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Citations to this article

The gut-bone axis: how bacterial metabolites bridge the distance
Mario M. Zaiss, … , Georg Schett, Roberto Pacifici
Mario M. Zaiss, … , Georg Schett, Roberto Pacifici
Published July 15, 2019
Citation Information: J Clin Invest. 2019;129(8):3018-3028. https://doi.org/10.1172/JCI128521.
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The gut-bone axis: how bacterial metabolites bridge the distance

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Abstract

The gut microbiome is a key regulator of bone health that affects postnatal skeletal development and skeletal involution. Alterations in microbiota composition and host responses to the microbiota contribute to pathological bone loss, while changes in microbiota composition that prevent, or reverse, bone loss may be achieved by nutritional supplements with prebiotics and probiotics. One mechanism whereby microbes influence organs of the body is through the production of metabolites that diffuse from the gut into the systemic circulation. Recently, short-chain fatty acids (SCFAs), which are generated by fermentation of complex carbohydrates, have emerged as key regulatory metabolites produced by the gut microbiota. This Review will focus on the effects of SCFAs on the musculoskeletal system and discuss the mechanisms whereby SCFAs regulate bone cells.

Authors

Mario M. Zaiss, Rheinallt M. Jones, Georg Schett, Roberto Pacifici

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Total citations by year

Year: 2025 2024 2023 2022 2021 2020 2019 Total
Citations: 10 43 41 31 31 15 2 173
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Gut Microbiota Characteristics Are Associated With Severity of Acute Radiation-Induced Esophagitis
Lin MQ, Wu YH, Yang J, Lin HC, Liu LY, Yu YL, Yao QW, Li JC
Frontiers in microbiology 2022
Common Dietary Modifications in Preclinical Models to Study Skeletal Health
Rendina-Ruedy E, Smith BJ
Frontiers in Endocrinology 2022
Intestinal microbiota of layer hens and its association with egg quality and safety.
Dai D, Qi GH, Wang J, Zhang HJ, Qiu K, Wu SG
Poultry science 2022
New Advances in Improving Bone Health Based on Specific Gut Microbiota.
Yan Q, Cai L, Guo W
Frontiers in Cellular and Infection Microbiology 2022
Altered Intestinal Microbiomes and Lipid Metabolism in Patients With Prolonged Disorders of Consciousness.
Yu J, Cheng Q, He F, Meng F, Yu Y, Xu C, Wen X, Hong L, Gao J, Li J, Pan G, Li MD, Luo B
Frontiers in immunology 2022
A TrkB agonist prodrug prevents bone loss via inhibiting asparagine endopeptidase and increasing osteoprotegerin.
Xiong J, Liao J, Liu X, Zhang Z, Adams J, Pacifici R, Ye K
Nature Communications 2022
NMR-Based Metabolomics to Decipher the Molecular Mechanisms in the Action of Gut-Modulating Foods.
He W, Bertram HC
2022
Acyloxyacyl hydrolase deficiency induces chronic inflammation and bone loss in male mice.
Cheng X, Song X, Li Z, Yuan C, Lei X, Feng M, Hong Z, Zhang L, Hong D
Journal of Molecular Medicine 2022
One-year supplementation with Lactobacillus reuteri ATCC PTA 6475 counteracts a degradation of gut microbiota in older women with low bone mineral density
Li P, Ji B, Luo H, Sundh D, Lorentzon M, Nielsen J
npj Biofilms and Microbiomes 2022
Gut microbiome and human health: Exploring how the probiotic genus Lactobacillus modulate immune responses
Rastogi S, Singh A
Frontiers in pharmacology 2022
Lipopolysaccharide-binding protein and bone health: data from a population-based sample of men.
Cleminson JR, Pasco JA, Bortolasci CC, Holloway-Kew KL, Hodge JM, Anderson KB, Kotowicz MA, Samarasinghe RM, Williams LJ
Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 2022
Modulatory Effect of Gut Microbiota on the Gut-Brain, Gut-Bone Axes, and the Impact of Cannabinoids
