Volume 37 Issue 3
May  2021
Turn off MathJax
Article Contents
Article Navigation >  Journal of Nanjing University of traditional Chinese Medicine  > 2021  >  37(3): 465-472
WEI Wei, CHEN Ling, ZHOU Yong-jin, XU Zhui-cheng, LI Wan-hong, WEI Ai-chun, HUANG Gui-cheng. Progress on Gut Microbiota-Regulated Bone Metabolism Imbalance and Implications for Chinese Medicine Intervention[J]. Journal of Nanjing University of traditional Chinese Medicine, 2021, 37(3): 465-472. doi: 10.14148/j.issn.1672-0482.2021.0465
Citation: WEI Wei, CHEN Ling, ZHOU Yong-jin, XU Zhui-cheng, LI Wan-hong, WEI Ai-chun, HUANG Gui-cheng. Progress on Gut Microbiota-Regulated Bone Metabolism Imbalance and Implications for Chinese Medicine Intervention[J]. Journal of Nanjing University of traditional Chinese Medicine, 2021, 37(3): 465-472. doi: 10.14148/j.issn.1672-0482.2021.0465
shu

Progress on Gut Microbiota-Regulated Bone Metabolism Imbalance and Implications for Chinese Medicine Intervention

doi: 10.14148/j.issn.1672-0482.2021.0465
  • 1.

    The First Clinical Medical College, Nanjing University of Chinese Medicine, Nanjing, 210023, China

  • 2.

    Hai'an Chinese Medicine Hospital Affilliated to Hanlin College, Nanjing University of Chinese Medicine, Nantong, 226600, China

  • 3.

    School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, 210023, China

  • Received Date: 2021-03-05
    Available Online: 2021-12-21
  • Publish Date: 2021-05-10
    Abstract
  • Gut microbiota has the most category and highest density among all microbial habitats in human body. They can regulate human physiological functions and immune status through gut microbiota-host metabolism and then maintain our healthy. Recently, accumulating clinical researches and preclinical studies have reported that gut microbiota can regulate bone metabolism through various ways. For example, alterations in microbiota composition induced by a variety of pathological states and medicine, especially the antibiotics, may contribute to pathological bone loss. With the development of some new techniques such as high-throughput sequencing, gene knockout and germ-free mice, the recent studies implicated that gut microbiota can regulate bone metabolism balance through direct regulation, the metabolism of endogenous substances and the alterations of related hormones. This review describes recent data uncovering the relationship between gut microbiota and bone metabolism, with a focus on potential regulating pathways and Traditional Chinese Medicine intervention. The implications for treatment of bone metabolism disorders such as osteoporosis and drug target research are discussed as well.

     

