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Energy Balance and Bone Health: a Nutrient Availability Perspective

  • Nutrition, Exercise and Lifestyle (S Shapses and R Daly, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Obesity is highly prevalent and is associated with bone fragility and fracture. The changing nutrient availability to bone in obesity is an important facet of bone health. The goal of this article is to summarize current knowledge on the effects of carbohydrate and dietary fat availability on bone, particularly in the context of other tissues.

Recent Findings

The skeleton is a primary site for fatty acid and glucose uptake. The trafficking of carbohydrates and fats into tissues changes with weight loss and periods of weight gain. Exercise acutely influences nutrient uptake into bone and may affect nutrient partitioning to bone. Bone cells secrete hormones that signal to the brain and other tissues information about its energetic state, which may alter whole-body nutrient trafficking.

Summary

There is a critical need for studies to address the changes that metabolic perturbations have on nutrient availability in bone.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Ahmadi N, Sadr SM, Mohammadi MR, Mirzaei M, Mehrparvar AH, Yassini Ardekani SM, Sarebanhassanabadi M, Nilforoshan N, Mostafavi SA. Prevalence of abdominal obesity and metabolic syndrome in children and adolescents: a community based cross-sectional study. Iran J Public Health. 2020;49(2):360–8.

    PubMed  PubMed Central  Google Scholar 

  2. Liu AW, Song SO, Hayashi T, Sato KK, Kahn SE, Leonetti DL, Fujimoto WY, Boyko EJ. Change in CT-measured abdominal subcutaneous and visceral but not thigh fat areas predict future insulin sensitivity. Diabetes Res Clin Pract. 2019;154:17–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Nicklas BJ, Chmelo E, Delbono O, Carr JJ, Lyles MF, Marsh AP. Effects of resistance training with and without caloric restriction on physical function and mobility in overweight and obese older adults: a randomized controlled trial. Am J Clin Nutr. 2015;101(5):991–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kessler J, Koebnick C, Smith N, Adams A. Childhood obesity is associated with increased risk of most lower extremity fractures. Clin Orthop Relat Res. 2013;471(4):1199–207.

    Article  PubMed  Google Scholar 

  5. Felson DT, Zhang Y, Hannan MT, Anderson JJ. Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res. 1993;8(5):567–73.

    Article  CAS  PubMed  Google Scholar 

  6. Rodriguez-Gomez I, Manas A, Losa-Reyna J, Rodriguez-Manas L, Chastin SFM, Alegre LM, et al. Associations between sedentary time, physical activity and bone health among older people using compositional data analysis. PLoS ONE. 2018;13(10):e0206013.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Tamme R, Jurimae J, Maestu E, Remmel L, Purge P, Mengel E, et al. Physical activity in puberty is associated with total body and femoral neck bone mineral characteristics in males at 18 years of age. Medicina (Kaunas). 2019;55(5).

  8. Kim HY, Jung HW, Hong H, Kim JH, Shin CH, Yang SW, Lee YA. The role of overweight and obesity on bone health in Korean adolescents with a focus on lean and fat mass. J Korean Med Sci. 2017;32(10):1633–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zeng FF, Wu BH, Fan F, Xie HL, Xue WQ, Zhu HL, Chen YM. Dietary patterns and the risk of hip fractures in elderly Chinese: a matched case-control study. J Clin Endocrinol Metab. 2013;98(6):2347–55.

    Article  CAS  PubMed  Google Scholar 

  10. Wolfel EM, Jahn-Rickert K, Schmidt FN, Wulff B, Mushumba H, Sroga GE, et al. Individuals with type 2 diabetes mellitus show dimorphic and heterogeneous patterns of loss in femoral bone quality. Bone. 2020;140:115556.

    Article  PubMed  Google Scholar 

  11. • Merlo K, Aaronson J, Vaidya R, Rezaee T, Chalivendra V, Karim L. In vitro-induced high sugar environments deteriorate human cortical bone elastic modulus and fracture toughness. J Orthop Res. 2020;38(5):972-83. This paper observed reductions in elastic modulus and fracture toughness in human cortical bone specimens incubated with ribose compared to bone samples that were not treated.

  12. Yang L, Liu J, Shan Q, Geng G, Shao P. High glucose inhibits proliferation and differentiation of osteoblast in alveolar bone by inducing pyroptosis. Biochem Biophys Res Commun. 2020;522(2):471–8.

