Cited by 755Gut microbiota and healthBone Metabolism and DiseasesGrowth Hormone and Insulin-like Growth Factors

The DOI matches its Crossref record; 65 of the 65 references it cites were found in a registry or an index.

Gut microbiota induce IGF-1 and promote bone formation and growth

Open access

Yan, Jing, Herzog, Jeremy W., Tsang, Kelly, Brennan, Caitlin A., Bower, Maureen A., Garrett, Wendy S., Sartor, Balfour R., Aliprantis, Antonios O., Charles, Julia F.·2016·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1607235113PMC PMC5127374

Open this paper in CoChat — free account Open PDF

Abstract

Appreciation of the role of the gut microbiome in regulating vertebrate metabolism has exploded recently. However, the effects of gut microbiota on skeletal growth and homeostasis have only recently begun to be explored. Here, we report that colonization of sexually mature germ-free (GF) mice with conventional specific pathogen-free (SPF) gut microbiota increases both bone formation and resorption, with the net effect of colonization varying with the duration of colonization. Although colonization of adult mice acutely reduces bone mass, in long-term colonized mice, an increase in bone formation and growth plate activity predominates, resulting in equalization of bone mass and increased longitudinal and radial bone growth. Serum levels of insulin-like growth factor 1 (IGF-1), a hormone with known actions on skeletal growth, are substantially increased in response to microbial colonization, with significant increases in liver and adipose tissue IGF-1 production. Antibiotic treatment of conventional mice, in contrast, decreases serum IGF-1 and inhibits bone formation. Supplementation of antibiotic-treated mice with short-chain fatty acids (SCFAs), products of microbial metabolism, restores IGF-1 and bone mass to levels seen in nonantibiotic-treated mice. Thus, SCFA production may be one mechanism by which microbiota increase serum IGF-1. Our study demonstrates that gut microbiota provide a net anabolic stimulus to the skeleton, which is likely mediated by IGF-1. Manipulation of the microbiome or its metabolites may afford opportunities to optimize bone health and growth.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1073/pnas.1607235113

Cites

65 of 65 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Dietary Modulation of the Human Colonic Microbiota: Introducing the Concept of Prebiotics
Gibson, G. R., & Roberfroid, M. B. (1995) · Journal of Nutrition · doi:10.1093/jn/125.6.1401 · Cited by 7,659
The gut microbiota as an environmental factor that regulates fat storage
Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., & Gordon, J. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407076101 · Cited by 6,245
Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells
Furusawa, Y., Obata, Y., Fukuda, S., Endo, T. A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., et al. (2013) · Nature · doi:10.1038/nature12721 · Cited by 5,549
The Microbial Metabolites, Short-Chain Fatty Acids, Regulate Colonic T reg Cell Homeostasis
Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly-Y, M., Glickman, J. N., & Garrett, W. S. (2013) · Science · doi:10.1126/science.1241165 · Cited by 5,413
Self-citation
The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism
den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D.-J., & Bakker, B. M. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r036012 · Cited by 5,048
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029
Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation
Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J. R., Pfeffer, K., Coffer, P. J., et al. (2013) · Nature · doi:10.1038/nature12726 · Cited by 4,838
Interactions Between the Microbiota and the Immune System
Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012) · Science · doi:10.1126/science.1223490 · Cited by 4,173
Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis
Yano, J. M., Yu, K., Donaldson, G. P., Shastri, G. G., Ann, P., Ma, L., Nagler, C. R., Ismagilov, R. F., Mazmanian, S. K., & Hsiao, E. Y. (2015) · Cell · doi:10.1016/j.cell.2015.02.047 · Cited by 3,614
Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee
Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., & Parfitt, A. M. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1805 · Cited by 2,543

