25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation.
Bone remodeling; HS; Inflammation; Intestinal barrier; Tibial mass
Abstract :
[en] BACKGROUND: Alterations in ambient temperature have been associated with multiple detrimental effects on broilers such as intestinal barrier disruption and dysbiosis resulting in systemic inflammation. Inflammation and 25-hydroxycholecalciferol (25-OH-D(3)) have shown to play a negative and positive role, respectively, in the regulation of bone mass. Hence the potential of 25-OH-D(3) in alleviating heat induced bone alterations and its mechanisms was studied. RESULTS: Heat stress (HS) directly induced a decrease in tibia material properties and bone mass, as demonstrated by lower mineral content, and HS caused a notable increase in intestinal permeability. Treatment with dietary 25-OH-D(3) reversed the HS-induced bone loss and barrier leak. Broilers suffering from HS exhibited dysbiosis and increased expression of inflammatory cytokines in the ileum and bone marrow, as well as increased osteoclast number and activity. The changes were prevented by dietary 25-OH-D(3) administration. Specifically, dietary 25-OH-D(3) addition decreased abundance of B- and T-cells in blood, and the expression of inflammatory cytokines, especially TNF-α, in both the ileum and bone marrow, but did not alter the diversity and population or composition of major bacterial phyla. With regard to bone remodeling, dietary 25-OH-D(3) supplementation was linked to a decrease in serum C-terminal cross-linked telopeptide of type I collagen reflecting bone resorption and a concomitant decrement in osteoclast-specific marker genes expression (e.g. cathepsin K), whereas it did not apparently change serum bone formation markers during HS. CONCLUSIONS: These data underscore the damage of HS to intestinal integrity and bone health, as well as that dietary 25-OH-D(3) supplementation was identified as a potential therapy for preventing these adverse effects.
Disciplines :
Food science
Author, co-author :
Zhang, Huaiyong
Majdeddin, Maryam
Gaublomme, Djoere
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Boone, Matthieu
Elewaut, Dirk
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Josipovic, Iván
Zhang, Keying
Michiels, Joris
Language :
English
Title :
25-hydroxycholecalciferol reverses heat induced alterations in bone quality in finisher broilers associated with effects on intestinal integrity and inflammation.
Deeb N, Cahaner A. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci. 2002;81(3):293–301. 10.1093/ps/81.3.293. DOI: 10.1093/ps/81.3.293
Hosseini-Vashan SJ, Golian A, Yaghobfar A. Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers fed diets supplemented with tomato pomace. Int J Biometeorol. 2016;60(8):1183–92. 10.1007/s00484-015-1112-9. DOI: 10.1007/s00484-015-1112-9
Yan FF, Mohammed AA, Murugesan GR, Cheng HW. Effects of a dietary synbiotic inclusion on bone health in broilers subjected to cyclic heat stress episodes. Poult Sci. 2019;98(3):1083–9. 10.3382/ps/pey508. DOI: 10.3382/ps/pey508
Koelkebeck KW, Harrison PC, Madindou T. effect of carbonated drinking water on production performance and bone characteristics of laying hens exposed to high environmental temperatures. Poult Sci. 1993;72(9):1800–3. https://doi.org/10.3382/ps.0721800.
Jankowski J, Mikulski D, Tatara MR, Krupski W. Effects of increased stocking density and heat stress on growth, performance, carcase characteristics and skeletal properties in turkeys. Vet Rec. 2015;176(1):21. 10.1136/vr.102216. DOI: 10.1136/vr.102216
Rath NC, Huff GR, Huff WE, Balog JM. Factors regulating bone maturity and strength in poultry. Poult Sci. 2000;79(7):1024–32. 10.1093/ps/79.7.1024. DOI: 10.1093/ps/79.7.1024
Reiter K, Bessei W. Effect of locomotor activity on leg disorder in fattening chicken. Berliner und Munchener tierarztliche Wochenschrift. 2009;122(7–8):264–70.