    • FullText(HTML)
  • loading
    • References(52)
  • [1]
    QIN JJ, LI RQ, RAES J, et al. A human gut microbial gene catalogue established by metagenomic sequencing[J]. Nature, 2010, 464(7285): 59-65. doi: 10.1038/nature08821
    [2]
    SHETH T, PITCHUMONI CS, DAS KM. Musculoskeletal manifestations in inflammatory bowel disease: A revisit in search of immunopathophysiological mechanisms[J]. J Clin Gastroenterol, 2014, 48(4): 308-317. doi: 10.1097/MCG.0000000000000067
    [3]
    SCHVLE S, ROSSEL JB, FREY D, et al. Widely differing screening and treatment practice for osteoporosis in patients with inflammatory bowel diseases in the Swiss IBD cohort study[J]. Medicine, 2017, 96(22): e6788. doi: 10.1097/MD.0000000000006788
    [4]
    DI STEFANO M, VENETO G, MALSERVISI S, et al. Small intestine bacterial overgrowth and metabolic bone disease[J]. Dig Dis Sci, 2001, 46(5): 1077-1082. doi: 10.1023/A:1010722314493
    [5]
    DAS M, CRONIN O, KEOHANE DM, et al. Gut microbiota alterations associated with reduced bone mineral density in older adults[J]. Rheumatology, 2019, 58(12): 2295-2304. doi: 10.1093/rheumatology/kez302
    [6]
    GUSS JD, HORSFIELD MW, FONTENELE FF, et al. Alterations to the gut microbiome impair bone strength and tissue material properties[J]. J Bone Miner Res, 2017, 32(6): 1343-1353. doi: 10.1002/jbmr.3114
    [7]
    SJOGREN K, ENGDAHL C, HENNING P, et al. The gut microbiota regulates bone mass in mice[J]. J Bone Mineral Res, 2012, 27(6): 1357-1367. doi: 10.1002/jbmr.1588
    [8]
    LI JY, CHASSAING B, TYAGI AM, et al. Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics[J]. J Clin Invest, 2016, 126(6): 2049-2063. doi: 10.1172/JCI86062
    [9]
    TOPPING DL, CLIFTON PM. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides[J]. Physiol Rev, 2001, 81(3): 1031-1064. doi: 10.1152/physrev.2001.81.3.1031
    [10]
    CHANG MC, CHEN YJ, LIAN YC, et al. Butyrate stimulates histone H3 acetylation, 8-isoprostane production, RANKL expression, and regulated osteoprotegerin expression/secretion in MG-63 osteoblastic cells[J]. Int J Mol Sci, 2018, 19(12): E4071. doi: 10.3390/ijms19124071
    [11]
    TANG X, MA SH, LI YR, et al. Evaluating the activity of sodium butyrate to prevent osteoporosis in rats by promoting osteal GSK-3β/Nrf2 signaling and mitochondrial function[J]. J Agric Food Chem, 2020, 68(24): 6588-6603. doi: 10.1021/acs.jafc.0c01820
    [12]
    MOROZUMI A. High concentration of sodium butyrate suppresses osteoblastic differentiation and mineralized nodule formation in ROS17/2.8 cells[J]. J Oral Sci, 2011, 53(4): 509-516. doi: 10.2334/josnusd.53.509
    [13]
    LUCAS S, OMATA Y, HOFMANN J, et al. Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss[J]. Nat Commun, 2018, 9(1): 55. doi: 10.1038/s41467-017-02490-4
    [14]
    TYAGI AM, YUMC, DARBY TM, et al. The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression[J]. Immunity, 2018, 49(6): 1116-1131. doi: 10.1016/j.immuni.2018.10.013
    [15]
    MONTALVANY-ANTONUCCI CC, DUFFLES LF, DE ARRUDA JAA, et al. Short-chain fatty acids and FFAR2 as suppressors of bone resorption[J]. Bone, 2019, 125: 112-121. doi: 10.1016/j.bone.2019.05.016
    [16]
    YANO JM, YU K, DONALDSON GP, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis[J]. Cell, 2015, 161(2): 264-276. doi: 10.1016/j.cell.2015.02.047
    [17]
    CLARKE G, GRENHAM S, SCULLY P, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner[J]. Mol Psychiatry, 2013, 18(6): 666-673. doi: 10.1038/mp.2012.77
    [18]
    ZELANTE T, IANNITTI RG, CUNHA C, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22[J]. Immunity, 2013, 39(2): 372-385. doi: 10.1016/j.immuni.2013.08.003
    [19]
    DUCY P, KARSENTY G. The two faces of serotonin in bone biology[J]. J Cell Biol, 2010, 191(1): 7-13. doi: 10.1083/jcb.201006123
    [20]
    YADAV VK, RYU JH, SUDA NN, et al. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum[J]. Cell, 2008, 135(5): 825-837. doi: 10.1016/j.cell.2008.09.059
    [21]
    YUN HM, PARK KR, HONG JT, et al. Peripheral serotonin-mediated system suppresses bone development and regeneration via serotonin 6 G-protein-coupled receptor[J]. Sci Rep, 2016, 6: 30985. doi: 10.1038/srep30985