Show all 65 references

Sorted by citations

Items 301–400 of 755

Deciphering the gut microbiome’s metabolic code: pathways to bone health and novel therapeutic avenues
Hwang, D., Chong, E. G., Li, Y., Li, Y., & Roh, K. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1553655 · Cited by 29
The gut microbiota in osteoporosis: dual roles and therapeutic prospects
Xie, X., Liu, H., Wan, K., Li, J., & Qi, P. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1617459 · Cited by 23
Characteristics of Gut Microbiome and Its Metabolites, Short-Chain Fatty Acids, in Children With Idiopathic Short Stature
Li, L., Chen, L., Yang, Y., Wang, J., Guo, L., An, J., Ma, X., Lü, W., Xiao, Y., Wang, X., et al. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.890200 · Cited by 24
Lactobacillus rhamnosus JYLR-005 Prevents Thiram-Induced Tibial Dyschondroplasia by Enhancing Bone-Related Growth Performance in Chickens
Liu, F., Kong, A., Fu, P.-F., Cao, Q., Tao, K.-S., Liu, D.-Y., Wang, X., Tong, Z.-X., Rehman, M. U., & Huang, S. (2020) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-020-09670-7 · Cited by 23
Tim4 deficiency reduces CD301b+ macrophage and aggravates periodontitis bone loss
Wang, Z., Zeng, H., Wang, C., Wang, J., Zhang, J., Qu, S., Han, Y., Liu, Y., Ni, Y., Peng, W., et al. (2024) · International Journal of Oral Science · doi:10.1038/s41368-023-00270-z · Cited by 27
Biomarkers of Human Gut Microbiota Diversity and Dysbiosis
Rüb, A., Tsakmaklis, A., Gräfe, S. K., Simon, M., Vehreschild, M. J. G. T., & Wüthrich, I. (2021) · Biomarkers in Medicine · doi:10.2217/bmm-2020-0353 · Cited by 24
The Mediating Role of the Gut Microbiota in the Physical Growth of Children
Durda, M., Ciomborowska-Basheer, J., Makałowska, I., & Szwed, A. (2022) · Life · doi:10.3390/life12020152 · Cited by 23
Bone Perspectives in Functional Hypothalamic Amenorrhoea: An Update and Future Avenues
Behary, P., & Comninos, A. N. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.923791 · Cited by 22
Osteoporosis and vascular calcifications
Martini, N., Streckwall, L., & McCarthy, A. D. (2023) · Endocrine Connections · doi:10.1530/ec-23-0305 · Cited by 22
A framework of biomarkers for skeletal aging: a consensus statement by the Aging Biomarker Consortium
Suo, J., Gan, Y., Xie, Y., Xu, S., Wang, J., Chen, D., Chen, L., Deng, L., Feng, S., Han, J. J., et al. (2023) · Life Medicine · doi:10.1093/lifemedi/lnad045 · Cited by 23
The Pan-liver Network Theory
Zhang, Y., & Fang, X.-M. (2023) · The Chinese Journal of Physiology · doi:10.4103/cjop.cjop-d-22-00131 · Cited by 22
Microbiota and Resveratrol: How Are They Linked to Osteoporosis?
Meyer, C., Brockmueller, A., de Porras, V. R., & Shakibaei, M. (2024) · Cells · doi:10.3390/cells13131145 · Cited by 24
The Stem Cell Division Theory of CancerPreprint
López‐Lázaro, M. (2017) · Preprints.org · doi:10.20944/preprints201707.0074.v1 · Cited by 21
The mechanism of action of indole-3-propionic acid on bone metabolism
Xu, H., Luo, Y., An, Y., & Wu, X. (2025) · Food & Function · doi:10.1039/d4fo03783a · Cited by 22
Enhancement of Lower Limb Muscle Strength and Reduction of Inflammation in the Elderly: A Randomized, Double-Blind Clinical Trial Comparing Lacticaseibacillus paracasei PS23 Probiotic with Heat-Treated Supplementation
Lee, M., Hsu, Y.-J., Yang, H.-J., & Huang, C. (2025) · Nutrients · doi:10.3390/nu17030463 · Cited by 21
Dried Plum’s Polyphenolic Compounds and Carbohydrates Contribute to Its Osteoprotective Effects and Exhibit Prebiotic Activity in Estrogen Deficient C57BL/6 Mice
Smith, B. J., Hatter, B., Washburn, K. F., Graef-Downard, J., Ojo, B. A., El-Rassi, G. D., Cichewicz, R. H., Payton, M. E., & Lucas, E. A. (2022) · Nutrients · doi:10.3390/nu14091685 · Cited by 23
Immunology of Gut-Bone Signaling
Collins, F. L., Schepper, J. D., Rios‐Arce, N. D., Steury, M. D., Kang, H. J., Mallin, H., Schoenherr, D. T., Camfield, G., Chishti, S., McCabe, L. R., et al. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-66653-2_5 · Cited by 22
