Bone Remodeling and the Microbiome

Pacifici, Roberto

doi:10.1101/cshperspect.a031203

Cited by 101Gut microbiota and healthBone Metabolism and DiseasesOral microbiology and periodontitis research

Bone Remodeling and the Microbiome

Open access

Pacifici, Roberto·2018·Cold Spring Harbor Perspectives in Medicine

DOI 10.1101/cshperspect.a031203PMC PMC5880157

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Abstract

Exposed surfaces of mammals are colonized with 100 trillion indigenous bacteria, fungi, and viruses, creating a diverse ecosystem known as the microbiome. The gastrointestinal tract harbors the greatest numbers of these microorganisms, which regulate human nutrition, metabolism, and immune system function. Moreover, the intestinal microbiota contains pro- and anti-inflammatory products that modulate immune responses and may play a role in maintaining gut barrier function. Therefore, the community composition of the microbiota has profound effects on the immune status of the host and impacts the development and/or progression of inflammatory diseases. Accordingly, numerous studies have shown differences in the microbiota of patients with and without a given inflammatory condition. There is now strong evidence that the gut microbiome regulates bone homeostasis in health and disease, and that prebiotic and probiotics protect against bone loss. Herein, the evidence supporting the role of the microbiota and the effects of prebiotic and probiotics will be reviewed.

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Gut microbiome health affects nutrient production, host growth, and immune homeostasis.
“GM health also affects nutrient production, host growth, and immune homeostasis [25,26,27].”
From Osteoporosis: Molecular Pathology, Diagnostics, and Therapeutics (2023) · cites this paper as [27]
The paper’s opening discussion says gut microorganisms regulate human nutrition and immune-system function. The section “Microbiota Regulates Bone Growth and Bone Mass Acquisition” also describes microbiota-dependent changes in body growth in mice. The copy discusses nutrient absorption and use, but does not establish the claimed effect on nutrient production. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Complex diseases such as diabetes mellitus, transient ischemic attacks, and rheumatoid arthritis have been linked to changes in the gut microbiome.
“Moreover, complex diseases, such as diabetes mellitus (DM), transient ischemic attacks, and rheumatoid arthritis, have all been linked to changes in the GM [25,26,27].”
From Osteoporosis: Molecular Pathology, Diagnostics, and Therapeutics (2023) · cites this paper as [27]
The main text (page unavailable) links changes in the gut microbiome to diabetes risk. It discusses rheumatoid arthritis in connection with the oral microbiome, not the gut microbiome, and does not link transient ischemic attacks to microbiome changes. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Bone-active cytokines are released directly by immune cells in the gut, absorbed, and then circulate to the bone, playing a pivotal role in the gut microbiome-immune-bone axis.
“Bone-active cytokines are released directly by immune cells in the gut, absorbed, and then circulate to the bone; these cytokines play a pivotal role in the GM–immune–bone axis [15,27].”
From Osteoporosis: Molecular Pathology, Diagnostics, and Therapeutics (2023) · cites this paper as [27]
In “Microbiota and the Bone Loss Induced by Sex Steroid Deficiency,” the paper considers gut-produced cytokines circulating to bone but says it is still unclear whether that occurs. It instead describes preliminary evidence favoring immune cells that travel from the gut to bone marrow and produce cytokines there. The claim presents the proposed direct route as established. (LLM, conf=0.88)
Experimental — accuracy not yet measured

