Anti-osteoporosis; Bone mineral density; Bone turnover markers; Chondroitin sulfate calcium complex; Gut microbiota; Chondroitin Sulfates; Calcium; Animals; Bacteria/metabolism; Bone Density/drug effects; Calcium/therapeutic use; Chondroitin Sulfates/therapeutic use; Dietary Supplements; Feces/microbiology; Femur/drug effects; Femur/pathology; Femur/ultrastructure; Gastrointestinal Microbiome/drug effects; Gastrointestinal Microbiome/physiology; Male; Metabolome/drug effects; Osteoporosis/diet therapy; Rats, Sprague-Dawley; Bone turnover marker; Calcium complexes; Chondroitin sulphate calcium complex; Chondroitinsulfate; In-vitro; Metabolite profiles; Ovariectomized rats; Organic Chemistry; Polymers and Plastics; Materials Chemistry
Abstract :
[en] Although chondroitin sulfate calcium complex (CSCa) was claimed to have the bioactivity for bone care in vitro, its anti-osteoporosis bioactivity was little reported in vivo. Here, the effects of CSCa on osteoporosis rats were investigated. Results showed that, compared with the osteoporosis rats, CSCa could improve the bone mineral density and microstructure of femur, and change the bone turnover markers level in serum. 16S rRNA sequencing and metabolomics analysis indicated CSCa intervention altered the composition of gut microbiota along with metabolite profiles in ovariectomized rat faeces. The correlation analysis showed some gut microbiota taxa were significantly correlated with osteoporosis phenotypes and the enriched metabolites. Taken together, dietary CSCa intervention has the potential to alleviate the osteoporosis and related symptoms probably involving gut microbiota or the metabolite profiles as demonstrated in rats. This study provides some scientific evidence for the potential effects of CSCa as the food supplement on the osteoporosis.
Zhang, Chunhui; Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China. Electronic address: dr_zch@163.com
Qin, Xiaojie; Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Zhang, Hongru ; Université de Liège - ULiège > TERRA Research Centre
Zhang, Zhiqiang; Shandong Haiyu Biotechnology Co., Ltd., Jining 272113, China
Richel, Aurore ; Université de Liège - ULiège > TERRA Research Centre > Smart Technologies for Food and Biobased Products (SMARTECH)
Language :
English
Title :
Modulation of gut microbiota by chondroitin sulfate calcium complex during alleviation of osteoporosis in ovariectomized rats.
Aaseth, J., Boivin, G., Andersen, O., Osteoporosis and trace elements—An overview. Journal of Trace Elements in Medicine and Biology 26:2–3 (2012), 149–152.
Akesson, K., Marsh, D., Mitchell, P.J., McLellan, A.R., Stenmark, J., Pierroz, D.D., Cooper, C., Capture the fracture: A best practice framework and global campaign to break the fragility fracture cycle. Osteoporosis International 24:8 (2013), 2135–2152.
Alaam, M.M., Hussien, N.I., A comparative study between the effect of 17-β estradiol and angiotensin converting enzyme inhibitor on osteoporosis in ovariectomized rats. General Physiology and Biophysics 35:4 (2016), 433–441.
Amini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of The Royal Statistical Society. Series B 57:1 (1995), 289–300.
Balkhi, B., Seoane-Vazquez, E., Rodriguez-Monguio, R., Changes in the utilization of osteoporosis drugs after the 2010 FDA bisphosphonate drug safety communication. Saudi Pharmaceutical Journal 26:2 (2018), 238–243.
Beral, V., Bull, D., Reeves, G., Endometrial cancer and hormone-replacement therapy in the Million Women Study. Lancet (London, England) 365:9470 (2005), 1543–1551.
Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30:15 (2014), 2114–2120.
Boyd, S.K., Davison, P., Müller, R., Gasser, J.A., Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone 39:4 (2006), 854–862.
Britton, R.A., Irwin, R., Quach, D., Schaefer, L., Zhang, J., Lee, T., McCabe, L.R., Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. Journal of Cellular Physiology 229:11 (2014), 1822–1830.