Bone and the gut microbiome: a new dimension
Medina‐Gómez, C. (2018) · Journal of Laboratory and Precision Medicine · doi:10.21037/jlpm.2018.11.03 · Cited by 21
Nutritional support in cirrhotic patients with sarcopenia
Vasques, J., Guerreiro, C. S., Sousa, J., Pinto, M., & Cortez‐Pinto, H. (2019) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2019.07.011 · Cited by 21
Extracellular Matrix and Oxidative Phosphorylation: Important Role in the Regulation of Hypothalamic Function by Gut Microbiota
Qi, X., Zhong, X., Xu, S., Zeng, B., Chen, J., Zang, G., Zeng, L., Bai, S., Zhou, C., Wei, H., et al. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00520 · Cited by 21
Gut microbiome-mediated changes in bone metabolism upon infrared light exposure in rats
Lu, Y., Yang, J., Dong, C., Fu, Y., & Liu, H. (2021) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2021.112156 · Cited by 20
Gut microbiota in patients with newly diagnosed acromegaly: a pilot cross-sectional study
Hacıoğlu, A., Gündoğdu, A., Nalbantoglu, U., Karaca, Z., Urhan, M. E., Şahin, S., Dökmetaş, H. S., Kadıoğlu, P., Keleştimur, F., & Pituitary Microbiom Study Group (PITMIT-SG) (2021) · Pituitary · doi:10.1007/s11102-021-01137-4 · Cited by 21
Short-Chain Fatty Acids Calibrate RARα Activity Regulating Food Sensitization
Yuan, X., Tang, H., Wu, R., Li, X., Jiang, H., Liu, Z., & Zhang, Z. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.737658 · Cited by 21
Immune cells: the key mediator between the gut microbiota and osteoporosis
Ma, T., Zhang, T., Peng, C., Liu, K., Xiong, Y., Chen, K., Peng, N., Wei, Z., Kuang, J., & Ou, L. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1680021 · Cited by 22
Infants with cystic fibrosis have altered fecal functional capacities with potential clinical and metabolic consequences
Eng, A., Hayden, H. S., Pope, C. E., Brittnacher, M., Vo, A. T., Weiss, E. J., Hager, K. R., Leung, D. H., Heltshe, S. L., Raftery, D., et al. (2021) · BMC Microbiology · doi:10.1186/s12866-021-02305-z · Cited by 22
Communication in non-communicable diseases (NCDs) and role of immunomodulatory nutraceuticals in their management
Kumar, A., Sakhare, K. R., Bhattacharya, D., Chattopadhyay, R., Parikh, P. M., Narayan, K. P., & Mukherjee, A. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.966152 · Cited by 22
Gut microbiota-dependent trimethylamine n-oxide pathway contributes to the bidirectional relationship between intestinal inflammation and periodontitis
Wang, Q., Sun, Y., Zhou, T., Jiang, C., Lan, A., & Xu, W. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.1125463 · Cited by 23
Endocrine, Metabolic, and Immune Pathogenesis of Postmenopausal Osteoporosis. Is there a Therapeutic Role in Natural Products?
Lisco, G., Triggiani, D., Giagulli, V. A., Pergola, G. D., Guastamacchia, E., Piazzolla, G., Jirillo, E., & Triggiani, V. (2023) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530323666230330121301 · Cited by 20
Microbiota-Derived Short-Chain Fatty Acids Promote BMP Signaling by Inhibiting Histone Deacetylation and Contribute to Dentinogenic Differentiation in Murine Incisor Regeneration
Ren, Y., Su, S., Liu, X., Zhang, Y., Zhao, Y., & Xiao, E. (2020) · Stem Cells and Development · doi:10.1089/scd.2020.0057 · Cited by 20
Effects of 25‐ hydroxyvitamin D3 on growth performance, serum parameters, fecal microbiota, and metabolites in weaned piglets fed diets with low calcium and phosphorus
Zhang, L., Yang, M., & Piao, X. (2021) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.11388 · Cited by 20
Gut microbiota-mediated regulation of skeletal development: A review of mechanistic analysis and interventional strategies
Liu, C., Yang, Y., Guo, S., Cao, Y., Wang, L., & Wu, C. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.07.033 · Cited by 23
Microbes, metabolites and muscle: Is the gut–muscle axis a plausible therapeutic target in Duchenne muscular dystrophy?
Marullo, A. L., & O’Halloran, K. D. (2023) · Experimental Physiology · doi:10.1113/ep091063 · Cited by 24