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Bone Mineral Density in the Complete Androgen Insensitivity and 5α-Reductase-2 Deficiency Syndromes
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Prebiotics Enhance Magnesium Absorption and Inulin‐based Fibers Exert Chronic Effects on Calcium Utilization in a Postmenopausal Rodent Model
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Autoimmune Arthritis
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Mortality and serum urea and electrolytes on admission for hip fracture patients
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Slevin, M. M., Allsopp, P. J., Magee, P. J., Bonham, M. P., Naughton, V. R., Strain, J., Duffy, M. E., Wallace, J. M. W., & McSorley, E. M. (2014) · Journal of Nutrition · doi:10.3945/jn.113.188144 · Cited by 82 · see citing works
Agave Fructans: Their Effect on Mineral Absorption and Bone Mineral Content
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Estradiol rapidly inhibits osteoclastogenesis and RANKL expression in bone marrow cultures in postmenopausal women: a pilot study
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IL-17A-mediated sRANK ligand elevation involved in postmenopausal osteoporosis
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Premature T cell senescence in Ovx mice is inhibited by repletion of estrogen and medicarpin: a possible mechanism for alleviating bone loss
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Supplementation of broccoli or Bifidobacterium longum–fermented broccoli suppresses serum lipid peroxidation and osteoclast differentiation on alveolar bone surface in rats fed a high-cholesterol diet
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Bone Loss in Surgically Ovariectomized Premenopausal Women Is Associated With T Lymphocyte Activation and Thymic Hypertrophy
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Expression of G protein-coupled estrogen receptor in irritable bowel syndrome and its clinical significance.
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A novel shift in estrogen receptor expression occurs as estradiol suppresses inflammation-associated colon tumor formation
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Bone-Resorbing Cytokines from Peripheral Blood Mononuclear Cells after Hormone Replacement Therapy: A Longitudinal Study
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Estrogen Deficiency, Postmenopausal Osteoporosis, and Age-Related Bone Loss
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Self-citation
T helper cell populations: As flexible as the skin?
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Time-course of vertebral and femoral bone loss in rats administered gonadotrophin-releasing hormone agonist
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“In female mice, the acute effects of sex steroid deficiency are modeled by ovariectomy (ovx), or treatment with gonadotrophin-releasing hormone (GN-RH) agonists (Kurabayashi et al. 1993; Wang et al. 2000).”
Background
Comparison of the effects of add-back therapy with various natural oestrogens on bone metabolism in rats administered a long-acting gonadotrophin-releasing hormone agonist
Wang, Y., Yano, T., Kikuchi, A., Yano, N., Matsumi, H., Ando, K., Kasai, Y., Watanabe, M., Okagaki, R., Osuga, Y., et al. (2000) · Journal of Endocrinology · doi:10.1677/joe.0.1650467 · Cited by 13 · see citing works
Estrogen deficiency induced intestinal inflammation and permeability is linked with osteoporosis (488.8)
Raehtz, S., Fedorko, A., & McCabe, L. R. (2014) · The FASEB Journal · doi:10.1096/fasebj.28.1_supplement.488.8 · Cited by 7 · see citing works