    [22]
    NAM SS, LEE JC, KIM HJ, et al. Serotonininhibits osteoblast differentiation and bone regeneration in rats[J]. J Periodontol, 2016, 87(4): 461-469. doi: 10.1902/jop.2015.150302
    [23]
    KODE A, MOSIALOU I, SILVA BC, et al. FOXO1 orchestrates the bone-suppressing function of gut-derived serotonin[J]. J Clin Invest, 2012, 122(10): 3490-3503. doi: 10.1172/JCI64906
    [24]
    REFAEY ME, MCGEE-LAWRENCE ME, FULZELE S, et al. Kynurenine, atryptophan metabolite that accumulates with age, induces bone loss[J]. J Bone Miner Res, 2017, 32(11): 2182-2193. doi: 10.1002/jbmr.3224
    [25]
    PIERCE JL, ROBERTS RL, YU KL, et al. Kynurenine suppresses osteoblastic cell energeticsin vitro and osteoblast numbers in vivo[J]. Exp Gerontol, 2020, 130: 110818. doi: 10.1016/j.exger.2019.110818
    [26]
    KIM BJ, HAMRICK MW, YOO HJ, et al. Thedetrimental effects of kynurenine, a tryptophan metabolite, on human bone metabolism[J]. J Clin Endocrinol Metab, 2019, 104(6): 2334-2342. doi: 10.1210/jc.2018-02481
    [27]
    ZHANG XQ, HE Y, DING M. Simultaneous determination of tryptophan and kynurenine in plasma samples of children patients with Kawasaki disease by high-performance liquid chromatography with programmed wavelength ultraviolet detection[J]. J Chromatogr B Analyt Technol Biomed Life Sci, 2009, 877(16/17): 1678-1682. http://www.sciencedirect.com/science/article/pii/S1570023209002682
    [28]
    DINCEL E. Evaluation of tryptophan/kynurenine pathway relevance with immune system biomarkers of low energy trauma hip fractures in osteoporotic patients[J]. Arch Rheumatol, 2017, 32(3): 203-208. doi: 10.5606/ArchRheumatol.2017.6216
    [29]
    GUSS JD, TAYLOR E, ROUSE Z, et al. The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength[J]. Bone, 2019, 127: 146-154. doi: 10.1016/j.bone.2019.06.010
    [30]
    ZHOU T, HEIANZA Y, CHEN YH, et al. Circulating gut microbiota metabolite trimethylamine N-oxide (TMAO) and changes in bone density in response to weight loss diets: The POUNDS lost trial[J]. Diabetes Care, 2019, 42(8): 1365-1371. doi: 10.2337/dc19-0134
    [31]
    YU MC, MALIK TYAGI A, LI JY, et al. PTH induces bone loss via microbial-dependent expansion of intestinal TNF+ T cells and Th17 cells[J]. Nat Commun, 2020, 11(1): 468. doi: 10.1038/s41467-019-14148-4
    [32]
    LI JY, YU M, PAL S, et al. Parathyroid hormone-dependent bone formation requires butyrate production by intestinal microbiota[J]. J Clin Invest, 2020, 130(4): 1767-1781. doi: 10.1172/JCI133473
    [33]
    SCHEPPER JD, COLLINS F, RIOS-ARCE ND, et al. Involvement of thegut microbiota and barrier function in glucocorticoid-induced osteoporosis[J]. J Bone Miner Res, 2020, 35(4): 801-820. doi: 10.1002/jbmr.3947
    [34]
    YAN J, HERZOG JW, TSANG K, et al. Gut microbiota induce IGF-1 and promote bone formation and growth[J]. PNAS, 2016, 113(47): E7554-E7563.
    [35]
    KEREZOUDI EN, MITSOU EK, GIOTI K, et al. Fermentation of Pleurotus ostreatus and Ganoderma lucidum mushrooms and their extracts by the gut microbiota of healthy and osteopenic women: Potential prebiotic effect and impact of mushroom fermentation products on human osteoblasts[J]. Food Funct, 2021, 12(4): 1529-1546. doi: 10.1039/D0FO02581J
    [36]
    ZHAO X, WANG YJ, NIE ZY, et al. Eucommia ulmoides leaf extract alters gut microbiota composition, enhances short-chain fatty acids production, and ameliorates osteoporosis in the senescence-accelerated mouse P6 (SAMP6) model[J]. Food Sci Nutr, 2020, 8(9): 4897-4906. doi: 10.1002/fsn3.1779
    [37]
    ZHAO X, AI JQ, MAO HP, et al. Effects of Eclipta prostrata on gut microbiota of SAMP6 mice with osteoporosis[J]. J Med Microbiol, 2019, 68(3): 402-416. doi: 10.1099/jmm.0.000936
    [38]
    LI L, CHEN BB, ZHU RY, et al. Fructus Ligustri Lucidi preserves bone quality through the regulation of gut microbiota diversity, oxidative stress, TMAO and Sirt6 levels in aging mice[J]. Aging, 2019, 11(21): 9348-9368. doi: 10.18632/aging.102376
    [39]