Bronner, F., Calcium and osteoporosis. The American Journal of Clinical Nutrition 60:6 (1994), 831–836.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Knight, R., QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:5 (2010), 335–336.
Chen, D., Zhao, C.M., The possible existence of a gut-bone axis suggested by studies of genetically manipulated mouse models?. Current Pharmaceutical Design 17:16 (2011), 1552–1555.
Chiu, Y.H., Tsai, J.J., Lin, S.L., Lin, M.Y., Lactobacillus casei MYL01 modulates the proinflammatory state induced by ethanol in an in vitro model. Journal of Dairy Science 97:4 (2014), 2009–2016.
Conigrave, A.D., Quinn, S.J., Brown, E.M., L-amino acid sensing by the extracellular Ca2+-sensing receptor. PNAS 97:9 (2000), 4814–4819.
Dashnyam, K., Bayaraa, O., Mandakhbayar, N., Park, J.-H., Lee, J.-H., Jang, T.-S., Kim, H.-W., Nanoscale calcium salt-based formulations as potential therapeutics for osteoporosis. ACS Biomaterials Science & Engineering 6:8 (2020), 4604–4613.
Eastell, R., Szulc, P., Use of bone turnover markers in postmenopausal osteoporosis. The Lancet Diabetes & Endocrinology 5:11 (2017), 908–923.
Edgar, R.C., UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10:10 (2013), 996–998.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27:16 (2011), 2194–2200.
Ejtahed, H.S., Soroush, A.R., Angoorani, P., Larijani, B., Hasani-Ranjbar, S., Gut microbiota as a target in the pathogenesis of metabolic disorders: A new approach to novel therapeutic agents. Hormone and Metabolic Research 48:6 (2016), 349–358.
Fenbo, M., Xingyu, X., Bin, T., Strontium chondroitin sulfate/silk fibroin blend membrane containing microporous structure modulates macrophage responses for guided bone regeneration. Carbohydrate Polymers 213 (2019), 266–275.
Giaze, T.R., Shuid, A.N., Soelaiman, I.N., Muhammad, N., Jamal, J.A., Fauzi, M.B., Mohamed, N., Comparative anti-osteoporotic properties of the leaves and roots of Marantodes pumilum var. alata in postmenopausal rat model. Journal of Traditional and Complementary Medicine 9:4 (2019), 393–400.
Hao, M.L., Wang, G.Y., Zuo, X.Q., Qu, C.J., Yao, B.C., Wang, D.L., Gut microbiota: An overlooked factor that plays a significant role in osteoporosis. The Journal of International Medical Research 47:9 (2019), 4095–4103.
He, J., Xu, S., Zhang, B., Xiao, C., Chen, Z., Si, F., Chen, J., Gut microbiota and metabolite alterations associated with reduced bone mineral density or bone metabolic indexes in postmenopausal osteoporosis. Aging (Albany NY) 12:9 (2020), 8583–8604.
Henrotin, Y., Marty, M., Mobasheri, A., What is the current status of chondroitin sulfate and glucosamine for the treatment of knee osteoarthritis?. Maturitas 78:3 (2014), 184–187.
John, G.K., Mullin, G.E., The gut microbiome and obesity. Current Oncology Reports, 18(7), 2016, 45.
Johnell, O., The socioeconomic burden of fractures: Today and in the 21st century. The American Journal of Medicine 103:2a (1997), 20S–25S (Discussion 25S-26S).
Karna, E., Szoka, L., Huynh, T.Y.L., Palka, J.A., Proline-dependent regulation of collagen metabolism. Cellular and Molecular Life Sciences: CMLS 77:10 (2020), 1911–1918.
Kaunitz, A.M., Mcclung, M.R., Feldman, R.G., Wysocki, S.J.J.F.P., Postmenopausal osteoporosis: Fracture risk and prevention. The Journal of Fimaly Practice 58:11 Suppl Postmenopausal (2009), S1–S6.
Klotzbuecher, C.M., Ross, P.D., Landsman, P.B., Abbott, T.A. 3rd, Berger, M., Patients with prior fractures have an increased risk of future fractures: A summary of the literature and statistical synthesis. Journal of Bone and Mineral Research 15:4 (2000), 721–739.