Wiernusz CJ, Teeter RG. Acclimation effects on fed and fasted broiler thermobalance during thermoneutral and high ambient temperature exposure. Br Poult Sci. 1996;37(3):677–87. 10.1080/00071669608417897. DOI: 10.1080/00071669608417897
D'Amelio P, Sassi F. Gut microbiota, immune system, and bone. Calcif Tissue Int. 2018;102(4):415–25. 10.1007/s00223-017-0331-y. DOI: 10.1007/s00223-017-0331-y
Koch F, Thom U, Albrecht E, Weikard R, Nolte W, Kuhla B, et al. Heat stress directly impairs gut integrity and recruits distinct immune cell populations into the bovine intestine. Proc Natl Acad Sci U S A. 2019;116(21):10333–8. 10.1073/pnas.1820130116. DOI: 10.1073/pnas.1820130116
Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol. 2001;280(2):H509–21. 10.1152/ajpheart.2001.280.2.H509. DOI: 10.1152/ajpheart.2001.280.2.H509
Zhu L, Liao R, Wu N, Zhu G, Yang C. Heat stress mediates changes in fecal microbiome and functional pathways of laying hens. Appl Microbiol Biotechnol. 2019;103(1):461–72. 10.1007/s00253-018-9465-8. DOI: 10.1007/s00253-018-9465-8
Shi D, Bai L, Qu Q, Zhou S, Yang M, Guo S, et al. Impact of gut microbiota sturcture in heat-stressed broilers. Poult Sci. 2019;98(6):2405–13. 10.3382/ps/pez026. DOI: 10.3382/ps/pez026
Wang XJ, Feng JH, Zhang MH, Li XM, Ma DD, Chang SS. Effects of high ambient temperature on the community structure and composition of ileal microbiome of broilers. Poult Sci. 2018;97(6):2153–8. 10.3382/ps/pey032. DOI: 10.3382/ps/pey032
Chen YC, Greenbaum J, Shen H, Deng HW. Association between gut microbiota and bone health: potential mechanisms and prospective. J Clin Endocrinol Metab. 2017;102(10):3635–46. 10.1210/jc.2017-00513. DOI: 10.1210/jc.2017-00513
Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science. 2016;351(6275):854–7. 10.1126/science.aad8588. DOI: 10.1126/science.aad8588
Yan J, Charles JF. Gut microbiome and bone: to build, destroy, or both? Curr Osteoporos Rep. 2017;15(4):376–84. 10.1007/s11914-017-0382-z. DOI: 10.1007/s11914-017-0382-z
Ohlsson C, Nigro G, Boneca IG, Backhed F, Sansonetti P, Sjogren K. Regulation of bone mass by the gut microbiota is dependent on NOD1 and NOD2 signaling. Cell Immunol. 2017;317:55–8. 10.1016/j.cellimm.2017.05.003. DOI: 10.1016/j.cellimm.2017.05.003
Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, et al. The gut microbiota regulates bone mass in mice. J Bone Miner Res. 2012;27(6):1357–67. 10.1002/jbmr.1588. DOI: 10.1002/jbmr.1588
Henneicke H, Gasparini SJ, Brennan-Speranza TC, Zhou H, Seibel MJ. Glucocorticoids and bone: local effects and systemic implications. Trends Endocrinol Metab. 2014;25(4):197–211. 10.1016/j.tem.2013.12.006. DOI: 10.1016/j.tem.2013.12.006
Wauquier F, Leotoing L, Coxam V, Guicheux J, Wittrant Y. Oxidative stress in bone remodelling and disease. Trends Mol Med. 2009;15(10):468–77. 10.1016/j.molmed.2009.08.004. DOI: 10.1016/j.molmed.2009.08.004
Sun ZW, Yan L, G YY, Zhao JP, Lin H, Guo YM. Increasing dietary vitamin D3 improves the walking ability and welfare status of broiler chickens reared at high stocking densities. Poult Sci. 2013;92(12):3071–9. 10.3382/ps.2013-03278.
