Advertisement

Nutritional influence on bone: role of gut microbiota

  • René RizzoliEmail author
Review

Abstract

Gut microbiota (GM) located within the intestinal tract lumen comprises the largest number of cells (10E14) in the human body. The gut microbiome refers to the collection of genomes and genes present in gut microbiota. GM can vary according to age, sex, genetic background, immune status, geography, diet, prebiotics, which are non-digestible fibers metabolized in the distal part of the gastrointestinal tract, probiotics, which are micro-organisms conferring a health benefit on the host when administered in adequate amounts, living conditions, diseases and drugs. A source of probiotics is fortified fermented dairy products, which in addition provide calcium, protein, phosphorus and various micronutrients. Bone homeostasis is influenced by GM composition and/or products. GM appears to be a major player in the various determinants of bone health. However, it remains to be demonstrated in well conducted long-term randomized controlled trials, whether interventions changing GM composition and/or function are capable of reducing fracture risk.

Keywords

Intestinal calcium absorption Bone turnover Bone mineral density Osteoporosis Prebiotics Probiotics 

Notes

Compliance with ethical standards

Conflict of interest

RR has received fees for consultancy or lecture from Danone, EffRx, Nestlé, ObsEva, Pfizer, Radius Health, Sandoz and TEVA/Theramex.

Statement of human and animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of paper, formal consent is not required.