Lauder, R.M., Chondroitin sulphate: A complex molecule with potential impacts on a wide range of biological systems. Complementary Therapies in Medicine 17:1 (2009), 56–62.
Li, C., Huang, Q., Yang, R., Dai, Y., Zeng, Y., Tao, L., Wang, Q., Gut microbiota composition and bone mineral loss-epidemiologic evidence from individuals in Wuhan, China. Osteoporosis International 30:5 (2019), 1003–1013.
Liu, F., Zhang, N., Li, Z., Wang, X., Shi, H., Xue, C., Tang, Q., Chondroitin sulfate disaccharides modified the structure and function of the murine gut microbiome under healthy and stressed conditions. Scientific Reports, 7(1), 2017, 6783.
Liu, J., Liu, J., Liu, L., Zhang, G., Zhou, A., Peng, X., The gut microbiota alteration and the key bacteria in Astragalus polysaccharides (APS)-improved osteoporosis. Food Research International, 138(Pt B), 2020, 109811.
Ma, F.B., Liu, N., Hu, N., Wen, C.Y., Tang, B., Synthesis of strontium chondroitin sulfate and the evaluation of its capability to attenuate osteoarthritis. Carbohydrate Polymers 170 (2017), 217–225.
Magoč, T., Salzberg, S.L., FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:21 (2011), 2957–2963.
Mathavan, N., Turunen, M.J., Tägil, M., Isaksson, H., Characterising bone material composition and structure in the ovariectomized (OVX) rat model of osteoporosis. Calcified Tissue International 97:2 (2015), 134–144.
McCabe, L., Britton, R.A., Parameswaran, N., Prebiotic and probiotic regulation of bone health: Role of the intestine and its microbiome. Current Osteoporosis Reports 13:6 (2015), 363–371.
Mikami, T., Kitagawa, H., Biosynthesis and function of chondroitin sulfate. Biochimica et Biophysica Acta 1830:10 (2013), 4719–4733.
Qi, H., Bao, J., An, G., Ouyang, G., Zhang, P., Wang, C., Zhang, Q., Association between the metabolome and bone mineral density in pre- and post-menopausal Chinese women using GC-MS. Molecular BioSystems 12:7 (2016), 2265–2275.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Glöckner, F.O., The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research 41:Database issue (2013), D590–D596.
Sánchez, A., Blanco, R., Osteonecrosis of the jaw (ONJ) and atypical femoral fracture (AFF) in an osteoporotic patient chronically treated with bisphosphonates. Osteoporosis International 28:3 (2017), 1145–1147.
Shang, Q., Shi, J., Song, G., Zhang, M., Cai, C., Hao, J., Yu, G., Structural modulation of gut microbiota by chondroitin sulfate and its oligosaccharide. International Journal of Biological Macromolecules 89 (2016), 489–498.
Shang, Q., Yin, Y., Zhu, L., Li, G., Yu, G., Wang, X., Degradation of chondroitin sulfate by the gut microbiota of Chinese individuals. International Journal of Biological Macromolecules 86 (2016), 112–118.
Shen, Q., Zhang, C., Mo, H., Zhang, H., Qin, X., Li, J., Richel, A., Fabrication of chondroitin sulfate calcium complex and its chondrocyte proliferation in vitro. Carbohydrate Polymers, 2020, 117282.
Shi, Y., Meng, Y.-C., Li, J.r., Chen, J., Liu, Y.h., Bai, X., Chondroitin sulfate: Extraction, purification, microbial and chemical synthesis. Journal of Chemical Technology and Biotechnology 89:10 (2014), 1445–1465.
Sjögren, K., Engdahl, C., Henning, P., Lerner, U.H., Tremaroli, V., Lagerquist, M.K., Ohlsson, C., The gut microbiota regulates bone mass in mice. Journal of Bone and Mineral Research 27:6 (2012), 1357–1367.