Jiang S, Jiang Z, Yang K, Chen F, Zheng C, Wang L. Dietary vitamin D3 requirement of Chinese yellow-feathered broilers. Poult Sci. 2015;94(9):2210–20. 10.3382/ps/pev163. DOI: 10.3382/ps/pev163
Khan SH, Shahid R, Mian AA, Sardar R, Anjum MA. Effect of the level of cholecalciferol supplementation of broiler diets on the performance and tibial dyschondroplasia. J Anim Physiol Anim Nutr (Berl). 2010;94(5):584–93. 10.1111/j.1439-0396.2009.00943.x. DOI: 10.1111/j.1439-0396.2009.00943.x
Christakos S, Dhawan P, Porta A, Mady LJ, Seth T. Vitamin D and intestinal calcium absorption. Mol Cell Endocrinol. 2011;347(1–2):25–9. DOI: 10.1016/j.mce.2011.05.038
Nakamichi Y, Udagawa N, Suda T, Takahashi N. Mechanisms involved in bone resorption regulated by vitamin D. J Steroid Biochem Mol Biol. 2018;177:70–6. 10.1016/j.jsbmb.2017.11.005. DOI: 10.1016/j.jsbmb.2017.11.005
van Driel M, van Leeuwen J. Vitamin D endocrinology of bone mineralization. Mol Cell Endocrinol. 2017;453:46–51. 10.1016/j.mce.2017.06.008. DOI: 10.1016/j.mce.2017.06.008
Waterhouse M, Hope B, Krause L, Morrison M, Protani MM, Zakrzewski M, et al. Vitamin D and the gut microbiome: a systematic review of in vivo studies. Eur J Nutr. 2018;58(7):2895–910. DOI: 10.1007/s00394-018-1842-7
Sepidarkish M, Farsi F, Akbari-Fakhrabadi M, Namazi N, Almasi-Hashiani A, Maleki Hagiagha A, et al. The effect of vitamin D supplementation on oxidative stress parameters: a systematic review and meta-analysis of clinical trials. Pharmacol Res. 2019;139:141–52. 10.1016/j.phrs.2018.11.011. DOI: 10.1016/j.phrs.2018.11.011
Domazetovic V, Marcucci G, Iantomasi T, Brandi ML, Vincenzini MT. Oxidative stress in bone remodeling: role of antioxidants. Clin Cases Miner Bone Metab. 2017;14(2):209–16. 10.11138/ccmbm/2017.14.1.209. DOI: 10.11138/ccmbm/2017.14.1.209
Lee C, Lau E, Chusilp S, Filler R, Li B, Zhu H, et al. Protective effects of vitamin D against injury in intestinal epithelium. Pediatr Surg Int. 2019;35(12):1395–401. 10.1007/s00383-019-04586-y. DOI: 10.1007/s00383-019-04586-y
Dong S, Singh TP, Wei X, Yao H, Wang H. Protective effect of 1,25-dihydroxy vitamin D3 on pepsin-trypsin-resistant gliadin-induced tight junction injuries. Dig Dis Sci. 2018;63(1):92–104. 10.1007/s10620-017-4738-0. DOI: 10.1007/s10620-017-4738-0
Guo C, Gombart AF. The antibiotic effects of vitamin D. Endocr Metab Immune Disord Drug Targets. 2014;14(4):255–66. 10.2174/1871530314666140709085159. DOI: 10.2174/1871530314666140709085159
Jain SK, Micinski D. Vitamin D upregulates glutamate cysteine ligase and glutathione reductase, and GSH formation, and decreases ROS and MCP-1 and IL-8 secretion in high-glucose exposed U937 monocytes. Biochem Biophys Res Commun. 2013;437(1):7–11. 10.1016/j.bbrc.2013.06.004. DOI: 10.1016/j.bbrc.2013.06.004
Han JC, Chen GH, Wang JG, Zhang JL, Qu HX, Zhang CM, et al. Evaluation of relative bioavailability of 25-hydroxycholecalciferol to cholecalciferol for broiler chickens. Asian-Australas J Anim Sci. 2016;29(8):1145–51. 10.5713/ajas.15.0553. DOI: 10.5713/ajas.15.0553
Spranghers T, Michiels J, Vrancx J, Ovyn A, Eeckhout M, De Clercq P, et al. Gut antimicrobial effects and nutritional value of black soldier fly (Hermetia illucens L.) prepupae for weaned piglets. Anim Feed Sci Tech. 2018;235:33–42. DOI: 10.1016/j.anifeedsci.2017.08.012