References

  1. 1.
    Consortium HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214CrossRefGoogle Scholar
  2. 2.
    Gordon JI (2012) Honor thy gut symbionts redux. Science 336:1251–1253CrossRefPubMedGoogle Scholar
  3. 3.
    Lucas S, Omata Y, Hofmann J et al (2018) Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss. Nat Commun 9:55CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Cani PD (2017) Gut cell metabolism shapes the microbiome. Science 357:548–549CrossRefPubMedGoogle Scholar
  5. 5.
    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:e1004406CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    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 87:280–290CrossRefPubMedGoogle Scholar
  7. 7.
    Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Lahti L, Salojarvi J, Salonen A et al (2014) Tipping elements in the human intestinal ecosystem. Nat Commun 5:4344CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Claesson MJ, Cusack S, O’Sullivan O et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108:4586–4591CrossRefPubMedGoogle Scholar
  10. 10.
    Claesson MJ, Jeffery IB, Conde S et al (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488:178–184CrossRefPubMedGoogle Scholar
  11. 11.
    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:e10667CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    David LA, Maurice CF, Carmody RN et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563CrossRefPubMedGoogle Scholar
  13. 13.
    Beaumont M, Portune KJ, Steuer N et al (2017) Quantity and source of dietary protein influence metabolite production by gut microbiota and rectal mucosa gene expression: a randomized, parallel, double-blind trial in overweight humans. Am J Clin Nutr 106:1005–1019CrossRefPubMedGoogle Scholar
  14. 14.
    Faith JJ, Guruge JL, Charbonneau M et al (2013) The long-term stability of the human gut microbiota. Science 341:1237439CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Devkota S (2016) MICROBIOME. Prescription drugs obscure microbiome analyses. Science 351:452–453CrossRefPubMedGoogle Scholar
  16. 16.
    Maier L, Pruteanu M, Kuhn M et al (2018) Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555:623–628CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Sekirov I, Russell SL, Antunes LC et al (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904CrossRefPubMedGoogle Scholar
  18. 18.
    Ticinesi A, Lauretani F, Milani C et al (2017) Aging gut microbiota at the cross-road between nutrition, physical frailty, and sarcopenia: is there a gut-muscle axis? Nutrients 9:1303.  https://doi.org/10.3390/nu9121303 CrossRefPubMedCentralGoogle Scholar
  19. 19.
    Grosicki GJ, Fielding RA, Lustgarten MS (2018) Gut microbiota contribute to age-related changes in skeletal muscle size, composition, and function: biological basis for a gut-muscle axis. Calcif Tissue Int 102:433–442CrossRefPubMedGoogle Scholar
  20. 20.
    Ticinesi A, Tana C, Nouvenne A (2019) The intestinal microbiome and its relevance for functionality in older persons. Curr Opin Clin Nutr Metab Care 22:4–12CrossRefPubMedGoogle Scholar
  21. 21.
    Rizzoli R (2018) Diet, microbiota, and bone health. In: Weaver CM, Bischoff-Ferrari H, Daly R, Wong MS (eds) Nutritional influences on bone health. Springer Nature, Cham, pp 143–168Google Scholar
  22. 22.
    Sjogren K, Engdahl C, Henning P et al (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Schwarzer M, Strigini M, Leulier F (2018) Gut microbiota and host juvenile growth. Calcif Tissue Int 102:387–405.  https://doi.org/10.1007/s00223-017-0368-y CrossRefPubMedGoogle Scholar
  24. 24.
    Yan J, Herzog JW, Tsang K et al (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci USA 113:E7554–E7563CrossRefPubMedGoogle Scholar
  25. 25.
    Fransen F, Zagato E, Mazzini E et al (2015) BALB/c and C57BL/6 mice differ in polyreactive IgA abundance, which impacts the generation of antigen-specific IgA and microbiota diversity. Immunity 43:527–540CrossRefPubMedGoogle Scholar
  26. 26.
    Weaver CM (2015) Diet, gut microbiome, and bone health. Curr Osteoporos Rep 13:125–130CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Druart C, Alligier M, Salazar N et al (2014) Modulation of the gut microbiota by nutrients with prebiotic and probiotic properties. Adv Nutr 5:624 s–633 sCrossRefGoogle Scholar
  28. 28.
    Denou E, Marcinko K, Surette MG et al (2016) High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity. Am J Physiol Endocrinol Metab 310:E982–E993CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Suez J, Korem T, Zeevi D et al (2014) Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514:181–186CrossRefPubMedGoogle Scholar
  30. 30.
    Mitsou EK, Kakali A, Antonopoulou S et al (2017) Adherence to the Mediterranean diet is associated with the gut microbiota pattern and gastrointestinal characteristics in an adult population. Br J Nutr 117:1645–1655CrossRefPubMedGoogle Scholar
  31. 31.