Possible relationship between the gut leaky syndrome and musculoskeletal injuries: the important role of gut microbiota as indirect modulator
Álvarez‐Herms, J., González, A., Corbi, F., Odriozola, I., & Odriozola, A. (2023) · AIMS Public Health · doi:10.3934/publichealth.2023049 · Cited by 22
The Role of the Gut Microbiome in Health and Disease in the Elderly
Chen, L. A., & Boyle, K. (2024) · Current Gastroenterology Reports · doi:10.1007/s11894-024-00932-w · Cited by 22
The Role of G Protein-Coupled Receptors in the Regulation of Orthopaedic Diseases by Gut Microbiota
Sun, P., Liu, J., Chen, G., & Guo, Y. (2025) · Nutrients · doi:10.3390/nu17101702 · Cited by 19
The bone-protective mechanisms of active components from TCM drugs in rheumatoid arthritis treatment
Lu, Q., Xu, J., Jiang, H., Wei, Q., Huang, R., & Huang, G. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1000865 · Cited by 19
A systematic review of associations between gut microbiota composition and growth failure in preterm neonates
Neves, L. L., Hair, A. B., & Preidis, G. A. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2190301 · Cited by 18
Mechanism of action of gut microbiota and probiotic Lactobacillus rhamnosus GG on skeletal remodeling in mice
Tyagi, A. M. (2023) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.440 · Cited by 18
Gut microbiota and short-chain fatty acids signatures in postmenopausal osteoporosis patients: A retrospective study
Li, S., Wang, J., Zhang, Y., Wang, J., Zhou, T., Xie, Y., Zhou, Y., Tang, L., Hu, L., Dong, Q., et al. (2024) · Medicine · doi:10.1097/md.0000000000040554 · Cited by 17
The Mediating Role of Bioactive Molecules in Gut Microbiota–Bone Metabolism Crosstalk
Liang, X., & Wang, L. (2025) · Nutrients · doi:10.3390/nu17213421 · Cited by 19
Integrative Analysis of LGR5/6 Gene Variants, Gut Microbiota Composition and Osteoporosis Risk in Elderly Population
Di, D., Li, C., Dai, Y., Wei, M., Wang, S., Song, W., Zhou, H., Cui, Y., Zhang, R., Huang, Q., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.765008 · Cited by 17
Effects of High-Fructose Corn Syrup on Bone Health and Gastrointestinal Microbiota in Growing Male Mice
Han, X., Feng, Z., Chen, Y., Zhu, L., Li, X., Wang, X., Sun, H., & Li, J. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.829396 · Cited by 17
A systematic review and meta-analysis of the effects of probiotics on bone outcomes in rodent models
Yumol, J. L., Gittings, W., de Souza, R. J., & Ward, W. E. (2024) · Journal of Bone and Mineral Research · doi:10.1093/jbmr/zjae187 · Cited by 16
Gut microbiota and bone aging: Focusing on the gut-X axis modes
Zhang, Y.-W., Li, R.-Y., Wu, Y., Wang, P., Zhou, Q., & Su, J. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2026.101064 · Cited by 17
Excess Growth Hormone Alters the Male Mouse Gut Microbiome in an Age-dependent Manner
Jensen, E., Young, J. A., Jackson, Z., Busken, J., Kuhn, J., Onusko, M., Carroll, R. K., List, E. O., Brown, J. M., Kopchick, J. J., et al. (2022) · Endocrinology · doi:10.1210/endocr/bqac074 · Cited by 16
Identifying microbial signatures for patients with postmenopausal osteoporosis using gut microbiota analyses and feature selection approaches
Huang, D., Wang, J., Zeng, Y. H., Li, Q., & Wang, Y. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1113174 · Cited by 16
Christensenellaceae minuta modulates epithelial healing via PI3K-AKT pathway and macrophage differentiation in the colitis
Yao, T., Wu, Y., Fu, L., Lv, J., Lv, L., & Li, . (2024) · Microbiological Research · doi:10.1016/j.micres.2024.127927 · Cited by 17
The interplay between gut bacteria and targeted therapies: implications for future cancer treatments
He, J., Chen, Y., Zhao, H., & Li, Y. (2025) · Molecular Medicine · doi:10.1186/s10020-025-01108-6 · Cited by 20
Fundamentals of Human Bone and Dental Biology
Lynnerup, N., & Klaus, H. D. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809738-0.00004-1 · Cited by 19
Heritability and quantitative trait locus analyses of intermuscular bones in mirror carp (Cyprinus carpio)
