2,357
Views
56
CrossRef citations to date
0
Altmetric
Article

Gut microbiota-bone axis

, &
Pages 1664-1672 | Received 28 Nov 2014, Accepted 16 Jan 2015, Published online: 01 Mar 2017

References

  • Assessment of Fracture Risk and its Application to Screening for Postmenopausal Osteoporosis. (1994). WHO technical report series Geneva.
  • Adlerberth, I. and Wold, A. E. (2009). Establishment of the gut microbiota in Western infants. Acta Paediatr. 98:229–238.
  • Akesson, K., Marsh, D., Mitchell, P. J., et al. (2013). Capture the Fracture: A Best Practice Framework and global campaign to break the fragility fracture cycle. Osteoporos. Int. 24:2135–2152.
  • Arai, F., Miyamoto, T., Ohneda, O., et al. (1999). Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J. Exp. Med. 190:1741–1754.
  • Avella, M. A., Place, A., Du, S. J., et al. (2012). Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems. PLoS One. 7:e45572.
  • Avershina, E., Storro, O., Oien, T., et al. (2014). Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol. Ecol. 87:280–290.
  • Backhed, F., Ding, H., Wang, T., et al. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA. 101:15718–15723.
  • Backhed, F., Fraser, C. M., Ringel, Y., et al. (2012). Defining a healthy human gut microbiome: Current concepts, future directions, and clinical applications. Cell Host. Microbe. 12:611–622.
  • Baird, J., Kurshid, M. A., Kim, M., et al. (2011). Does birthweight predict bone mass in adulthood? A systematic review and meta-analysis. Osteoporos. Int. 22:1323–1334.
  • Biagi, E., Nylund, L., Candela, M., et al. (2010). Through ageing, and beyond: Gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 5:e10667.
  • Bliziotes, M., Eshleman, A., Burt-Pichat, B., et al. (2006). Serotonin transporter and receptor expression in osteocytic MLO-Y4 cells. Bone. 39:1313–1321.
  • Boyle, W. J., Simonet, W. S. and Lacey, D. L. (2003). Osteoclast differentiation and activation. Nature. 423:337–342.
  • Britton, R. A., Irwin, R., Quach, D., et al. (2014). Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J. Cell. Physiol.
  • Campbell, J. M., Fahey, G. C., Jr., Wolf, B. W. (1997). Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J. Nutr. 127:130–136.
  • Cani, P. D., Amar, J., Iglesias, M. A., et al. (2007a). Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 56:1761–1772.
  • Cani, P. D., Neyrinck, A. M., Fava, F., et al. (2007b). Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 50:2374–2383.
  • Chen, D. and Zhao, C. M. (2011). The possible existence of a gut-bone axis suggested by studies of genetically manipulated mouse models? Curr. Pharm. Des. 17:1552–1555.
  • Chiang, S. S. and Pan, T. M. (2011). Antiosteoporotic effects of Lactobacillus -fermented soy skim milk on bone mineral density and the microstructure of femoral bone in ovariectomized mice. J. Agric. Food Chem. 59:7734–7742.
  • Chonan, O., Matsumoto, K. and Watanuki, M. (1995). Effect of galactooligosaccharides on calcium absorption and preventing bone loss in ovariectomized rats. Biosci. Biotechnol. Biochem. 59:236–239.
  • Chonan, O. and Watanuki, M. (1996). The effect of 6′-galactooligosaccharides on bone mineralization of rats adapted to different levels of dietary calcium. Int. J. Vitam. Nutr. Res. 66:244–249.
  • Claesson, M. J., Jeffery, I. B., Conde, S., et al. (2012). Gut microbiota composition correlates with diet and health in the elderly. Nature. 488:178–184.
  • Cote, F., Thevenot, E., Fligny, C., et al. (2003). Disruption of the nonneuronal tph1 gene demonstrates the importance of peripheral serotonin in cardiac function. Proc. Natl. Acad. Sci. USA. 100:13525–13530.
  • Cui, Y., Niziolek, P. J., MacDonald, B. T., et al. (2011). Lrp5 functions in bone to regulate bone mass. Nat. Med. 17:684–691.
  • Czerwinski, E., Badurski, J. E., Marcinowska-Suchowierska, E., et al. (2007). Current understanding of osteoporosis according to the position of the World Health Organization (WHO) and International Osteoporosis Foundation. Ortop. Traumatol. Rehabil. 9:337–356.
  • De Palma, G., Nadal, I., Medina, M., et al. (2010). Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 10:63.
  • Dial, S., Alrasadi, K., Manoukian, C., et al. (2004). Risk of Clostridium difficile diarrhea among hospital inpatients prescribed proton pump inhibitors: Cohort and case-control studies. CMAJ. 171:33–38.