    De Filippis F, Pellegrini N, Vannini L et al (2016) High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut 65:1812–1821CrossRefPubMedGoogle Scholar
  32. 32.
    Tosti V, Bertozzi B, Fontana L (2018) Health benefits of the mediterranean diet: metabolic and molecular mechanisms. J Gerontol A Biol Sci Med Sci 73:318–326CrossRefPubMedGoogle Scholar
  33. 33.
    Byberg L, Bellavia A, Larsson SC et al (2016) Mediterranean diet and hip fracture in Swedish men and women. J Bone Miner Res 31:2098–2105CrossRefPubMedGoogle Scholar
  34. 34.
    Haring B, Crandall CJ, Wu C et al (2016) Dietary patterns and fractures in postmenopausal women: results from the women’s health initiative. JAMA Intern Med 176:645–652CrossRefPubMedGoogle Scholar
  35. 35.
    Smith MI, Yatsunenko T, Manary MJ et al (2013) Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339:548–554CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Blanton LV, Charbonneau MR, Salih T et al (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science.  https://doi.org/10.1126/science.aad3311 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Whisner CM, Castillo LF (2018) Prebiotics, bone and mineral metabolism. Calcif Tissue Int 102:443–479CrossRefPubMedGoogle Scholar
  38. 38.
    Garcia-Vieyra MI, Del Real A, Lopez MG (2014) Agave fructans: their effect on mineral absorption and bone mineral content. J Med Food 17:1247–1255CrossRefPubMedGoogle Scholar
  39. 39.
    Weaver CM, Martin BR, Nakatsu CH et al (2011) Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J Agric Food Chem 59:6501–6510CrossRefPubMedGoogle Scholar
  40. 40.
    Ammann P, Rizzoli R, Fleisch H (1988) Influence of the disaccharide lactitol on intestinal absorption and body retention of calcium in rats. J Nutr 118:793–795CrossRefPubMedGoogle Scholar
  41. 41.
    Lee C, Kim BG, Kim JH et al (2017) Sodium butyrate inhibits the NF-kappa B signaling pathway and histone deacetylation, and attenuates experimental colitis in an IL-10 independent manner. Int Immunopharmacol 51:47–56CrossRefPubMedGoogle Scholar
  42. 42.
    Langlands SJ, Hopkins MJ, Coleman N et al (2004) Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 53:1610–1616CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Bindels LB, Delzenne NM, Cani PD et al (2015) Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 12:303–310CrossRefPubMedGoogle Scholar
  44. 44.
    Macfarlane S, Macfarlane GT, Cummings JH (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24:701–714CrossRefPubMedGoogle Scholar
  45. 45.
    Scholz-Ahrens KE, Ade P, Marten B et al (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137:838 s–846 sCrossRefGoogle Scholar
  46. 46.
    Mitamura R, Hara H (2006) Ingestion of difructose anhydride III partially restores calcium absorption impaired by vitamin D and estrogen deficiency in rats. Eur J Nutr 45:242–249CrossRefPubMedGoogle Scholar
  47. 47.
    Ohta A, Uehara M, Sakai K et al (2002) A combination of dietary fructooligosaccharides and isoflavone conjugates increases femoral bone mineral density and equol production in ovariectomized mice. J Nutr 132:2048–2054CrossRefPubMedGoogle Scholar
  48. 48.
    Zafar TA, Weaver CM, Zhao Y et al (2004) Nondigestible oligosaccharides increase calcium absorption and suppress bone resorption in ovariectomized rats. J Nutr 134:399–402CrossRefPubMedGoogle Scholar
  49. 49.
    Ammann P, Rizzoli R, Fleisch H (1986) Calcium absorption in rat large intestine in vivo: availability of dietary calcium. Am J Physiol 251:G14–G18PubMedGoogle Scholar
  50. 50.
    Mathey J, Puel C, Kati-Coulibaly S et al (2004) Fructooligosaccharides maximize bone-sparing effects of soy isoflavone-enriched diet in the ovariectomized rat. Calcif Tissue Int 75:169–179CrossRefPubMedGoogle Scholar
  51. 51.
    Yang LC, Wu JB, Lu TJ et al (2013) The prebiotic effect of Anoectochilus formosanus and its consequences on bone health. Br J Nutr 109:1779–1788CrossRefPubMedGoogle Scholar
  52. 52.
    Muhlbauer RC, Li F (1999) Effect of vegetables on bone metabolism. Nature 401:343–344CrossRefPubMedGoogle Scholar
  53. 53.
    Muhlbauer RC, Lozano A, Reinli A (2002) Onion and a mixture of vegetables, salads, and herbs affect bone resorption in the rat by a mechanism independent of their base excess. J Bone Miner Res 17:1230–1236CrossRefPubMedGoogle Scholar
  54. 54.
    Chaplin A, Parra P, Laraichi S et al (2016) Calcium supplementation modulates gut microbiota in a prebiotic manner in dietary obese mice. Mol Nutr Food Res 60:468–480CrossRefPubMedGoogle Scholar
  55. 55.
    Charbonneau MR, O’Donnell D, Blanton LV et al (2016) Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164:859–871CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Sjogren YM, Tomicic S, Lundberg A et al (2009) Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy 39:1842–1851CrossRefPubMedGoogle Scholar
  57. 57.