    Article  CAS  PubMed  Google Scholar 

  13. Pahwa H, Khan MT, Sharan K. Hyperglycemia impairs osteoblast cell migration and chemotaxis due to a decrease in mitochondrial biogenesis. Mol Cell Biochem. 2020;469(1-2):109–18.

    Article  CAS  PubMed  Google Scholar 

  14. Inzana JA, Kung M, Shu L, Hamada D, Xing LP, Zuscik MJ, Awad HA, Mooney RA. Immature mice are more susceptible to the detrimental effects of high fat diet on cancellous bone in the distal femur. Bone. 2013;57(1):174–83.

    Article  CAS  PubMed  Google Scholar 

  15. Wee NKY, Enriquez RF, Nguyen AD, Horsnell H, Kulkarni R, Khor EC, Herzog H, Baldock PA. Diet-induced obesity suppresses cortical bone accrual by a neuropeptide Y-dependent mechanism. Int J Obes (Lond). 2018;42(11):1925–38.

    Article  CAS  PubMed  Google Scholar 

  16. Sherk VD, Heveran CM, Foright RM, Johnson GC, Presby DM, Ferguson VL, MacLean PS. Sex differences in the effect of diet, obesity, and exercise on bone quality and fracture toughness. Bone. 2021;145:115840.

    Article  CAS  PubMed  Google Scholar 

  17. Niemeier A, Niedzielska D, Secer R, Schilling A, Merkel M, Enrich C, Rensen PCN, Heeren J. Uptake of postprandial lipoproteins into bone in vivo: impact on osteoblast function. Bone. 2008;43(2):230–7.

    Article  CAS  PubMed  Google Scholar 

  18. Picke AK, Sylow L, Moller LLV, Kjobsted R, Schmidt FN, Steejn MW, et al. Differential effects of high-fat diet and exercise training on bone and energy metabolism. Bone. 2018;116:120–34.

    Article  CAS  PubMed  Google Scholar 

  19. • Al Saedi A, Bermeo S, Plotkin L, Myers DE, Duque G. Mechanisms of palmitate-induced lipotoxicity in osteocytes. Bone. 2019;127:353-9. This paper observed decreases in RANKL, DKK1, and sclerostin expression in MLO-Y4 cells treated with palmitic acid compared to cells not treated. These conditions replicate what cells may experience in an environment exposed to an excess high-fat diet.

  20. Al Saedi A, Myers DE, Stupka N, Duque G. 1,25(OH)2D3 ameliorates palmitate-induced lipotoxicity in human primary osteoblasts leading to improved viability and function. Bone. 2020;141:115672.

    Article  PubMed  Google Scholar 

  21. McCabe LR, Irwin R, Tekalur A, Evans C, Schepper JD, Parameswaran N, et al. Exercise prevents high fat diet-induced bone loss, marrow adiposity and dysbiosis in male mice. Bone. 2019;118:20–31.

    Article  CAS  PubMed  Google Scholar 

  22. Mizokami A, Kawakubo-Yasukochi T, Hirata M. Osteocalcin and its endocrine functions. Biochem Pharmacol. 2017;132:1–8.

    Article  CAS  PubMed  Google Scholar 

  23. Mosialou I, Shikhel S, Liu JM, Maurizi A, Luo N, He Z, Huang Y, Zong H, Friedman RA, Barasch J, Lanzano P, Deng L, Leibel RL, Rubin M, Nickolas T, Chung W, Zeltser LM, Williams KW, Pessin JE, Kousteni S. MC4R-dependent suppression of appetite by bone-derived lipocalin 2. Nature. 2017;543(7645):385–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. •• Mosialou I, Shikhel S, Luo N, Petropoulou PI, Panitsas K, Bisikirska B, et al. Lipocalin -2 counteracts metabolic dysregulation in obesity and diabetes. J Exp Med. 2020;217(10). Bone is emerging as an endocrine organ and this paper demonstrates how reducing lipocalin-2 expression in mice leads to metabolic dysfunction, increases in fat mass, and glucose intolerance.

  25. Bartelt A, Koehne T, Todter K, Reimer R, Muller B, Behler-Janbeck F, et al. Quantification of bone fatty acid metabolism and its regulation by adipocyte lipoprotein lipase. Int J Mol Sci. 2017;18(6).

