Interaction between the intestinal microbiome and bone
Main Article Content
Abstract
The microbiome is not only constituted by microbes, but by all the components that live in the same habitat forming an ecological niche. It is conformed by the microorganisms ( bacteria, fungi, protozoa, etc), the entire spectrum of molecules produced by them (nucleic acids, proteins, lipid and carbohydrates, metabolites, toxins, etc) and the molecules produced by the host. The intestinal microbiome (IM) has emerged as a factor with great effects on the quantity, quality and strength of bone. The investigations reveal that bone homeostasis is linked to the healthy microbiome, while the dysbiosis (alteration in the microbial biodiversity) can exacerbate the osteoclastic activity and promote osteoporosis. The potential mechanisms involved in the interaction between IM and bone are the influence of the host metabolism, the maintenance of the intestinal integrity and regulation of the nutrient absorption, the regulation of the intestine/ immune system axis and the modulation of the endocrine system. That is, there are multiple ways through which IM influences on bone, but these and other mechanisms need to be further studied. It is also necessary to identify and characterize the microorganisms associated with the bone diseases. Knowledge of these aspects could be useful to develop therapeutical tools based on the IM that could improve the efficacy of the current treatments.
Article Details
Derechos de autor: Actualizaciones en Osteología es la revista oficial de la Asociación Argentina de Osteología y Metabolismo Mineral (AAOMM) que posee los derechos de autor de todo el material publicado en dicha revista.
References
Marchesi J, Ravel J. The vocabularyof microbiome research: a proposal.Microbiome 2015; 3:31. doi: 10.1186/s40168-015-0094-5.
Bhardwaj A, Sapra L, Tiwari A,Mishra PK, Sharma S, SrivastavaRK. “Osteomicrobiology”: The NexusBetween Bone and Bugs. Frontiers in Microbiology 2022; 12:812466. doi: 10.3389/fmicb.2021.812466.
Berg G, Rybakova D, Fischer D, et al.Microbiome definition re-visited: oldconcepts and new challenges. Microbiome2020;8:103. doi: 10.1186/s40168-020-00875-0.
Sommer F, Bäckhed F. The gut microbiota--masters of host development andphysiology. Nat Rev Microbiol 2013;11:227-38. doi: 10.1038/nrmicro2974.
Annalisa N, Alessio T, Claudette TD,Erald V, Antonino DL, Nicola DD. GutMicrobioma Population: An IndicatorReally Sensible to Any Change in Age,Diet, Metabolic Syndrome, and Life-Style.Mediators Inflamm 2014; 901308.doi:10.1155/2014/901308.
Rinninella E, Raoul P, Cintoni M, et al.What is the Healthy Gut MicrobiotaComposition? A Changing Ecosystemacross Age, Environment, Diet, andDiseases. Microorganisms 2019; 7:14. doi:10.3390/microorganisms7010014.
Thursby E, Juge N. Introduction to thehuman gut microbiota. Biochemical J 2017; 474:1823-36. doi: 10.1042/BCJ20160510.
Ding K, Hua F, Ding W. Gut Microbiomeand Osteoporosis. Aging and Dis 2020;11:438-47. doi: 10.14336/AD.2019.0523
Ramos C, Gibson GR, Walton GE,Magistro D, Will Kinnear W, Hunter K.Systematic Review of the Effects ofExercise and Physical Activity on the GutMicrobiome of Older Adults. Nutrients2022; 14:674. doi: 10.3390/nu14030674.
Behera J, Ison J, Tyagi SC, Tyagi N. Therole of gut microbiota in bone homeostasis. Bone 2020; 135:115317. doi: 10.1016/j.bone.2020.115317.
McDaniel L, Breitbart M, MobberleyJ, et al. Metagenomic Analysis ofLysogeny in Tampa Bay: Implicationsfor Prophage Gene Expression. PLoSOne 2008; 3:e3263. doi: 10.1371/journal.pone.0003263.
Ionescu RF, Enache RM, Cretoiu SM,Cretoiu D. The Interplay Between GutMicrobiota and miRNAs in CardiovascularDiseases. Front Cardiovasc Med 2022;9:856901. doi: 10.3389/fcvm.2022.856901.
Eckburg PB, Bik EM, Bernstein CN, et al.Diversity of the human intestinal microbialflora. Science 2005 10;308:1635-8. doi: 10.1126/science.1110591.
Mariat D, Firmesse O, Levenez F. TheFirmicutes/Bacteroidetes ratio of the humanmicrobiota changes with age. BMC Microbio2009; 9:123. doi: 10.1186/1471-2180-9-123.
Dominguez-Bello MG, Costello EK,Contreras M. Delivery mode shapesthe acquisition and structure of theinitial microbiota across multiple bodyhabitats in newborns. Proc Natl AcadSci USA 2010;107:11971-5. doi:10.1073/pnas.1002601107.
Shukla SD, Budden KF, Neal R, Hansbro PM. Microbiome effects on immunity, health anddisease in the lung. Clin Transl Immunology2017; 6:e133. doi: 10.1038/cti.2017.6.