    XIAO HH, SHAM TT, CHAN CO, et al. Ametabolomics study on the bone protective effects of a lignan-rich fraction from Sambucus williamsii Ramulus in aged rats[J]. Front Pharmacol, 2018, 9: 932. doi: 10.3389/fphar.2018.00932
    [40]
    MEI FF, MENG KK, GU ZP, et al. Arecanut (Areca catechu L. ) seed polyphenol-ameliorated osteoporosis by altering gut microbiome via LYZ and the immune system in estrogen-deficient rats[J]. J Agric Food Chem, 2021, 69(1): 246-258. doi: 10.1021/acs.jafc.0c06671
    [41]
    LIU JS, LIU J, LIU L, et al. The gut microbiota alteration and the key bacteria inAstragalus polysaccharides (APS)-improved osteoporosis[J]. Food Res Int, 2020, 138: 109811. doi: 10.1016/j.foodres.2020.109811
    [42]
    LI B, LIU M, WANG Y, et al. Puerarin improves the bone micro-environment to inhibit OVX-induced osteoporosis via modulating SCFAs released by the gut microbiota and repairing intestinal mucosal integrity[J]. Biomed Pharmacother, 2020, 132: 110923. doi: 10.1016/j.biopha.2020.110923
    [43]
    WANG YK, CHEN J, CHEN J, et al. Daphnetin ameliorates glucocorticoid-induced osteoporosis via activation of Wnt/GSK-3β/β-catenin signaling[J]. Toxicol Appl Pharmacol, 2020, 409: 115333. doi: 10.1016/j.taap.2020.115333
    [44]
    YAN F, WANG LH, SHI Y, et al. Berberine promotes recovery of colitis and inhibits inflammatory responses in colonic macrophages and epithelial cells in DSS-treated mice[J]. Am J Physiol Gastrointest Liver Physiol, 2012, 302(5): G504-G514. http://www.medicinabiomolecular.com.br/biblioteca/pdfs/Doencas/do-1352.pdf
    [45]
    JIA X, JIA L, MO L, et al. Berberineameliorates periodontal bone loss by regulating gut microbiota[J]. J Dent Res, 2019, 98(1): 107-116. doi: 10.1177/0022034518797275
    [46]
    BRON PA, VAN BAARLEN P, KLEEREBEZEM M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa[J]. Nat Rev Microbiol, 2011, 10(1): 66-78. http://www.onacademic.com/detail/journal_1000034864202510_975d.html
    [47]
    GIBSON GR, PROBERT HM, LOO JV, et al. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics[J]. Nutr Res Rev, 2004, 17(2): 259-275. doi: 10.1079/NRR200479
    [48]
    PAN HD, GUO RJ, JU YM, et al. A single bacterium restores the microbiome dysbiosis to protect bones from destruction in a rat model of rheumatoid arthritis[J]. Microbiome, 2019, 7(1): 107. doi: 10.1186/s40168-019-0719-1
    [49]
    TANABE K, NAKAMURA S, MORIYAMA-HASHIGUCHI M, et al. Dietaryfructooligosaccharide and glucomannan alter gut microbiota and improve bone metabolism in senescence-accelerated mouse[J]. J Agric Food Chem, 2019, 67(3): 867-874. doi: 10.1021/acs.jafc.8b05164
    [50]
    COWARDIN CA, AHERN PP, KUNG VL, et al. Mechanisms by which sialylated milk oligosaccharides impact bone biology in a gnotobiotic mouse model of infant undernutrition[J]. Proc Natl Acad Sci USA, 2019, 116(24): 11988-11996. http://www.researchgate.net/publication/333445167_Mechanisms_by_which_sialylated_milk_oligosaccharides_impact_bone_biology_in_a_gnotobiotic_mouse_model_of_infant_undernutrition
    [51]
    LI JJ, YANG MY, LU CY, et al. Tunabone powder alleviates glucocorticoid-induced osteoporosis via coregulation of the NF-κB and wnt/β-catenin signaling pathways and modulation of gut microbiota composition and metabolism[J]. Mol Nutr Food Res, 2020, 64(5): e1900861. doi: 10.1002/mnfr.201900861
    [52]
    GUO DJ, LIU WW, ZHANG X, et al. Duck egg white-derived peptide VSEE (val-Ser-glu-glu) regulates bone and lipid metabolisms by wnt/β-catenin signaling pathway and intestinal microbiota[J]. Mol Nutr Food Res, 2019, 63(24): e1900525. doi: 10.1002/mnfr.201900525
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(1)

    Get Citation
    PDF
    XML

    Article Metrics

    Article views (302) PDF downloads(207) Cited by()
    Proportional views
    Related

    Copyright © Journal of Nanjing University of traditional Chinese Medicine

    Sponsored by：Nanjing University of traditional Chinese MedicineAddress：No.138 xianlin Avenue, Qixia District, Nanjing cityChina Pos：210023

    Tel：025-85811935Email：xb@njucm.edu.cn

    Supported by: Beijing Renhe Information Technology Co., Ltd.    

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return