    He Y, Liu S, Leone S et al (2014) Human colostrum oligosaccharides modulate major immunologic pathways of immature human intestine. Mucosal Immunol 7:1326–1339CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Peng L, Li ZR, Green RS et al (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139:1619–1625CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Rizzoli R, Bianchi ML, Garabedian M et al (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46:294–305CrossRefPubMedGoogle Scholar
  60. 60.
    Abrams SA, Griffin IJ, Hawthorne KM et al (2005) A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 82:471–476CrossRefPubMedGoogle Scholar
  61. 61.
    van den Heuvel EG, Muys T, van Dokkum W et al (1999) Oligofructose stimulates calcium absorption in adolescents. Am J Clin Nutr 69:544–548CrossRefPubMedGoogle Scholar
  62. 62.
    Whisner CM, Martin BR, Schoterman MH et al (2013) Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr 110:1292–1303CrossRefPubMedGoogle Scholar
  63. 63.
    Whisner CM, Martin BR, Nakatsu CH et al (2014) Soluble maize fibre affects short-term calcium absorption in adolescent boys and girls: a randomised controlled trial using dual stable isotopic tracers. Br J Nutr 112:446–456CrossRefPubMedGoogle Scholar
  64. 64.
    Slevin MM, Allsopp PJ, Magee PJ et al (2014) Supplementation with calcium and short-chain fructo-oligosaccharides affects markers of bone turnover but not bone mineral density in postmenopausal women. J Nutr 144:297–304CrossRefPubMedGoogle Scholar
  65. 65.
    Whisner CM, Martin BR, Nakatsu CH et al (2016) Soluble corn fiber increases calcium absorption associated with shifts in the gut microbiome: a randomized dose-response trial in free-living pubertal females. J Nutr 146:1298–1306CrossRefPubMedGoogle Scholar
  66. 66.
    McCabe LR, Parameswaran N (2018) Advances in probiotic regulation of bone and mineral metabolism. Calcif Tissue Int 102:480–488CrossRefPubMedGoogle Scholar
  67. 67.
    McCabe LR, 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 228:1793–1798CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Britton RA, Irwin R, Quach D et al (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Zhang J, Motyl KJ, Irwin R et al (2015) Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri. Endocrinology 156:3169–3182CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Ohlsson C, Engdahl C, Fak F et al (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9:e92368CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Chiang SS, Pan TM (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 59:7734–7742CrossRefPubMedGoogle Scholar
  72. 72.
    Narva M, Rissanen J, Halleen J et al (2007) Effects of bioactive peptide, valyl-prolyl-proline (VPP), and lactobacillus helveticus fermented milk containing VPP on bone loss in ovariectomized rats. Ann Nutr Metab 51:65–74CrossRefPubMedGoogle Scholar
  73. 73.
    Parvaneh K, Ebrahimi M, Sabran MR et al (2015) Probiotics (Bifidobacterium longum) increase bone mass density and upregulate sparc and Bmp-2 genes in rats with bone loss resulting from ovariectomy. Biomed Res Int 2015:897639CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Li JY, Chassaing B, Tyagi AM et al (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Investig 126:2049–2063CrossRefPubMedGoogle Scholar
  75. 75.
    Rizzoli R, Biver E (2018) Effects of fermented milk products on bone. Calcif Tissue Int 102:489–500CrossRefPubMedGoogle Scholar
  76. 76.
    Alvaro E, Andrieux C, Rochet V et al (2007) Composition and metabolism of the intestinal microbiota in consumers and non-consumers of yogurt. Br J Nutr 97:126–133CrossRefPubMedGoogle Scholar
  77. 77.
    Sahni S, Tucker KL, Kiel DP et al (2013) Milk and yogurt consumption are linked with higher bone mineral density but not with hip fracture: the Framingham Offspring Study. Arch Osteoporos 8:119CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Biver E, Durosier-Izart C, Merminod F et al (2018) Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein, and energy intakes in healthy postmenopausal women. Osteoporos Int 29:1771–1782CrossRefPubMedGoogle Scholar
  79. 79.
    Laird E, Molloy AM, McNulty H et al (2017) Greater yogurt consumption is associated with increased bone mineral density and physical function in older adults. Osteoporos Int 28:2409–2419CrossRefPubMedGoogle Scholar
  80. 80.
    Michaelsson K, Wolk A, Lemming EW et al (2018) Intake of milk or fermented milk combined with fruit and vegetable consumption in relation to hip fracture rates: a cohort study of Swedish women. J Bone Miner Res 33:449–457CrossRefPubMedGoogle Scholar
  81. 81.
    Michaëlsson K, Wolk A, Langenskiöld S et al (2014) Milk intake and risk of mortality and fractures in women and men: cohort studies. BMJ 349:g6015CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Radavelli-Bagatini S, Zhu K et al (2014) Dairy food intake, peripheral bone structure, and muscle mass in elderly ambulatory women. J Bone Miner Res 29:1691–1700CrossRefPubMedGoogle Scholar
  83. 83.
    Rizzoli R, Biver E, Bonjour JP et al (2018) Benefits and safety of dietary protein for bone health-an expert consensus paper endorsed by the European Society for Clinical and Economical Aspects of Osteoporosis, Osteoarthritis, and Musculoskeletal Diseases and by the International Osteoporosis Foundation. Osteoporos Int 29:1933–1948.  https://doi.org/10.1007/s00198-018-4534-5 CrossRefGoogle Scholar