Tang, G., Lv, W., Sun, Z., Cao, D., Zheng, X., Tong, G., Wang, H., Zhang, X., & Kuang, Y. (2019) · Aquaculture · doi:10.1016/j.aquaculture.2019.734601 · Cited by 17
Human Respiratory and Gut Microbiomes—Do They Really Contribute to Respiratory Health?
Durack, J., & Christophersen, C. T. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.00528 · Cited by 18
Microbial and nutritional influence on endocrine control of growth
Vadder, F. D., Joly, A., & Leulier, F. (2021) · Journal of Molecular Endocrinology · doi:10.1530/jme-20-0288 · Cited by 16
Effects of Stress on the Mucus-microbial Interactions in the Gut
He, J., Guo, H., Zheng, W., & Yao, W. (2018) · Current Protein and Peptide Science · doi:10.2174/1389203719666180514152406 · Cited by 17
Dietary fiber derived short-chain fatty acids as a critical driver of the gut–bone axis in animal bone health: A review
Zulfiqar, Z., Huang, S., & Shi, Y. (2025) · Animal nutrition · doi:10.1016/j.aninu.2025.05.002 · Cited by 17
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
Zhou, T., Sun, D., Li, X., Heianza, Y., LeBoff, M. S., Bray, G. A., Sacks, F. M., & Qi, L. (2021) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqab037 · Cited by 15
Exploring the regulatory mechanism of osteoporosis based on intestinal flora: A review
Awuti, K., Wang, X., Sha, L., & Leng, X. (2022) · Medicine · doi:10.1097/md.0000000000032499 · Cited by 16
Peiminine regulates bone‐fat balance by canonical Wnt/β‐catenin pathway in an ovariectomized rat model
Gu, H., & Wei, J. (2023) · Phytotherapy Research · doi:10.1002/ptr.7780 · Cited by 15
Effect of gastrodin against cognitive impairment and neurodegeneration in APP/PS1 mice via regulating gut microbiota–gut–brain axis
Zhang, Y., Chen, Y., Yuan, S., Yu, Q., Fu, J., Chen, L., Liu, J., & He, Y. (2023) · Experimental Brain Research · doi:10.1007/s00221-023-06632-7 · Cited by 15
Gut microbiota in regulation of childhood bone growth
Lui, J. C. K. (2023) · Experimental Physiology · doi:10.1113/ep091620 · Cited by 17
Dietary Clostridium butyricum and 25-Hydroxyvitamin D3 modulate bone metabolism of broilers through the gut—brain axis
Cao, G., Yu, Y., Wang, H., Yang, H., Tao, F., Yang, S., Liu, J., Li, Z., & Yang, C. (2024) · Poultry Science · doi:10.1016/j.psj.2024.103966 · Cited by 16
Renal Health Through Medicine–Food Homology: A Comprehensive Review of Botanical Micronutrients and Their Mechanisms
Zhao, Y., Song, J., Feng, R., Hu, J.-C., Xu, H., Ye, M.-L., Jiang, J.-D., Chen, L., & Wang, Y. (2024) · Nutrients · doi:10.3390/nu16203530 · Cited by 17
Progress of research on the gut microbiome and its metabolite short-chain fatty acids in postmenopausal osteoporosis: a literature review
Chen, Y., Xie, Y., & Yu, X. (2025) · Frontiers of Medicine · doi:10.1007/s11684-025-1129-3 · Cited by 16
Bone Health in Women With Polycystic Ovary Syndrome: A Narrative Review
Noroozzadeh, M., Amiri, M., Farhadi‐Azar, M., & Tehrani, F. R. (2022) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2022.02.005 · Cited by 14
Characterization of Fecal Microbiomes of Osteoporotic Patients in Korea
Ul-Haq, A., Seo, H., Jo, S., Park, H., Kim, S., Lee, Y., Lee, S., Jeong, J. H., & Song, H. (2022) · Polish Journal of Microbiology · doi:10.33073/pjm-2022-045 · Cited by 16
Causal effects of gut microbiota on scoliosis: A bidirectional two-sample mendelian randomization study
Lai, B.-W., Jiang, H., Gao, Y., & Zhou, X. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e21654 · Cited by 14
Aging Gut Microbiome in Healthy and Unhealthy Aging
Yangyanqiu, W., Qu, Z., Chu, J., & Han, S. (2024) · Aging and Disease · doi:10.14336/ad.2024.0331 · Cited by 17
SVHRSP protects against rotenone-induced neurodegeneration in mice by inhibiting TLR4/NF-κB-mediated neuroinflammation via gut microbiota
Chen, M., Zhang, Y., Hou, L., Zhao, Z., Tang, P., Sun, Q., Zhao, J., & Wang, Q. (2025) · npj Parkinson s Disease · doi:10.1038/s41531-025-00892-6 · Cited by 16