Ibrahim I, Syamala S, Ayariga JA, Xu J, Robertson BK, Meenakshisundaram S, Ajayi OS
Metabolites 2022
Mathematical modeling of the effects of Wnt-10b on bone metabolism.
Cook CV, Islam MA, Smith BJ, Versypt ANF
2022
Yogurt Benefits Bone Mineralization in Ovariectomized Rats with Concomitant Modulation of the Gut Microbiome
He W, Xie Z, Wittig NK, Zachariassen LF, Andersen A, Andersen HJ, Birkedal H, Nielsen DS, Hansen AK, Bertram HC
Molecular Nutrition & Food Research 2022
Gut microbiota and fecal metabolic signatures in rat models of disuse-induced osteoporosis
Qiao X, Zhang K, Li X, Lv Z, Wei W, Zhou R, Yan L, Pan Y, Yang S, Sun X, Li P, Xu C, Feng Y, Tian Z
Frontiers in Cellular and Infection Microbiology 2022
Colon epithelial cell-specific Bmal1 deletion impairs bone formation in mice
Ko FC, Jochum SB, Wilson BM, Adra A, Patel N, Lee H, Wilber S, Shaikh M, Forsyth C, Keshavarzian A, Swanson GR, Sumner DR
Bone 2022
Ovariectomy induces bone loss via microbial-dependent trafficking of intestinal TNF+ T cells and Th17 cells
Mingcan Yu, Subhashis Pal, Cameron W. Paterson, Jau-Yi Li, Abdul M. Tyagi, Jonathan Adams, Craig M. Coopersmith, M. Neale Weitzmann, Roberto Pacifici
Journal of Clinical Investigation 2021
Energy Metabolism and Ketogenic Diets: What about the Skeletal Health? A Narrative Review and a Prospective Vision for Planning Clinical Trials on this Issue
D Merlotti, R Cosso, C Eller-Vainicher, F Vescini, I Chiodini, L Gennari, A Falchetti
International journal of molecular sciences 2021
Omega-3 fatty acid modulation of serum and osteocyte tumor necrosis factor-α in adult mice exposed to ionizing radiation
SE Little-Letsinger, ND Turner, JR Ford, LJ Suva, SA Bloomfield
Journal of applied physiology 2021
25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation
H Zhang, M Majdeddin, D Gaublomme, B Taminiau, M Boone, D Elewaut, G Daube, I Josipovic, K Zhang, J Michiels
Journal of Animal Science and Biotechnology 2021
Gut-Bone Axis: A Non-Negligible Contributor to Periodontitis
X Jia, R Yang, J Li, L Zhao, X Zhou, X Xu
Frontiers in Cellular and Infection Microbiology 2021
High fat diet, gut microbiome and gastrointestinal cancer
Y Tong, H Gao, Q Qi, X Liu, J Li, J Gao, P Li, Y Wang, L Du, C Wang
Theranostics 2021
Effector memory CD4+T cells in mesenteric lymph nodes mediate bone loss in food-allergic enteropathy model mice, creating IL-4 dominance
A Ono-Ohmachi, S Yamada, S Uno, M Tamai, K Soga, S Nakamura, N Udagawa, Y Nakamichi, M Koide, Y Morita, T Takano, T Itoh, S Kakuta, C Morimoto, S Matsuoka, Y Iwakura, M Tomura, H Kiyono, S Hachimura, H Nakajima-Adachi
Mucosal Immunology 2021
Metabolic Alterations in Older Women With Low Bone Mineral Density Supplemented With Lactobacillus reuteri
P Li, D Sundh, B Ji, D Lappa, L Ye, J Nielsen, M Lorentzon
JBMR Plus 2021
Effects of Probiotic Culture Supernatant on Cariogenic Biofilm Formation and RANKL-Induced Osteoclastogenesis in RAW 264.7 Macrophages
JI Jung, SM Baek, TH Nguyen, JW Kim, CH Kang, S Kim, JY Imm
Molecules (Basel, Switzerland) 2021
The gut microbiota is a transmissible determinant of skeletal maturation
AM Tyagi, TM Darby, E Hsu, M Yu, S Pal, H Dar, JY Li, J Adams, RM Jones, R Pacifici
eLife 2021
Bone Homeostasis and Gut Microbial-Dependent Signaling Pathways
X Zhong, F Zhang, X Yin, H Cao, X Wang, D Liu, J Chen, X Chen
Journal of Microbiology and Biotechnology 2021
The Human Gut Microbiota: A Key Mediator of Osteoporosis and Osteogenesis
KD Seely, CA Kotelko, H Douglas, B Bealer, AE Brooks
International journal of molecular sciences 2021
Regulation of Bone Cell Differentiation and Activation by Microbe-Associated Molecular Patterns
Y Kwon, C Park, J Lee, DH Park, S Jeong, CH Yun, OJ Park, SH Han
International journal of molecular sciences 2021