  • Dixon, D. R. and Darveau, R. P. (2005). Lipopolysaccharide heterogeneity: Innate host responses to bacterial modification of lipid a structure. J. Dent. Res. 84:584–595.
  • Dobber, R., Hertogh-Huijbregts, A., Rozing, J., et al. (1992). The involvement of the intestinal microflora in the expansion of CD4+ T cells with a naive phenotype in the periphery. Dev. Immunol. 2:141–150.
  • Engelbregt, M. J., van Weissenbruch, M. M., Lips, P., et al. (2004). Body composition and bone measurements in intra-uterine growth retarded and early postnatally undernourished male and female rats at the age of 6 months: Comparison with puberty. Bone. 34:180–186.
  • Faith, J. J., Guruge, J. L., Charbonneau, M., et al. (2013). The long-term stability of the human gut microbiota. Science. 341:1237439.
  • Fanca-Berthon, P., Hoebler, C., Mouzet, E., et al. (2010). Intrauterine growth restriction not only modifies the cecocolonic microbiota in neonatal rats but also affects its activity in young adult rats. J. Pediatr. Gastroenterol. Nutr. 51:402–413.
  • FAO/WHO. (2001). Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria 2001.
  • Favier, C. F., Vaughan, E. E., De Vos, W. M., et al. (2002). Molecular monitoring of succession of bacterial communities in human neonates. Appl. Environ. Microbiol. 68:219–226.
  • Frank, D. N., St Amand, A. L., Feldman, R. A., et al. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA. 104:13780–13785.
  • Furet, J. P., Kong, L. C., Tap, J., et al. (2010). Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: Links with metabolic and low-grade inflammation markers. Diabetes. 59:3049–3057.
  • Gershon, M. D. and Tack, J. (2007). The serotonin signaling system: From basic understanding to drug development for functional GI disorders. Gastroenterology. 132:397–414.
  • Gosalbes, M. J., Llop, S., Valles, Y., et al. (2013). Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy. 43:198–211.
  • Greco, E. A., Fornari, R., Rossi, F., et al. (2010). Is obesity protective for osteoporosis? Evaluation of bone mineral density in individuals with high body mass index. Int. J. Clin. Pract. 64:817–820.
  • Gupta, S. and Shen, B. (2013). Bone loss in patients with the ileostomy and ileal pouch for inflammatory bowel disease. Gastroenterol. Rep. (Oxf). 1:159–165.
  • Harvey, N., Dennison, E. and Cooper, C. (2014). Osteoporosis—A lifecourse approach. J. Bone Miner. Res.
  • Hernandez, C. J., Beaupre, G. S. and Carter, D. R. (2003). A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos. Int. 14:843–847.
  • Hill, C., Guarner, F., Reid, G., et al. (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11:506–514.
  • Holzapfel, W. H., Haberer, P., Snel, J., et al. (1998). Overview of gut flora and probiotics. Int. J. Food Microbiol. 41:85–101.
  • Inose, H., Zhou, B., Yadav, V. K., et al. (2011). Efficacy of serotonin inhibition in mouse models of bone loss. J. Bone Miner. Res. 26:2002–2011.
  • Javaid, M. K., Crozier, S. R., Harvey, N. C., et al. (2006). Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: A longitudinal study. Lancet. 367:36–43.
  • Johnell, O. (1997). The socioeconomic burden of fractures: Today and in the 21st century. Am. J. Med. 103:20S–25S; discussion 25S–26S.
  • Johnell, O. and Kanis, J. A. (2006). An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos. Int. 17:1726–1733.
  • Kajiya, M., Giro, G., Taubman, M. A., et al. (2010). Role of periodontal pathogenic bacteria in RANKL-mediated bone destruction in periodontal disease. J. Oral. Microbiol. 2.
  • Kalliomaki, M., Collado, M. C., Salminen, S., et al. (2008). Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 87:534–538.
  • Kao, C. and Levytam, S. (2009). The Role of the ‘eubiotic’ diet in intestinal dysbiosis and hypertension. International Journal of Naturopathic Medicine 4:42–49.
  • Kelly, C. J., Colgan, S. P. and Frank, D. N. (2012). Of microbes and meals: The health consequences of dietary endotoxemia. Nutr. Clin. Pract. 27:215–225.
  • Kim, J. H., Choi, H. J., Kim, M. J., et al. (2012). Fat mass is negatively associated with bone mineral content in Koreans. Osteoporos. Int. 23:2009–2016.
  • Kimoto-Nira, H., Suzuki, C., Kobayashi, M., et al. (2007). Anti-ageing effect of a lactococcal strain: Analysis using senescence-accelerated mice. Br. J. Nutr. 98:1178–1186.