Tanida, M., Shen, J., Maeda, K., Horii, Y., Yamano, T., Fukushima, Y., Nagai, K., High-fat diet-induced obesity is attenuated by probiotic strain Lactobacillus paracasei ST11 (NCC2461) in rats. Obesity Research & Clinical Practice 2:3 (2008), 159–169.
Tousen, Y., Matsumoto, Y., Nagahata, Y., Kobayashi, I., Inoue, M., Ishimi, Y., Resistant starch attenuates bone loss in ovariectomised mice by regulating the intestinal microbiota and bone-marrow inflammation. Nutrients, 11(2), 2019, 297.
Villa, C.R., Ward, W.E., Comelli, E.M., Gut microbiota-bone axis. Critical Reviews in Food Science and Nutrition 57:8 (2017), 1664–1672.
Volpi, N., Condrosulf®: Structural characterization, pharmacological activities and mechanism of action. Current Medicinal Chemistry 21:34 (2014), 3949–3961.
Weaver, C.M., Diet, gut microbiome, and bone health. Current Osteoporosis Reports 13:2 (2015), 125–130.
Xia, G., Zhao, Y., Yu, Z., Tian, Y., Wang, Y., Wang, S., Xue, C., Phosphorylated peptides from antarctic krill (Euphausia superba) prevent estrogen deficiency induced osteoporosis by inhibiting bone resorption in ovariectomized rats. Journal of Agricultural Food and Chemistry 63:43 (2015), 9550–9557.
Yan, C., Huang, D., Shen, X., Qin, N., Jiang, K., Zhang, D., Zhang, Q., Identification and characterization of a polysaccharide from the roots of Morinda officinalis, as an inducer of bone formation by up-regulation of target gene expression. International Journal of Biological Macromolecules 133 (2019), 446–456.
Yan, J., Herzog, J.W., Tsang, K., Brennan, C.A., Bower, M.A., Garrett, W.S., Charles, J.F., Gut microbiota induce IGF-1 and promote bone formation and growth. PNAS 113:47 (2016), E7554–e7563.
Yatsonsky Ii, D., Pan, K., Shendge, V.B., Liu, J., Ebraheim, N.A., Linkage of microbiota and osteoporosis: A mini literature review. World Journal of Orthopedics 10:3 (2019), 123–127.
Ye, M., Yu, J., Shi, X., Zhu, J., Gao, X., Liu, W., Polysaccharides catabolism by the human gut bacterium-Bacteroides thetaiotaomicron: Advances and perspectives. Critical Reviews in Food Science and Nutrition, 2020, 1–20.
Ye, M., Zhang, C., Jia, W., Shen, Q., Qin, X., Zhang, H., Zhu, L., Metabolomics strategy reveals the osteogenic mechanism of yak (Bos grunniens) bone collagen peptides on ovariectomy-induced osteoporosis in rats. Food & Function 11:2 (2020), 1498–1512.
Yuan, H., Xiao, L., Min, W., Yuan, W., Lu, S., Huang, G., Bu-Shen-Tong-Luo decoction prevents bone loss via inhibition of bone resorption and enhancement of angiogenesis in ovariectomy-induced osteoporosis of rats. Journal of Ethnopharmacology 220 (2018), 228–238.
Zhang, M., Wang, Y., Zhang, Q., Wang, C., Zhang, D., Wan, J.B., Yan, C., UPLC/Q-TOF-MS-based metabolomics study of the anti-osteoporosis effects of Achyranthes bidentata polysaccharides in ovariectomized rats. International Journal of Biological Macromolecules 112 (2018), 433–441.
Zheng, P., Li, Z., Zhou, Z., Gut microbiome in type 1 diabetes: A comprehensive review. Diabetes/Metabolism Research and Reviews, 34(7), 2018, e3043.
Zhu, Z., Zhu, B., Sun, Y., Ai, C., Wang, L., Wen, C., Liu, X., Sulfated polysaccharide from sea cucumber and its depolymerized derivative prevent obesity in association with modification of gut microbiota in high-fat diet-fed mice. Molecular Nutrition & Food Research, 62(23), 2018, e1800446.