Melatonin alleviates titanium nanoparticles induced osteolysis via activation of butyrate/GPR109A signaling pathway
Y Wu, F He, C Zhang, Q Zhang, X Su, X Zhu, A Liu, W Shi, W Lin, Z Jin, H Yang, J Lin
Journal of nanobiotechnology 2021
Probiotic supplements and bone health in postmenopausal women: a meta-analysis of randomised controlled trials
J Yu, G Cao, S Yuan, C Luo, J Yu, M Cai
BMJ Open 2021
The role of gut microbiota in bone homeostasis: a systematic review of preclinical animal studies
J Li, WT Ho, C Liu, SK Chow, M Ip, J Yu, HS Wong, WH Cheung, JJ Sung, RM Wong
Bone & joint research 2021
Gut microbial-derived short-chain fatty acids and bone: a potential role in fracture healing
A Wallimann, W Magrath, K Thompson, T Moriarty, R Richards, C Akdis, L O'Mahony, Hernandez
European Cells and Materials 2021
Microbial Metabolite Sodium Butyrate Attenuates Cartilage Degradation by Restoring Impaired Autophagy and Autophagic Flux in Osteoarthritis Development
H Zhou, G Li, Y Wang, R Jiang, Y Li, H Wang, F Wang, H Ma, L Cao
Frontiers in pharmacology 2021
Piezoelectric Microvibration Mitigates Estrogen Loss-Induced Osteoporosis and Promotes Piezo1, MicroRNA-29a, and Wnt3a Signaling in Osteoblasts
RW Wu, WS Lian, YS Chen, JY Ko, SY Wang, H Jahr, FS Wang
International journal of molecular sciences 2021
Genetically determined SCFA concentration modifies the association of dietary fiber intake with changes in bone mineral density during weight loss: The Preventing Overweight Using Novel Dietary Strategies (POUNDS LOST) trial
T Zhou, D Sun, X Li, Y Heianza, MS LeBoff, GA Bray, FM Sacks, L Qi
The American journal of clinical nutrition 2021
Evaluation of Three Formulations of Essential Oils in Broiler Chickens under Cyclic Heat Stress
J Ruff, G Tellez, AJ Forga, R Señas-Cuesta, CN Vuong, ES Greene, X Hernandez-Velasco, ÁJ Uribe, BC Martínez, JA Angel-Isaza, S Dridi, CJ Maynard, CM Owens, BM Hargis, G Tellez-Isaias
Animals 2021
Association of Increased Circulating Acetic Acid With Poor Survival in Pseudomonas aeruginosa Ventilator-Associated Pneumonia Patients
X Qi, L Zhang, J Xu, Z Tao, X Wang, Y Qiu, T Pan, Z Liu, H Qu, R Tan, J Liu
Frontiers in Cellular and Infection Microbiology 2021
Isovaleric acid ameliorates ovariectomy‐induced osteoporosis by inhibiting osteoclast differentiation
KM Cho, YS Kim, M Lee, HY Lee, YS Bae
Journal of Cellular and Molecular Medicine 2021
Bacillus subtilis-Based Probiotic Improves Skeletal Health and Immunity in Broiler Chickens Exposed to Heat Stress
S Jiang, FF Yan, JY Hu, A Mohammed, HW Cheng
Animals 2021
Qu-Zhuo-Tong-Bi Decoction Alleviates Gouty Arthritis by Regulating Butyrate-Producing Bacteria in Mice
X Wen, Y Lou, S Song, Z He, J Chen, Z Xie, X Shi, C Wen, T Shao
Frontiers in pharmacology 2021
Role of Gut Microbiota and Probiotics in Colorectal Cancer: Onset and Progression
E Torres-Maravilla, AS Boucard, AH Mohseni, S Taghinezhad-S, NG Cortes-Perez, LG Bermúdez-Humarán
Microorganisms 2021
Probiotics and Isoflavones as a Promising Therapeutic for Calcium Status and Bone Health: A Narrative Review
IA Harahap, J Suliburska
Foods 2021
Bone Phenotyping Approaches in Human, Mice and Zebrafish – Expert Overview of the EU Cost Action GEMSTONE (“GEnomics of MusculoSkeletal traits TranslatiOnal NEtwork”)
I Foessl, JH Bassett, Å Bjørnerem, B Busse, Â Calado, P Chavassieux, M Christou, E Douni, IA Fiedler, JE Fonseca, E Hassler, W Högler, E Kague, D Karasik, P Khashayar, BL Langdahl, VD Leitch, P Lopes, G Markozannes, FE McGuigan, C Medina-Gomez, E Ntzani, L Oei, C Ohlsson, P Szulc, JH Tobias, K Trajanoska, Ş Tuzun, A Valjevac, B van Rietbergen, GR Williams, T Zekic, F Rivadeneira, B Obermayer-Pietsch
Frontiers in Endocrinology 2021
The Extraction, Functionalities and Applications of Plant Polysaccharides in Fermented Foods: A Review