Does the gut microbiota contribute to the oligodendrocyte progenitor niche?
Sauma, S., & Casaccia, P. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134574 · Cited by 14
The Microbiota-Bone-Allergy Interplay
Sirufo, M. M., Pietro, F. D., Catalogna, A., Ginaldi, L., & Martinis, M. D. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19010282 · Cited by 14
Disaggregation as an interaction mechanism among intestinal bacteria
Sundarraman, D., Smith, T. J., Kast, J., Guillemin, K. J., & Parthasarathy, R. (2022) · Biophysical Journal · doi:10.1016/j.bpj.2022.08.010 · Cited by 14
Probiotic supplement as a promising strategy in early tau pathology prevention: Focusing on GSK-3β?
Flynn, C. M., & Yuan, Q. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1159314 · Cited by 15
Impact of continuous low-dose antibiotic prophylaxis on growth in children with vesicoureteral reflux
Guidos, P. J., Arlen, A. M., Leong, T. L., Bonnett, M. A., & Cooper, C. S. (2018) · Journal of Pediatric Urology · doi:10.1016/j.jpurol.2018.07.007 · Cited by 14
Intestinal Bacteroides sp. Imbalance Associated With the Occurrence of Childhood Undernutrition in China
Li, D., Li, Y., Dai, W., Wang, H. H., Qiu, C., Feng, S., Zhou, Q., Wang, W., Feng, X., Yao, K., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02635 · Cited by 15
Enhancing Akkermansia growth via phytohormones: a strategy to modulate the gut-bone axis in postmenopausal osteoporosis therapy
Zhao, Z., Deng, Y., Li, L., Zhū, L., Wang, X., Sun, H., Li, X., Han, X., & Li, J. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06426-1 · Cited by 14
Deletion of hepatic growth hormone receptor (GHR) alters the mouse gut microbiota by affecting bile acid metabolism
Yu, Z., Wang, Y., Zhang, F., Ma, R., Yang, X., Yang, K., Mi, A., Ran, L., & Wu, Y. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2221098 · Cited by 13
Alteration in the gut microbiome is associated with changes in bone metabolism after laparoscopic sleeve gastrectomy
Wu, K. C., McCauley, K. E., Lynch, S. V., Nayak, R. R., King, N. J., Patel, S., Kim, T. Y., Condra, K., Fadrosh, D., Nguyen, D., et al. (2024) · Journal of Bone and Mineral Research · doi:10.1093/jbmr/zjad017 · Cited by 13
Gut microbiota alterations in postmenopausal women with osteoporosis and osteopenia from Shanghai, China
Ji, J., Zhengrong, G., Li, N., Dong, X. W., Wang, X., Yao, Q., Zhang, Z., Zhang, L., & Cao, L. (2024) · PeerJ · doi:10.7717/peerj.17416 · Cited by 15
Gut microbial dysbiosis and inflammation: Impact on periodontal health
Zhao, Y., Liu, Y. F., & Lü, J. (2024) · Journal of Periodontal Research · doi:10.1111/jre.13324 · Cited by 14
The Link Between the Gut Microbiome and Bone Metastasis
Ševčíková, A., Martiniaková, M., Omelka, R., Števurková, V., & Čierniková, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212086 · Cited by 14
Bone Mechanical Function and the Gut Microbiota
Hernandez, C. J. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-66653-2_12 · Cited by 13
Gut microbiota
Schwarzer, M. (2018) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000463 · Cited by 14
The gut microbiota can be a potential regulator and treatment target of bone metastasis
Contino, K. F., Yadav, H., & Shiozawa, Y. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.114916 · Cited by 14
Alterations in the fecal microbiota and serum metabolome in unstable angina pectoris patients
Liu, L., & Luo, F. (2022) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2703100 · Cited by 14
Targeting the gut to prevent and counteract metabolic disorders and pathologies during aging
Milenković, D., Capel, F., Combaret, L., Comte, B., Dardevet, D. P., Evrard, B., Guillet, C., Monfoulet, L., Pinel, A., Polakof, S., et al. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2089870 · Cited by 14
The Human Microbiome and Its Role in Musculoskeletal Disorders
Aboushaala, K. A., Wong, A. Y. L., Barajas, J. N., Lim, P., Al‐Harthi, L., Chee, A., Forsyth, C. B., Oh, C., Toro, S. J., Williams, F. M. K., et al. (2023) · Genes · doi:10.3390/genes14101937 · Cited by 13