Majdeddin M, Braun U, Lemme A, Golian A, Kermanshahi H, De Smet S, et al. Guanidinoacetic acid supplementation improves feed conversion in broilers subjected to heat stress associated with muscle creatine loading and arginine sparing. Poult Sci. 2020;99(9):4442–53. 10.1016/j.psj.2020.05.023. DOI: 10.1016/j.psj.2020.05.023
Knowles TG, Kestin SC, Haslam SM, Brown SN, Green LE, Butterworth A, et al. Leg disorders in broiler chickens: prevalence, risk factors and prevention. PLoS One. 2008;3(2):e1545. 10.1371/journal.pone.0001545. DOI: 10.1371/journal.pone.0001545
Baxter MFA, Merino-Guzman R, Latorre JD, Mahaffey BD, Yang Y, Teague KD, et al. Optimizing fluorescein isothiocyanate dextran measurement as a biomarker in a 24-h feed restriction model to induce gut permeability in broiler chickens. Front Vet Sci. 2017;4:56. 10.3389/fvets.2017.00056. DOI: 10.3389/fvets.2017.00056
Seliger C, Schaerer B, Kohn M, Pendl H, Weigend S, Kaspers B, et al. A rapid high-precision flow cytometry based technique for total white blood cell counting in chickens. Vet Immunol Immunopathol. 2012;145(1–2):86–99. DOI: 10.1016/j.vetimm.2011.10.010
Turner CH. Bone strength: current concepts. Ann N Y Acad Sci. 2006;1068(1):429–46. 10.1196/annals.1346.039. DOI: 10.1196/annals.1346.039
Masschaele B, Dierick M, Loo DV, Boone MN, Brabant L, Pauwels E, et al. HECTOR: a 240kV micro-CT setup optimized for research. J Phys Conf Ser. 2013;463:012012. 10.1088/1742-6596/463/1/012012. DOI: 10.1088/1742-6596/463/1/012012
Vlassenbroeck J, Dierick M, Masschaele B, Cnudde V, Van Hoorebeke L, Jacobs P. Software tools for quantification of X-ray microtomography at the UGCT. Nuclear Instruments Methods Phys Res Sec A. 2007;580(1):442–5. 10.1016/j.nima.2007.05.073. DOI: 10.1016/j.nima.2007.05.073
Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone. 2007;41(4):505–15. 10.1016/j.bone.2007.07.007. DOI: 10.1016/j.bone.2007.07.007
Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone. 2010;47(6):1076–9. 10.1016/j.bone.2010.08.023. DOI: 10.1016/j.bone.2010.08.023
van Nevel CJ, Decuypere JA, Dierick N, Molly K. The influence of Lentinus edodes (shiitake mushroom) preparations on bacteriological and morphological aspects of the small intestine in piglets. Archiv fur Tierernahrung. 2003;57(6):399–412. 10.1080/0003942032000161054. DOI: 10.1080/0003942032000161054
Grotto D, Santa Maria LD, Boeira S, Valentini J, Charão MF, Moro AM, et al. Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography-visible detection. J Pharm Biomed Anal. 2007;43(2):619–24. 10.1016/j.jpba.2006.07.030. DOI: 10.1016/j.jpba.2006.07.030
Hernández P, Zomeño L, Ariño B, Blasco A. Antioxidant, lipolytic and proteolytic enzyme activities in pork meat from different genotypes. Meat Sci. 2004;66(3):525–9. 10.1016/S0309-1740(03)00155-4. DOI: 10.1016/S0309-1740(03)00155-4
Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974;47(3):469–74. 10.1111/j.1432-1033.1974.tb03714.x. DOI: 10.1111/j.1432-1033.1974.tb03714.x
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41. 10.1128/AEM.01541-09. DOI: 10.1128/AEM.01541-09
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. 10.7717/peerj.2584. DOI: 10.7717/peerj.2584
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database issue):D590–6. 10.1093/nar/gks1219. DOI: 10.1093/nar/gks1219