Rodríguez JM, Murphy K, Stanton C, etal. The composition of the gut microbiotathroughout life, with an emphasis on earlylife. Microb Ecol Health Dis 2015;26:26050.doi: 10.3402/mehd.v26.26050.
Yuan Y, Yang J, Zhuge A, Li L, Ni S. Gutmicrobiota modulates osteoclast glutathione synthesis and mitochondrial biogenesis inmice subjected to ovariectomy. Cell Prolif2022; 55:e13194. doi: 10.1111/cpr.13194.
Seely KD, Kotelko CA, Douglas H, BealerB, Brooks AE. The Human Gut Microbiota:A Key Mediator of Osteoporosis andOsteogenesis. Int J Mol Sci 2021; 22:9452.doi: 10.3390/ijms22179452.
Sjögren K, Engdahl C, Henning P, et al.The gut microbiota regulates bone mass inmice. J. Bone Miner Res 2012; 27:1357-67.doi: 10.1002/jbmr.1588.
Yan J, Charles J F. Gut Microbiome andBone: to Build, Destroy, or Both? CurrOsteoporos Rep 2017; 15: 376-84. doi:10.1007/s11914-017-0382-z.
Ibáñez L, Rouleau M, Wakkach A, Blin-Wakkach C. Gut microbiome and bone.Joint Bone Spine 2019; 86: 43-7. doi:10.1016/j.jbspin.2018.02. 008.
Wallace TC, Marzorati M, Spence L,Weaver CM, Williamson PS. New frontiers in fibers: Innovative and emerging research on the gut microbiome and bone health. J Am Coll Nutr 2017;36:218-22. doi: 10.1080/07315724.2016.1257961.
Ohlsson C, Engdahl C, Fåk F, et al.Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One2014; 9:e92368. doi: 10.1371/journal.pone.0092368.
Cho I, Yamanishi S, Cox L, et al. Antibioticsin early life alter the murine colonicmicrobiome and adiposity. Nature 2012;488: 621-6. doi: 10.1038/nature11400.
Cox LM, Yamanishi S, Sohn J, et al. Alteringthe Intestinal Microbiota during a CriticalDevelopmental Window Has LastingMetabolic Consequences. Cell 2014;158:705-21. doi: 10.1016/ j.cell.2014.05.052.
Mikkelsen KH, Vilsbøll T, Holst JJ, Hartmann B, Knop FK, Frost M. No changes in levelsof bone formation and resorption markersfollowing a broad-spectrum antibioticcourse. BMC Endocr Disord 2018; 18:60.doi: 10.1186/s12902-018-0291-x.
Ríos-Arce ND, Schepper JD, Dagenais A,et al. Post-antibiotic gut dysbiosis-inducedtrabecular bone loss is dependent onlymphocytes. Bone 2020; 134:115269. doi:10.1016/j.bone.2020.115269.
Fiorucci S, Biagioli M, Zampella A, DistruttiE.Bile Acids Activated Receptors RegulateInnate Immunity. Front Immunol 2018;9:1853. doi: 10.3389/fimmu.2018.01853.
Cho SW, An JH, Park H, et al. Positiveregulation of osteogenesis by bileacid through FXR. J Bone Miner Res2013;28:2109-21. doi: 10.1002/jbmr.1961.
Marchionatti AM, Pérez A, Rivoira MA,Rodríguez VA, Tolosa de Talamoni NG.Lithocholic acid: a new emergent protectorof intestinal calcium absorption underoxidant conditions. Biochem Cell Biol2017;95:273-9. doi: 10.1139/bcb-2016-0164.
Muniz LR, Knosp C, Yeretssian G.Intestinal antimicrobial peptides duringhomeostasis, infection, and disease. Front Immunol 2012;3:310. doi: 10.3389/fimmu.2012.00310.
Li J-Y, Chassaing B, Tyagi AM, et al. Sexsteroid deficiency–associated bone lossis microbiota dependent and prevented byprobiotics. J Clin Invest 2016;126:2049-63.doi: 10.1172/JCI86062.
Nakajima M, Arimatsu K, Kato T, et al.Oral administration of P. gingivalis inducesdysbiosis of gut microbiota and impairedbarrier function leading to disseminationof enterobacteria to the liver. PLoS One2015;10:0134234. doi: 10.1371/journal.pone.0134234.
Matei DE, Menon M, Alber DG, et al.Intestinal barrier dysfunction plays anintegral role in arthritis pathology and canbe targeted to ameliorate disease. Med(NY) 2021;2:864.e–883.e. doi:10.1016/j.medj.2021.04.013.
McKenzie C, Tan J, Macia L, Mackay CR.The nutrition-gut microbiome-physiologyaxis and allergic diseases. Immunol Rev2017;278:277-95.doi: 10.1111/imr.12556. doi:10.1111/imr.12556.
Vaughn AC, Cooper EM, DiLorenzo PM,et al. Energy-dense diet triggers changesin gut microbiota, reorganization of gut-brain vagal communication and increasesbody fat accumulation. Acta Neurobiol Exp2017;77:18-30. doi: 10.21307/ane-2017-033.