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Osteoporosis: Pathophysiology and therapeutic options
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Extracellular Vesicles from Child Gut Microbiota Enter into Bone to Preserve Bone Mass and Strength
Liu, J., Chen, C., Liu, Z., Luo, Z., Rao, S., Jin, L., Wan, T., Yue, T., Tan, Y., Yin, H., et al. (2021) · Advanced Science · doi:10.1002/advs.202004831 · Cited by 256 · see citing works
T-Cell Mediated Inflammation in Postmenopausal Osteoporosis
Wu, D., Cline-Smith, A., Shashkova, E., Perla, A., Katyal, A., & Aurora, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.687551 · Cited by 214 · see citing works
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The Human Gut Microbiota: A Key Mediator of Osteoporosis and Osteogenesis
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Involvement of the gut microbiota and barrier function in glucocorticoid-induced osteoporosis
Schepper, J. D., Collins, F., Rios-Arce, N. D., Kang, H. J., Schaefer, L., Gardinier, J. D., Raghuvanshi, R., Quinn, R. A., Britton, R., Parameswaran, N., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3947 · Cited by 199 · see citing works
Fecal microbiota transplantation ameliorates bone loss in mice with ovariectomy-induced osteoporosis via modulating gut microbiota and metabolic function
Zhang, Y.-W., Cao, M.-M., Li, Y.-J., Lu, P.-P., Dai, G.-C., Zhang, M., Wang, H., & Rui, Y.-F. (2022) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2022.08.003 · Cited by 184 · see citing works
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The Association of Gut Microbiota With Osteoporosis Is Mediated by Amino Acid Metabolism: Multiomics in a Large Cohort
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Gut Microbiome and Space Travelers’ Health: State of the Art and Possible Pro/Prebiotic Strategies for Long-Term Space Missions
Turroni, S., Magnani, M., Pukar, K. C., Lesnik, P., Vidal, H., & Heer, M. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.553929 · Cited by 120 · see citing works
Bone diseases in patients with chronic liver disease
Jeong, H., & Kim, D. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174270 · Cited by 113 · see citing works
Exercise prevents high fat diet-induced bone loss, marrow adiposity and dysbiosis in male mice
McCabe, L. R., Irwin, R., Tekalur, A., Evans, C. C., Schepper, J. D., Parameswaran, N., & Ciancio, M. J. (2018) · Bone · doi:10.1016/j.bone.2018.03.024 · Cited by 112 · see citing works
Gut microbial-derived short-chain fatty acids and bone: a potential role in fracture healing
Wallimann, A., Magrath, W. J., Thompson, K., Moriarty, T. F., Richards, R. G., Akdiş, C. A., O’Mahony, L., & Hernandez, C. J. (2021) · European Cells and Materials · doi:10.22203/ecm.v041a29 · Cited by 111 · see citing works
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Targeting chronic inflammation as a potential adjuvant therapy for osteoporosis
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Biomarkers of aging in frailty and age-associated disorders: State of the art and future perspective
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Probiotics ameliorate alveolar bone loss by regulating gut microbiota
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Guss, J. D., Taylor, E., Rouse, Z., Roubert, S., Higgins, C. H., Thomas, C. J., Baker, S. P., Vashishth, D., Donnelly, E., Shea, M. K., et al. (2019) · Bone · doi:10.1016/j.bone.2019.06.010 · Cited by 77 · see citing works
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Martinis, M. D., Ginaldi, L., Allegra, A., Sirufo, M. M., Pioggia, G., Tonacci, A., & Gangemi, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21238887 · Cited by 65 · see citing works
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The influence of gut microbiome on bone health and related dietary strategies against bone dysfunctions
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Next-generation probiotics and engineered BEVs for precision therapeutics in osteoporosis
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Germ‐Free C57BL /6 Mice Have Increased Bone Mass and Altered Matrix Properties but Not Decreased Bone Fracture Resistance
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Diabetic Rats Induced Using a High-Fat Diet and Low-Dose Streptozotocin Treatment Exhibit Gut Microbiota Dysbiosis and Osteoporotic Bone Pathologies
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The gut microbiota in osteoporosis: dual roles and therapeutic prospects
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Linking the relation between gut microbiota and glucocorticoid-induced osteoporosis
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The human microbiome in space: parallels between Earth-based dysbiosis, implications for long-duration spaceflight, and possible mitigation strategies
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Immune cells: the key mediator between the gut microbiota and osteoporosis
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Identification of the Key Molecular Drivers of Phosphorus Utilization Based on Host miRNA-mRNA and Gut Microbiome Interactions
Ponsuksili, S., Reyer, H., Hadlich, F., Weber, F., Trakooljul, N., Oster, M., Siengdee, P., Muráni, E., Rodehutscord, M., Camarinha‐Silva, A., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082818 · Cited by 21 · see citing works
Possible relationship between the gut leaky syndrome and musculoskeletal injuries: the important role of gut microbiota as indirect modulator
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The probiotic Lactiplantibacillus plantarum attenuates ovariectomy-induced osteoporosis through osteoimmunological signaling
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Musculoskeletal microbiology: The utility of the microbiome in orthopedics
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New Horizons in the Treatment of Age-Associated Obesity, Sarcopenia and Osteoporosis
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Lactobacillus Reuteri 6475 Prevents Bone Loss in a Clinically Relevant Oral Model of Glucocorticoid‐Induced Osteoporosis in Male CD ‐1 Mice
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Calcium Bioavailability of Opuntia ficus-indica Cladodes in an Ovariectomized Rat Model of Postmenopausal Bone Loss
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A Review of Magnesium Alloys In Vivo Antibacterial Properties: Challenges, Solutions, and Perspectives in Implant‐Associated Orthopedic Infections
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Authors: Pacifici, R.
Affiliations: Emory University (US)
Corresponding author: Pacifici, Roberto
ORCID: Pacifici, Roberto
Venue: Cold Spring Harbor Perspectives in Medicine
Publisher: Cold Spring Harbor Laboratory
Published: 2017-08-28
Volume: 8
Issue: 4
Pages: a031203
ISSN: 2157-1422 (ISSN-L)
DOI: 10.1101/cshperspect.a031203
PMC: PMC5880157
OpenAlex: W2747488858
Cited by: 101
References: 185
Citations by year: 2026: 9 · 2025: 20 · 2024: 13 · 2023: 14 · 2022: 9 · 2021: 17 · 2020: 12 · 2019: 5 · 2018: 2
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Cold Spring Harbor Perspectives in Medicine (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (R01DK119229, R01DK112946)
National Center for Research Resources (S10RR028009)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Keywords: bone remodeling, gut microbiota, bone homeostasis, prebiotics, probiotics, bone loss, inflammation, immune regulation, intestinal barrier
MeSH terms: Gastrointestinal Microbiome, Animals, Bone and Bones, Female, Humans, Intestinal Mucosa, Male, Osteoporosis, Gonadal Steroid Hormones, Bone Remodeling, Probiotics, Mice, Prebiotics

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