Castro-Montoya J, De Campeneere S, Van Ranst G, Fievez V. Interactions between methane mitigation additives and basal substrates on in vitro methane and VFA production. Anim Feed Sci Tech. 2012;176(1–4):47–60. DOI: 10.1016/j.anifeedsci.2012.07.007
Quinteiro-Filho WM, Rodrigues MV, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sá LR, et al. Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation. J Anim Sci. 2012;90(6):1986–94. 10.2527/jas.2011-3949. DOI: 10.2527/jas.2011-3949
Lara LJ, Rostagno MH. Impact of heat stree on poultry production. Animals. 2013;3(2):356–69. 10.3390/ani3020356. DOI: 10.3390/ani3020356
Ruff J, Barros TL, Tellez G Jr, Blankenship J, Lester H, Graham BD, et al. Research note: evaluation of a heat stress model to induce gastrointestinal leakage in broiler chickens. Poult Sci. 2020;99(3):1687–92. 10.1016/j.psj.2019.10.075. DOI: 10.1016/j.psj.2019.10.075
Bruno LD, Furlan RL, Malheiros EB, Macari M. Influence of early quantitative food restriction on long bone growth at different environmental temperatures in broiler chickens. Br Poult Sci. 2000;41(4):389–94. 10.1080/713654955. DOI: 10.1080/713654955
Sharir A, Barak MM, Shahar R. Whole bone mechanics and mechanical testing. Vet J. 2008;177(1):8–17. 10.1016/j.tvjl.2007.09.012. DOI: 10.1016/j.tvjl.2007.09.012
Sahin K, Onderci M, Sahin N, Balci TA, Gursu MF, Juturu V, et al. Dietary arginine silicate inositol complex improves bone mineralization in quail. Poult Sci. 2006;85(3):486–92. 10.1093/ps/85.3.486. DOI: 10.1093/ps/85.3.486
Sahin N, Balci TA, Kucuk O, Smith MO, Sahin K. Effects of 25-hydroxycholecalciferol and soy isoflavones supplementation on bone mineralisation of quail. Br Poult Sci. 2009;50(6):709–15. 10.1080/00071660903261944. DOI: 10.1080/00071660903261944
Santiago M, David S, Alexandra N, Eduardo A, Jimmy Q. Effect of 25-hydroxycholecalciferol (25-OH-D3) on productive performance and bone mineralization in broiler. J Anim Sci. 2016;6(3):180–4.
Wideman RF Jr, Blankenship J, Pevzner IY, Turner BJ. Efficacy of 25-OH vitamin D3 prophylactic administration for reducing lameness in broilers grown on wire flooring. Poult Sci. 2015;94(8):1821–7. 10.3382/ps/pev160. DOI: 10.3382/ps/pev160
Zhang HY, Zeng QF, Bai SP, Wang JP, Ding XM, Xuan Y, et al. Effect of dietary 25-hydroxycholecalciferol on the sternal mass of meat ducks under different vitamin regimens. Poult Sci. 2020;99(3):1241–53. 10.1016/j.psj.2019.10.068. DOI: 10.1016/j.psj.2019.10.068
Cardoso EF, Donzele JL, de Oliveira Donzele RFM, Sufiate BL, Silva AD, Tizziani T. Non-phytate phosphorus requirement for broilers from 8 to 21 days of age under heat stress conditions. Trop Anim Health Prod. 2018;50(2):317–25. 10.1007/s11250-017-1434-1. DOI: 10.1007/s11250-017-1434-1
Kamiya Y, Kamiya M, Tanaka M. The effect of high ambient temperature on ca, P and mg balance and bone turnover in high-yielding dairy cows. Anim Sci J. 2010;81(4):482–6. 10.1111/j.1740-0929.2010.00761.x. DOI: 10.1111/j.1740-0929.2010.00761.x
Wagner D, Hanwell HE, Schnabl K, Yazdanpanah M, Kimball S, Fu L, et al. The ratio of serum 24,25-dihydroxyvitamin D (3) to 25-hydroxyvitamin D (3) is predictive of 25-hydroxyvitamin D (3) response to vitamin D (3) supplementation. J Steroid Biochem Mol Biol. 2011;126(3–5):72–7. DOI: 10.1016/j.jsbmb.2011.05.003