Rowland I, Gibson G, Heinken A, et al.Gut microbiota functions: metabolism ofnutrients and other food components. Eur JNutr 2018;57:1-24. doi: 10.1007/s00394-017-1445-8.
Lucas S, Omata Y, Hofmann J, et al. Short-chain fatty acids regulate systemic bonemass and protect from pathological boneloss. Nat Commun 2018; 9:55.doi: 10.1038/s41467-017-02490-4.
Tabatabaeizadeh S-A, Fazeli M, MeshkatZ, et al. The effects of high doses ofvitamin D on the composition of the gutmicrobiome of adolescent girls. Clin Nutr ESPEN 2020;35:103-8. doi: 10.1016/j.clnesp.2019.10.020.
Jones ML, Martoni CJ, Prakash S. Oralsupplementation with probiotic L. reuteriNCIMB 30242 increases mean circulating25-hydroxyvitamin D: a post hoc analysisof a randomized controlled trial. J ClinEndocrinol Metab 2013;98:2944-51. doi:10.1210/jc.2012-4262.
Wang M, Tian T, Yu S, He N, Ma D. Th17and Treg Cells in Bone Related Diseases.Clin Dev Immunol 2013;203705. doi:10.1155/2013/20 3705
Sapra L, Azam Z, Rani L, et al. Immunoporosis: Immunology of Osteoporosis. Proc NatlAcad Sci India Sect. B Biol Sci.2021. doi:10.1007/s40011-021-01238-x.
Ivanov II, Littman DR. Segmentedfilamentous bacteria take the stage.Mucosal Immunol 2010; 3: 209-12. doi:10.1038/mi.2010.3.
Rosser EC, Mauri C. Regulatory BCells: Origin, Phenotype, and Function.Immunity 2015;42: 607-12. doi: 10.1016/j.immuni.2015.04.005
Asarat M, Apostolopoulos V, Vasiljevic T,Donkor O. Short-Chain Fatty Acids RegulateCytokines and Th17/Treg Cells in HumanPeripheral Blood Mononuclear Cells in vitro.Immunol Invest 2016;205-22. doi: 10.3109/08820139.2015.1122613.
Rosser EC, Piper CJM, Matei DE, et al.Microbiota-Derived Metabolites SuppressArthritis by Amplifying Aryl-HydrocarbonReceptor Activation in Regulatory B Cells.Cell Metab 2020; 31: 837-51.e10. doi:10.1016/j.cmet.2020.03.003.
Li J-Y, Yu M, Pal S, et al. Parathyroidhormone-dependent bone formationrequires butyrate production by intestinalmicrobiota. J Clin Invest 2020;130:1767-81. doi: 10.1172/JCI133473.
Yan J, Herzog JW, Tsang K, et al. Gutmicrobiota induce IGF-1 and promote boneformation and growth. Proc Natl Acad SciUSA 2016;113:E7554-63. doi: 10.1073/pnas.1607235113.
Yano JM, Yu K, Donaldson GP, et al.Indigenous bacteria from the gut microbiotaregulate host serotonin biosynthesis.Cell 2015;161:264-76. doi: 10.1016/j.cell.2015.02.047.
Yu M, Tyagi AM, Li JY, et al. PTH inducesbone loss via microbial-dependentexpansion of intestinal TNF(+) T cells andTh17 cells. Nat Commun 2020;11:468. doi:10.1038/s41467-019-14148-4.
Schwarzer M, Makki K, Storelli G, et al.Lactobacillus plantarum strain maintainsgrowth of infant mice during chronicundernutrition. Science 2016;351:854-7. doi:10.1126/science.aad8588.
Tu Y, Yang R, Xu X, Zhou X . Themicrobiota-gut-bone axis and bone healthJ Leukoc Biol 2021;110:525-37 doi: 10.1002/JLB.3MR0321-755R.
Britton RA, Irwin R, Quach D, et al. ProbioticL.reuteri treatment prevents bone lossin a menopausal ovariectomized mousemodel. J Cell Physiol 2014;229:1822-30. doi:10.1002/jcp.24636.
Sato A, Pellegrini G, Crecory M, et al.Skeletal Protection and Promotion ofMicrobiome Diversity by Dietary Boostingof the Endogenous Antioxidant ResponseJ Bone Miner Res 2021;36:768-78. Doi:10.1002/jbmr.4231.
Rizzoli R, Biver E. Are Probiotics the NewCalcium and Vitamin D for Bone Health?Curr Osteoporos Rep 2020;18:273-84.doi:10.1007/s11914-020-00591-6.
Castaneda M, Strong JM, Alabi DA,Hernández CJ. The gut microbiome and bonestrength. Curr Osteoporos Rep 2020;18:677-83.doi:10.1007/s11914-00627-x.
Chen Y, Wang X, Zhang C, Liu Z, LiC, Ren Z. Gut Microbiota and BoneDiseases: A GrowingPartnership. FrontMicrobiol 2022 (https://doi.org/10.3389/fmicb.2022.877776).