Maternal supplementation with a combination of wheat bran and sugar beet pulp during late gestation and lactation improves growth and intestinal functions in piglets
Shang, Q., Liu, S., Liu, H., Mahfuz, S. U., & Piao, X. (2021) · Food & Function · doi:10.1039/d1fo00014d · Cited by 14
Inferring Bacterial Community Interactions and Functionalities Associated with Osteopenia and Osteoporosis in Taiwanese Postmenopausal Women
Kuo, Y., Chen, C., Hussain, B., Tsai, H., Hsu, G., Chen, J., Asif, A., Fan, C.-W., & Hsu, B. (2023) · Microorganisms · doi:10.3390/microorganisms11020234 · Cited by 12
Emerging nanotherapeutic strategies targeting gut-X axis against diseases
Sun, A., Liu, H., Sun, M., Yang, W., Liu, J., Lin, Y., Shi, X., Sun, J. Y., & Liu, L. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115577 · Cited by 13
Lactobacillus plantarum AR495 improves bone health of ovariectomized mice by improving gut microbiota
Zhang, H., Xia, Y., Yu, J., Wang, G., Xiong, Z., Zhang, H., Song, X., Yang, Y., Wei, G., & Ai, L. (2024) · Food Frontiers · doi:10.1002/fft2.359 · Cited by 12
Mechanisms of Male Reproductive Sterility Triggered by Dysbiosis of Intestinal Microorganisms
Wei, M., Liu, H., Wang, Y., Sun, M., & Shang, P. (2024) · Life · doi:10.3390/life14060694 · Cited by 15
Butyric Acid Modulates Gut Microbiota to Alleviate Inflammation and Secondary Bone Loss in Ankylosing Spondylitis
You, K., Yang, L., Su, Z., Shen, J., Fan, X., Guo, Y., Yuan, Z., & Lü, H. (2024) · Biomedicines · doi:10.3390/biomedicines13010009 · Cited by 13
Clinical correlation between intestinal flora profiles and the incidence of postmenopausal osteoporosis
Zhu, C., Zhang, Y., Pan, Y., Zhang, Z., Liu, Y., Lin, X., Cai, J., Xiong, Z., Pan, Y., & Nie, H. (2025) · Gynecological Endocrinology · doi:10.1080/09513590.2025.2465587 · Cited by 15
The Role of Probiotics in Modulating the Gut Microbiome in Alzheimer’s Disease: A Review
Dong, Y., Wu, X., Zhang, Y., Hu, A., Zhou, Q., Yue, X., Liu, Z., & Li, M. (2025) · Foods · doi:10.3390/foods14091531 · Cited by 15
Reconstitution of the host holobiont in germ-free born male rats acutely increases bone growth and affects marrow cellular content
Czernik, P. J., Golonka, R. M., Chakraborty, S., Yeoh, B. S., Abokor, A. A., Saha, P., Yeo, J., Mell, B., Cheng, X., Baroi, S., et al. (2021) · Physiological Genomics · doi:10.1152/physiolgenomics.00017.2021 · Cited by 13
Mathematical Modeling of the Gut–Bone Axis and Implications of Butyrate Treatment on Osteoimmunology
Islam, M. A., Cook, C. V., Smith, B. J., & Versypt, A. N. F. (2021) · Industrial & Engineering Chemistry Research · doi:10.1021/acs.iecr.1c02949 · Cited by 12
Lack of berberine effect on bone mechanical properties in rats with experimentally induced diabetes
Londzin, P., Kocik, S., Kisiel-Nawrot, E., Janas, A., Skoczyńska, A., Krivošíková, Z., Stefikova, K., Gajdoš, M., Cegieła, U., & Folwarczna, J. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112562 · Cited by 13
MGF-19E peptide promoted proliferation, differentiation and mineralization of MC3T3-E1 cell and promoted bone defect healing
Wei, W., Liu, S., Song, J., Feng, T., Yang, R., Cheng, Y., Li, H., & Hao, L. (2020) · Gene · doi:10.1016/j.gene.2020.144703 · Cited by 12
Deciphering Osteosarcopenia through the hallmarks of aging
Franulic, F., Salech, F., Rivas, D., & Duque, G. (2024) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2024.111997 · Cited by 14
Dental Pulp Stem Cell Conditioned Medium Enhance Osteoblastic Differentiation and Bone Regeneration
Chouaib, B., Desoutter, A., Cuisinier, F., & Collart-Dutilleul, P.-Y. (2024) · Stem Cell Reviews and Reports · doi:10.1007/s12015-024-10823-2 · Cited by 11
Effects of Supplementation with Encapsulated Different Postbiotics, Alone or with Inulin, on Growth Performance, Carcass and Organ Characteristics, Blood Parameters, Growth Hormone, and Insulin-like Growth Factor mRNA in Broilers
Atan, H., & Kırkpınar, F. (2025) · Animals · doi:10.3390/ani15071010 · Cited by 12