Murer H, Forster I, Biber J. The sodium phosphate cotransporter family SLC34. Pflugers Arch. 2004;447(5):763–7. 10.1007/s00424-003-1072-5. DOI: 10.1007/s00424-003-1072-5
Han JC, Wang JG, Chen GH, Zhang JL, Zhang N, Qu HX, et al. 1alpha-hydroxycholecalciferol improves the growth performance and up-regulates the mRNA expression of vitamin D receptor in the small intestine and kidney of broiler chickens. Poult Sci. 2018;97(4):1263–70. 10.3382/ps/pex423. DOI: 10.3382/ps/pex423
Liu L, Fu C, Yan M, Xie H, Li S, Yu Q, et al. Resveratrol modulates intestinal morphology and HSP70/90, NF-kappaB and EGF expression in the jejunal mucosa of black-boned chickens on exposure to circular heat stress. Food Funct. 2016;7(3):1329–38. 10.1039/C5FO01338K. DOI: 10.1039/C5FO01338K
Zhao Y, Yu B, Mao X, He J, Huang Z, Zheng P, et al. Dietary vitamin D supplementation attenuates immune responses of pigs challenged with rotavirus potentially through the retinoic acid-inducible gene I signalling pathway. Br J Nutr. 2014;112(3):381–9. 10.1017/S000711451400097X. DOI: 10.1017/S000711451400097X
Walters JR. Cell and molecular biology of the small intestine: new insights into differentiation, growth and repair. Curr Opin Gastroenterol. 2004;20(2):70–6. 10.1097/00001574-200403000-00004. DOI: 10.1097/00001574-200403000-00004
Zhang C, Zhao XH, Yang L, Chen XY, Jiang RS, Jin SH, et al. Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poult Sci. 2017;96(12):4325–32. 10.3382/ps/pex266. DOI: 10.3382/ps/pex266
Irwin R, Raehtz S, Parameswaran N, McCabe LR. Intestinal inflammation without weight loss decreases bone density and growth. Am J Physiol Regul Integr Comp Physiol. 2016;311(6):R1149–57. 10.1152/ajpregu.00051.2016. DOI: 10.1152/ajpregu.00051.2016
Xing S, Wang X, Diao H, Zhang M, Zhou Y, Feng J. Changes in the cecal microbiota of laying hens during heat stress is mainly associated with reduced feed intake. Poult Sci. 2019;98(11):5257–64. 10.3382/ps/pez440. DOI: 10.3382/ps/pez440
Stanley D, Geier MS, Denman SE, Haring VR, Crowley TM, Hughes RJ, et al. Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Vet Microbiol. 2013;164(1–2):85–92. DOI: 10.1016/j.vetmic.2013.01.030
Schirmer M, Franzosa EA, Lloyd-Price J, McIver LJ, Schwager R, Poon TW, et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol. 2018;3(3):337–46. 10.1038/s41564-017-0089-z. DOI: 10.1038/s41564-017-0089-z
Schepper JD, Collins FL, Rios-Arce ND, Raehtz S, Schaefer L, Gardinier JD, et al. Probiotic lactobacillus reuteri prevents postantibiotic bone loss by reducing intestinal dysbiosis and preventing barrier disruption. J Bone Miner Res. 2019;34(4):681–98. 10.1002/jbmr.3635. DOI: 10.1002/jbmr.3635
Zaiss MM, Jones RM, Schett G, Pacifici R. The gut-bone axis: how bacterial metabolites bridge the distance. J Clin Invest. 2019;129(8):3018–28. 10.1172/JCI128521. DOI: 10.1172/JCI128521
Lucas S, Omata Y, Hofmann J, Böttcher M, Iljazovic A, Sarter K, et al. Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss. Nat Commun. 2018;9(1):55. 10.1038/s41467-017-02490-4. DOI: 10.1038/s41467-017-02490-4
Yan J, Takakura A, Zandi-Nejad K, Charles JF. Mechanisms of gut microbiota-mediated bone remodeling. Gut Microbes. 2018;9(1):84–92. 10.1080/19490976.2017.1371893. DOI: 10.1080/19490976.2017.1371893