  • Lan, G. Q., Abdullah, N., Jalaludin, S., et al. (2002). Efficacy of supplementation of a phytase-producing bacterial culture on the performance and nutrient use of broiler chickens fed corn-soybean meal diets. Poult. Sci. 81:1522–1532.
  • Ley, R. E., Backhed, F., Turnbaugh, P., et al. (2005). Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA. 102:11070–11075.
  • Ley, R. E., Turnbaugh, P. J., Klein, S., et al. (2006). Microbial ecology: Human gut microbes associated with obesity. Nature. 444:1022–1023.
  • Liu, D., Xu, J. K., Figliomeni, L., et al. (2003). Expression of RANKL and OPG mRNA in periodontal disease: Possible involvement in bone destruction. Int. J. Mol. Med. 11:17–21.
  • Lorenzo, J., Horowitz, M. and Choi, Y. (2008). Osteoimmunology: Interactions of the bone and immune system. Endocr. Rev. 29:403–440.
  • Mackie, R. I., Sghir, A. and Gaskins, H. R. (1999). Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69:1035S–1045S.
  • Macpherson, A. J. and Harris, N. L. (2004). Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4:478–485.
  • Manichanh, C., Rigottier-Gois, L., Bonnaud, E., et al. (2006). Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 55:205–211.
  • Maradonna, F., Gioacchini, G., Falcinelli, S., et al. (2013). Probiotic supplementation promotes calcification in Danio rerio larvae: A molecular study. PLoS One. 8:e83155.
  • Mariat, D., Firmesse, O., Levenez, F., et al. (2009). The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9:123.
  • Markle, J. G., Frank, D. N., Mortin-Toth, S., et al. (2013). Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 339:1084–1088.
  • Martel, F. (2006). Recent advances on the importance of the serotonin transporter SERT in the rat intestine. Pharmacol. Res. 54:73–76.
  • Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., et al. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 122:107–118.
  • McCabe, L. R., Irwin, R., Schaefer, L., et al. (2013). Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J. Cell. Physiol. 228:1793–1798.
  • Moles, L., Gomez, M., Heilig, H., et al. (2013). Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One. 8:e66986.
  • Mosca, L. N., Goldberg, T. B., da Silva, V. N., et al. (2014). Excess body fat negatively affects bone mass in adolescents. Nutrition. 30:847–852.
  • Mutus, R., Kocabagli, N., Alp, M., et al. (2006). The effect of dietary probiotic supplementation on tibial bone characteristics and strength in broilers. Poult. Sci. 85:1621–1625.
  • Nadal, I., Donat, E., Ribes-Koninckx, C., et al. (2007). Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J. Med. Microbiol. 56:1669–1674.
  • Noor, S. O., Ridgway, K., Scovell, L., et al. (2010). Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol. 10:134.
  • Ohlsson, C., Engdahl, C., Fak, F., et al. (2014). Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One. 9:e92368.
  • Palmer, C., Bik, E. M., DiGiulio, D. B., et al. (2007). Development of the human infant intestinal microbiota. PLoS Biol. 5:e177.
  • Park, H. K., Shim, S. S., Kim, S. Y., et al. (2005). Molecular analysis of colonized bacteria in a human newborn infant gut. J. Microbiol. 43:345–3453.
  • Pineiro, M., Asp, N. G., Reid, G., et al. (2008). FAO Technical meeting on prebiotics. J. Clin. Gastroenterol. 42(Suppl 3 Pt 2):S156–S159.
  • Rawls, J. F., Mahowald, M. A., Ley, R. E., et al. (2006). Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 127:423–433.
  • Sadeghi, A. A. (2014). Bone mineralization of broiler chicks challenged with Salmonella enteritidis fed diet containing probiotic (Bacillus subtilis). Probiotics Antimicrob Proteins. 6:136–140.
  • Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31:107–133.
  • Sjogren, K., Engdahl, C., Henning, P., et al. (2012). The gut microbiota regulates bone mass in mice. J. Bone Miner. Res. 27:1357–1367.
  • Sokol, H., Pigneur, B., Watterlot, L., et al. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA. 105:16731–16736.
  • Taverniti, V. and Guglielmetti, S. (2011). The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: Proposal of paraprobiotic concept). Genes. Nutr. 6:261–274.
  • Tobias, J. H., Steer, C. D., Emmett, P. M., et al. (2005). Bone mass in childhood is related to maternal diet in pregnancy. Osteoporos. Int. 16:1731–1741.
  • Tsilingiri, K. and Rescigno, M. (2013). Postbiotics: What else? Benef. Microbes. 4:101–107.
  • Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., et al. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 444:1027–1031.
  • Turnbaugh, P. J., Backhed, F., Fulton, L., et al. (2008). Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host. Microbe. 3:213–223.
  • Turnbaugh, P. J., Hamady, M., Yatsunenko, T, et al. (2009). A core gut microbiome in obese and lean twins. Nature. 457:480–484.
  • Valles, Y., Artacho, A., Pascual-Garcia, A., et al. (2014). Microbial succession in the gut: Directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet. 10:e1004406.
  • van den Heuvel, E. G., Schoterman, M. H. and Muijs, T. (2000). Transgalactooligosaccharides stimulate calcium absorption in postmenopausal women. J. Nutr. 130:2938–2942.
  • Vestergaard, P., Krogh, K., Rejnmark, L., et al. (2000). Fracture risk is increased in Crohn's disease, but not in ulcerative colitis. Gut. 46:176–181.
  • Voth, D. E. and Ballard, J. D. (2005). Clostridium difficile toxins: Mechanism of action and role in disease. Clin. Microbiol. Rev. 18:247–263.
  • Vrieze, A., Holleman, F., Zoetendal, E. G., et al. (2010). The environment within: How gut microbiota may influence metabolism and body composition. Diabetologia. 53:606–613.
  • Wade, P. R., Chen, J., Jaffe, B., et al. (1996). Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. J. Neurosci. 16:2352–2364.
  • Walther, D. J., Peter, J. U., Bashammakh, S., et al. (2003). Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science. 299:76.
  • Wang, M., Ahrne, S., Antonsson, M., et al. (2004). T-RFLP combined with principal component analysis and 16S rRNA gene sequencing: An effective strategy for comparison of fecal microbiota in infants of different ages. J. Microbiol. Methods. 59:53–69.
  • Weaver, C. M., Martin, B. R., Nakatsu, C. H., et al. (2011). Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J. Agric. Food Chem. 59:6501–6510.
  • Wei, S., Kitaura, H., Zhou, P., et al. (2005). IL-1 mediates TNF-induced osteoclastogenesis. J. Clin. Invest. 115:282–290.
  • Whisner, C. M., Martin, B. R., Schoterman, M. H., et al. (2013). Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: A double-blind cross-over trial. Br. J. Nutr. 110:1292–1303.
  • WHO. (1994). Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. [No authors listed]. World Health Organ Tech Rep Ser. 843:1–129. PMID:7941614. Available at https://www.ncbi.nlm.nih.gov/pubmed/7941614
  • Xu, D. X., Chen, Y. H., Wang, H., et al. (2006). Tumor necrosis factor alpha partially contributes to lipopolysaccharide-induced intra-uterine fetal growth restriction and skeletal development retardation in mice. Toxicol. Lett. 163:20–29.
  • Xu, J. and Gordon, J. I. (2003). Honor thy symbionts. Proc. Natl. Acad. Sci. USA. 100:10452–10459.
  • Yadav, V. K., Ryu, J. H., Suda, N., et al. (2008). Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell. 135:825–837.
  • Yadav, V. K., Balaji, S., Suresh, P. S., et al. (2010). Pharmacological inhibition of gut-derived serotonin synthesis is a potential bone anabolic treatment for osteoporosis. Nat. Med. 16:308–312.
  • Yang, R. B., Mark, M. R., Gray, A., et al. (1998). Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature. 395:284–288.
  • Yarilina, A., Xu, K., Chen, J., et al. (2011). TNF activates calcium-nuclear factor of activated T cells (NFAT)c1 signaling pathways in human macrophages. Proc. Natl. Acad. Sci. USA. 108:1573–1578.
  • Yatsunenko, T., Rey, F. E., Manary, M. J., et al. (2012). Human gut microbiome viewed across age and geography. Nature. 486:222–227.
  • Yearsley, K. A., Gilby, L. J., Ramadas, A. V., et al. (2006). Proton pump inhibitor therapy is a risk factor for Clostridium difficile-associated diarrhoea. Aliment. Pharmacol. Ther. 24:613–619.
  • Yin, J., Dwyer, T., Riley, M., et al. (2010). The association between maternal diet during pregnancy and bone mass of the children at age 16. Eur. J. Clin. Nutr. 64:131–137.
  • Yoo, H. J., Park, M. S., Yang, S. J., et al. (2012). The differential relationship between fat mass and bone mineral density by gender and menopausal status. J. Bone Miner. Metab. 30:47–53.
  • Zhang, M., Qiu, X., Zhang, H., et al. (2014). Faecalibacterium prausnitzii inhibits interleukin-17 to ameliorate colorectal colitis in rats. PLoS One. 9:e109146.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.