  84. 84.
    Jones ML, Martoni CJ, Prakash S (2013) Oral supplementation with probiotic L. reuteri NCIMB 30242 increases mean circulating 25-hydroxyvitamin D: a post hoc analysis of a randomized controlled trial. J Clin Endocrinol Metab 98:2944–2951CrossRefPubMedGoogle Scholar
  85. 85.
    Nilsson AG, Sundh D, Backhed F et al (2018) Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial. J Intern Med.  https://doi.org/10.1111/joim.12805 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    McNulty NP, Yatsunenko T, Hsiao A et al (2011) The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 3:106ra106CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Waterhouse M, Hope B, Krause L et al (2018) Vitamin D and the gut microbiome: a systematic review of in vivo studies. Eur J Nutr.  https://doi.org/10.1007/s00394-018-1842-7 CrossRefPubMedGoogle Scholar
  88. 88.
    Kong J, Zhang Z, Musch MW et al (2008) Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier. Am J Physiol Gastrointest Liver Physiol 294:G208–G216CrossRefPubMedGoogle Scholar
  89. 89.
    Jin D, Wu S, Zhang YG et al (2015) Lack of vitamin D receptor causes dysbiosis and changes the functions of the murine intestinal microbiome. Clin Ther 37:996–1009.e1007CrossRefPubMedGoogle Scholar
  90. 90.
    Luthold RV, Fernandes GR, Franco-de-Moraes AC et al (2017) Gut microbiota interactions with the immunomodulatory role of vitamin D in normal individuals. Metabolism 69:76–86CrossRefPubMedGoogle Scholar
  91. 91.
    Wu S, Yoon S, Zhang YG et al (2015) Vitamin D receptor pathway is required for probiotic protection in colitis. Am J Physiol Gastrointest Liver Physiol 309:G341–G349CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Bashir M, Prietl B, Tauschmann M et al (2016) Effects of high doses of vitamin D3 on mucosa-associated gut microbiome vary between regions of the human gastrointestinal tract. Eur J Nutr 55:1479–1489CrossRefPubMedGoogle Scholar
  93. 93.
    Collins FL, Schepper JD, Rios-Arce ND et al (2017) Immunology of gut-bone signaling. Adv Exp Med Biol 1033:59–94CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Mineo H, Amano M, Minaminida K et al (2006) Two-week feeding of difructose anhydride III enhances calcium absorptive activity with epithelial cell proliferation in isolated rat cecal mucosa. Nutrition 22:312–320CrossRefPubMedGoogle Scholar
  95. 95.
    Donohoe DR, Garge N, Zhang X et al (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13:517–526CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Ma N, Guo P, Zhang J et al (2018) Nutrients mediate intestinal bacteria-mucosal immune crosstalk. Front Immunol 9:5CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Beaumont M, Andriamihaja M, Armand L et al (2017) Epithelial response to a high-protein diet in rat colon. BMC Genom 18:116CrossRefGoogle Scholar
  98. 98.
    Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485CrossRefPubMedGoogle Scholar
  99. 99.
    Ammann P, Rizzoli R, Bonjour JP et al (1997) Transgenic mice expressing soluble tumor necrosis factor-receptor are protected against bone loss caused by estrogen deficiency. J Clin Investig 99:1699–1703CrossRefPubMedGoogle Scholar
  100. 100.
    Terashima A, Takayanagi H (2018) Overview of osteoimmunology. Calcif Tissue Int 102:503–511.  https://doi.org/10.1007/s00223-018-0417-1 CrossRefPubMedGoogle Scholar
  101. 101.
    Li JY, Tawfeek H, Bedi B et al (2011) Ovariectomy disregulates osteoblast and osteoclast formation through the T-cell receptor CD40 ligand. Proc Natl Acad Sci USA 108:768–773CrossRefPubMedGoogle Scholar
  102. 102.
    Lee HW, Suh JH, Kim AY et al (2006) Histone deacetylase 1-mediated histone modification regulates osteoblast differentiation. Mol Endocrinol 20:2432–2443CrossRefPubMedGoogle Scholar
  103. 103.
    Katono T, Kawato T, Tanabe N et al (2008) Sodium butyrate stimulates mineralized nodule formation and osteoprotegerin expression by human osteoblasts. Arch Oral Biol 53:903–909CrossRefPubMedGoogle Scholar
  104. 104.
    Albenberg LG, Wu GD (2014) Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 146:1564–1572CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Rowland I, Gibson G, Heinken A et al (2018) Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr 57:1–24CrossRefPubMedGoogle Scholar
  106. 106.
    Rizzoli R, Bonjour JP (2006) Physiology of calcium and phosphate homeostasis. In: Seibel MJ, Robins SP, Bilezikian JP (eds) Dynamics of bone and cartilage metabolism: principles and clinical applications. Academic Press, San Diego, pp 345–360CrossRefGoogle Scholar
  107. 107.
    Yadav VK, Ryu JH, Suda N et al (2008) Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135:825–837CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Service of Bone DiseasesGeneva University Hospitals and Faculty of MedicineGeneva 14Switzerland

Personalised recommendations