Horowitz MC. Cytokines and estrogen in bone: anti-osteoporotic effects. Science. 1993;260(5108):626–7. 10.1126/science.8480174. DOI: 10.1126/science.8480174
Sato K, Takayanagi H. Osteoclasts, rheumatoid arthritis, and osteoimmunology. Curr Opin Rheumatol. 2006;18(4):419–26. 10.1097/01.bor.0000231912.24740.a5. DOI: 10.1097/01.bor.0000231912.24740.a5
Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000;106(12):1481–8. 10.1172/JCI11176. DOI: 10.1172/JCI11176
Li P, Schwarz EM, O'Keefe RJ, Ma L, Looney RJ, Ritchlin CT, et al. Systemic tumor necrosis factor alpha mediates an increase in peripheral CD11b high osteoclast precursors in tumor necrosis factor alpha-transgenic mice. Arthritis Rheum. 2004;50(1):265–76. 10.1002/art.11419. DOI: 10.1002/art.11419
Poli V, Balena R, Fattori E, Markatos A, Yamamoto M, Tanaka H, et al. Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. EMBO J. 1994;13(5):1189–96. 10.1002/j.1460-2075.1994.tb06368.x. DOI: 10.1002/j.1460-2075.1994.tb06368.x
Fujisaki K, Tanabe N, Suzuki N, Kawato T, Takeichi O, Tsuzukibashi O, et al. Receptor activator of NF-kappaB ligand induces the expression of carbonic anhydrase II, cathepsin K, and matrix metalloproteinase-9 in osteoclast precursor RAW264.7 cells. Life Sci. 2007;80(14):1311–8. 10.1016/j.lfs.2006.12.037. DOI: 10.1016/j.lfs.2006.12.037
Yamamoto Y, Udagawa N, Matsuura S, Nakamichi Y, Horiuchi H, Hosoya A, et al. Osteoblasts provide a suitable microenvironment for the action of receptor activator of nuclear factor-kappaB ligand. Endocrinology. 2006;147(7):3366–74. 10.1210/en.2006-0216. DOI: 10.1210/en.2006-0216
Guss JD, Horsfield MW, Fontenele FF, Sandoval TN, Luna M, Apoorva F, et al. Alterations to the gut microbiome impair bone strength and tissue material properties. J Bone Miner Res. 2017;32(6):1343–53. 10.1002/jbmr.3114. DOI: 10.1002/jbmr.3114
Nakamichi Y, Udagawa N, Horibe K, Mizoguchi T, Yamamoto Y, Nakamura T, et al. VDR in osteoblast-lineage cells primarily mediates vitamin D treatment-induced increase in bone mass by suppressing bone resorption. J Bone Miner Res. 2017;32(6):1297–308. 10.1002/jbmr.3096. DOI: 10.1002/jbmr.3096
Turner AG, Hanrath MA, Morris HA, Atkins GJ, Anderson PH. The local production of 1,25(OH)2D3 promotes osteoblast and osteocyte maturation. J Steroid Biochem Mol Biol. 2014;144(Pt A):114–8. DOI: 10.1016/j.jsbmb.2013.10.003
van der Meijden K, Lips P, van Driel M, Heijboer AC, Schulten EA, den Heijer M, et al. Primary human osteoblasts in response to 25-hydroxyvitamin D3, 1,25-dihydroxyvitamin D3 and 24R,25-dihydroxyvitamin D3. PLoS One. 2014;9(10):e110283. 10.1371/journal.pone.0110283. DOI: 10.1371/journal.pone.0110283
Lieben L, Carmeliet G. The delicate balance between vitamin D, calcium and bone homeostasis: lessons learned from intestinal- and osteocyte-specific VDR null mice. J Steroid Biochem Mol Biol. 2013;136:102–6. 10.1016/j.jsbmb.2012.09.019. DOI: 10.1016/j.jsbmb.2012.09.019
Yang D, Anderson PH, Wijenayaka AR, Barratt KR, Triliana R, Stapledon CJM, et al. Both ligand and VDR expression levels critically determine the effect of 1alpha,25-dihydroxyvitamin-D3 on osteoblast differentiation. J Steroid Biochem Mol Biol. 2018;177:83–90. 10.1016/j.jsbmb.2017.09.005. DOI: 10.1016/j.jsbmb.2017.09.005