T Niyigaba, D Liu, J de Dieu Habimana
Foods 2021
Gut Microbiota and Serum Metabolic Signatures of High-Fat-Induced Bone Loss in Mice
L Lu, M Tang, J Li, Y Xie, Y Li, J Xie, L Zhou, Y Liu, X Yu
Frontiers in Cellular and Infection Microbiology 2021
Mathematical Modeling of the Gut–Bone Axis and Implications of Butyrate Treatment on Osteoimmunology
M Islam, C Cook, B Smith, A Versypt
Industrial & engineering chemistry research 2021
Microbiota dependent production of butyrate is required for the bone anabolic activity of PTH
Jau-Yi Li, Mingcan Yu, Subhashis Pal, Abdul M. Tyagi, Hamid Y Dar, Jonathan Adams, M. Neale Weitzmann, Rheinallt M Jones, Roberto Pacifici
Journal of Clinical Investigation 2020
Role of Gut Microbiota in the Skeletal Response to PTH
R Pacifici
The Journal of clinical endocrinology and metabolism 2020
PTH induces bone loss via microbial-dependent expansion of intestinal TNF+ T cells and Th17 cells
M Yu, AM Tyagi, JY Li, J Adams, TL Denning, MN Weitzmann, RM Jones, R Pacifici
Nature Communications 2020
Helicobacter pylori Related Diseases and Osteoporotic Fractures (Narrative Review)
L Fisher, A Fisher, PN Smith
Journal of Clinical Medicine 2020
Plasma high-resolution metabolomics identifies linoleic acid and linked metabolic pathways associated with bone mineral density
MP Bellissimo, TR Ziegler, DP Jones, KH Liu, J Fernandes, JL Roberts, MN Weitzmann, R Pacifici, JA Alvarez
Clinical nutrition (Edinburgh, Scotland) 2020
Specific Commensal Bacterium Critically Regulates Gut Microbiota Osteoimmunomodulatory Actions During Normal Postpubertal Skeletal Growth and Maturation
JD HathawaySchrader, NA Poulides, MD Carson, JE Kirkpatrick, AJ Warner, BA Swanson, EV Taylor, ME Chew, SV Reddy, B Liu, C Westwater, CM Novince
JBMR Plus 2020
The Gut Microbiome and Bone Strength
M Castaneda, JM Strong, DA Alabi, CJ Hernandez
Current Osteoporosis Reports 2020
Metabolomic Associations with Serum Bone Turnover Markers
MP Bellissimo, JL Roberts, DP Jones, KH Liu, KR Taibl, K Uppal, MN Weitzmann, R Pacifici, H Drissi, TR Ziegler, JA Alvarez
Nutrients 2020
Osteoporosis: Pathophysiology and therapeutic options
Ursula Föger-Samwald, Peter Dovjak, Ursula Azizi-Semrad, Katharina Kerschan-Schindl, Peter Pietschmann
EXCLI J 2020
The Role of Gut Dysbiosis in the Bone–Vascular Axis in Chronic Kidney Disease
P Evenepoel, S Dejongh, K Verbeke, B Meijers
Toxins 2020
Dietary Short-Term Fiber Interventions in Arthritis Patients Increase Systemic SCFA Levels and Regulate Inflammation
K Dürholz, J Hofmann, A Iljazovic, J Häger, S Lucas, K Sarter, T Strowig, H Bang, J Rech, G Schett, MM Zaiss
Nutrients 2020
Loss and gain of bone in spondyloarthritis: what drives these opposing clinical features?
G Clunie, N Horwood
Therapeutic Advances in Musculoskeletal Diseases 2020
Dried plum mitigates spinal cord injury‐induced bone loss in mice
X Liu, M Liu, R Turner, U Iwaniec, H Kim, B Halloran
2020
Dietary Fiber, Genetic Variations of Gut Microbiota-derived Short-chain Fatty Acids, and Bone Health in UK Biobank
T Zhou, M Wang, H Ma, X Li, Y Heianza, L Qi
The Journal of clinical endocrinology and metabolism 2020
A gut butyrate‑producing bacterium Butyricicoccus pullicaecorum regulates short‑chain fatty acid transporter and receptor to reduce the progression of 1,2‑dimethylhydrazine‑associated colorectal cancer
SC Chang, MH Shen, CY Liu, CM Pu, JM Hu, CJ Huang
Oncology Letters 2020
The Role of Dietary Fiber in Rheumatoid Arthritis Patients: A Feasibility Study
J Häger, H Bang, M Hagen, M Frech, P Träger, MV Sokolova, U Steffen, K Tascilar, K Sarter, G Schett, J Rech, MM Zaiss
Nutrients 2019
Resolution of inflammation in arthritis
G Schett
Seminars in Immunopathology 2019

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