Authors: Yan, J., Herzog, J. W., Tsang, K., Brennan, C. A., Bower, M. A., Garrett, W. S., Sartor, B. R., Aliprantis, A. O., & Charles, J. F.
Affiliations: Brigham and Women's Hospital (US)
University of North Carolina at Chapel Hill (US)
Harvard University (US)
Broad Institute (US)
National Gnotobiotic Rodent Resource Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
Corresponding author: Charles, Julia F.
ORCID: Yan, Jing
Herzog, Jeremy W.
Brennan, Caitlin A.
Garrett, Wendy S.
Aliprantis, Antonios O.
Charles, Julia F.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2016-11-07
Volume: 113
Issue: 47
Pages: E7554-E7563
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1607235113
PMC: PMC5127374
OpenAlex: W2556090133
Cited by: 750
References: 65
Citations by year: 2026: 83 · 2025: 94 · 2024: 110 · 2023: 94 · 2022: 76 · 2021: 93 · 2020: 67 · 2019: 52 · 2018: 46 · 2017: 29 · 2016: 2
FWCI: 22.36
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.pnas.org/site/misc/userlicense.xhtml (vor, 181 d)
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: HHS | NIH | National Institute on Aging (AG046257)
HHS | NIH | National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR062590)
HHS | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (P30-DK034987)
HHS | NIH | NIH Office of the Director (5-P40-OD010995)
HHS | NIH | National Cancer Institute (CA154426)
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 › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
Keywords: gut microbiota, insulin-like growth factor I, bone formation, bone growth, bone mass, germ-free mice, microbial colonization, bone resorption, growth plate, short-chain fatty acids, antibiotic therapy, bone health, skeletal development
MeSH terms: Gastrointestinal Microbiome, Adipose Tissue, Animals, Bone and Bones, Bone Development, Fatty Acids, Volatile, Female, Insulin-Like Growth Factor I, Liver, Male, Osteogenesis, Specific Pathogen-Free Organisms, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Gut microbiota induce IGF-1 and promote bone formation and growth

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks