL-1 表达的影响. 实用口腔医学杂志, 2006, 22(5): 684-687.0.
24.	Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med, 1995, 332(5): 305-311.

1. Pallagatti S, Parnami P, Sheikh S, et al. Efficacy of Panoramic Radiography in the Detection of Osteoporosis in Post-Menopausal Women When Compared to Dual Energy X-Ray Absorptiometry. Open Dent J, 2017, 11: 350-359.
2. Kavitha MS, An SY, An CH, et al. Texture analysis of mandibular cortical bone on digital dental panoramic radiographs for the diagnosis of osteoporosis in Korean women. Oral Surg Oral Med Oral Pathol Oral Radiol, 2015, 119(3): 346-356.
3. Shang DP, Lian HY, Fu DP, et al. Relationship between estrogen receptor 1 gene polymorphisms and postmenopausal osteoporosis of the spine in Chinese women. Genet Mol Res, 2016, 15(2): 1-6.
4. 吴彬, 张勇, 陈明亮, 等. 雌马酚对去卵巢后大鼠骨质疏松症的影响. 第三军医大学学报, 2015, 37(3): 256-260.0.
5. 周建烈, 陈悦. 水解胶原蛋白的骨骼和关节效应研究进展. 中国骨质疏松杂志, 2010, 16(10): 798-801.0.
6. Li X, Shi F, Gong L, et al. Species-specific identification of collagen components in Colla corii asini using a nano-liquid chromatography tandem mass spectrometry proteomics approach. Int J Nanomedicine, 2017, 12: 4443-4454.
7. Wu H, Ren C, Yang F, et al. Extraction and identification of collagen-derived peptides with hematopoietic activity from Colla Corii Asini. J Ethnopharmacol, 2016, 182: 129-136.
8. Wang D, Ru W, Xu Y, et al. Chemical constituents and bioactivities of Colla corii asini. Drug Discov Ther, 2014, 8(5): 201-207.
9. 张鹤, 赵雨, 徐云凤, 等. 鹿骨胶原蛋白对去卵巢所致骨质疏松大鼠的治疗作用. 中药药理与临床, 2011, 27(5): 76-79.0.
10. 樊洁, 张德岩, 苗德深, 等. 狭鳕鱼皮胶原多肽理化性质研究. 青岛大学医学院学报, 2013, 49(6): 479-481.0.
11. 薛玲芳, 陈雪红, 徐宏伟, 等. 狭鳕鱼皮胶原肽对过氧化氢诱导的人成骨细胞氧化损伤作用. 安徽农业科学, 2016, 44(25): 142-145.0.
12. 卢玉坤. 鳕鱼皮胶原蛋白肽的促钙吸收作用研究. 青岛: 中国海洋大学, 2013.
13. Guo L, Harnedy PA, Zhang L, et al. In vitro assessment of the multifunctional bioactive potential of Alaska pollock skin collagen following simulated gastrointestinal digestion. J Sci Food Agric, 2015, 95(7): 1514-1520.
14. Beaudreuil J, Taboulet J, Orcel P, et al. Calcitonin receptor mRNA in mononuclear leucocytes from postmenopausal women: decrease during osteoporosis and link to bone markers with specific isoform involvement. Bone, 2000, 27(1): 161-168.
15. Lin CC, Li TC, Liu CS, et al. Associations of TNF-α and IL-6 polymorphisms with osteoporosis through joint effects and interactions with LEPR gene in Taiwan: Taichung Community Health Study for Elders (TCHS-E). Mol Biol Rep, 2016, 43(10): 1179-1191.
16. Xu J, Gao Y, Yin J, et al. Calcitonin receptor gene polymorphism in cCinese Xinjiang Han and Uygur women with primary osteoporosis. J Nutr Health Aging, 2014, 18(2): 204-208.
17. Ito A, Yoshimura M. Mechanisms of the analgesic effect of calcitonin on chronic pain by alteration of receptor or channel expression. Mol Pain, 2017, 13: 1744806917720316.
18. 柴建胜, 邓高荣, 黄巍. 降钙素受体在去势大鼠骨质疏松模型组织中的分布. 医学信息, 2013, 26(10 上): 141.0.
19. Gardner CR. Morphological analysis of osteoclastogenesis induced by RANKL in mouse bone marrow cell cultures. Cell Biol Int, 2007, 31(7): 672-682.
20. Mancini L, Paul-Clark MJ, Rosignoli G, et al. Calcitonin and prednisolone display antagonistic actions on bone and have synergistic effects in experimental arthritis. Am J Pathol, 2007, 170(3): 1018-1027.
21. Brandström H, Jonsson KB, Ohlsson C, et al. Regulation of osteoprotegerin mRNA levels by prostaglandin E2 in human bone marrow stroma cells. Biochem Biophys Res Commun, 1998, 247(2): 338-341.
22. Li H, Cuartas E, Cui W, et al. IL-1 receptor-associated kinase M is a central regulator of osteoclast differentiation and activation. J Exp Med, 2005, 201(7): 1169-1177.
23. 李晓红, 司红羚, 刘啸晨. 雌激素对骨质疏松大鼠牙槽骨改建过程中 IL-1 表达的影响. 实用口腔医学杂志, 2006, 22(5): 684-687.0.
24. Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med, 1995, 332(5): 305-311.

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