  26. Ferron M, Hinoi E, Karsenty G, Ducy P. Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci U S A. 2008;105(13):5266–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G. Endocrine regulation of energy metabolism by the skeleton. Cell. 2007;130(3):456–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kim SP, Frey JL, Li Z, Kushwaha P, Zoch ML, Tomlinson RE, da H, Aja S, Noh HL, Kim JK, Hussain MA, Thorek DLJ, Wolfgang MJ, Riddle RC. Sclerostin influences body composition by regulating catabolic and anabolic metabolism in adipocytes. Proc Natl Acad Sci U S A. 2017;114(52):E11238–E47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nguyen HH, Wu F, Oddy WH, Wills K, Winzenberg T, Jones G. Associations between dietary patterns and osteoporosis-related outcomes in older adults: a longitudinal study. Eur J Clin Nutr. 2021;75(5):792–800.

    Article  CAS  PubMed  Google Scholar 

  30. Qiu R, Cao WT, Tian HY, He J, Chen GD, Chen YM. Greater intake of fruit and vegetables is associated with greater bone mineral density and lower osteoporosis risk in middle-aged and elderly adults. PLoS ONE. 2017;12(1):e0168906.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Regu GM, Kim H, Kim YJ, Paek JE, Lee G, Chang N, et al. Association between dietary carotenoid intake and bone mineral density in Korean adults aged 30-75 years using data from the Fourth and Fifth Korean National Health and Nutrition Examination Surveys (2008-2011). Nutrients. 2017;9(9).

  32. Silva TRD, Martins CC, Ferreira LL, Spritzer PM. Mediterranean diet is associated with bone mineral density and muscle mass in postmenopausal women. Climacteric. 2019;22(2):162–8.

    Article  PubMed  Google Scholar 

  33. Perez-Rey J, Roncero-Martin R, Rico-Martin S, Rey-Sanchez P, Pedrera-Zamorano JD, Pedrera-Canal M, et al. Adherence to a Mediterranean diet and bone mineral density in Spanish premenopausal women. Nutrients. 2019;11(3).

  34. Malmir H, Saneei P, Larijani B, Esmaillzadeh A. Adherence to Mediterranean diet in relation to bone mineral density and risk of fracture: a systematic review and meta-analysis of observational studies. Eur J Nutr. 2018;57(6):2147–60.

    Article  PubMed  Google Scholar 

  35. Mu M, Wang SF, Sheng J, Zhao Y, Wang GX, Liu KY, Hu CL, Tao FB, Wang HL. Dietary patterns are associated with body mass index and bone mineral density in Chinese freshmen. J Am Coll Nutr. 2014;33(2):120–8.

    Article  CAS  PubMed  Google Scholar 

  36. Minematsu A, Nishii Y, Sakata S. High-fat/high-sucrose diet results in higher bone mass in aged rats. Bone Rep. 2018;8:18–24.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tian L, Wang C, Xie Y, Wan S, Zhang K, Yu X. High fructose and high fat exert different effects on changes in trabecular bone micro-structure. J Nutr Health Aging. 2018;22(3):361–70.

    Article  CAS  PubMed  Google Scholar 

  38. Hafner H, Chang E, Carlson Z, Zhu A, Varghese M, Clemente J, et al. Lactational high-fat diet exposure programs metabolic inflammation and bone marrow adiposity in male offspring. Nutrients. 2019;11(6).

  39. Zhang Z, Lin T, Meng Y, Hu M, Shu L, Jiang H, Gao R, Ma J, Wang C, Zhou X. FOS/GOS attenuates high-fat diet induced bone loss via reversing microbiota dysbiosis, high intestinal permeability and systemic inflammation in mice. Metabolism. 2021;119:154767.

    Article  CAS  PubMed  Google Scholar 

  40. Sherk VD, Jackman MR, Higgins JA, Giles ED, Foright RM, Presby DM, et al. Impact of exercise and activity on weight regain and musculoskeletal health post-ovariectomy. Med Sci Sports Exerc. 2019;51(12):2465–73.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Li Z, Frey JL, Wong GW, Faugere MC, Wolfgang MJ, Kim JK, Riddle RC, Clemens TL. Glucose transporter-4 facilitates insulin-stimulated glucose uptake in osteoblasts. Endocrinology. 2016;157(11):4094–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. • Rendina-Ruedy E, Guntur AR, Rosen CJ. Intracellular lipid droplets support osteoblast function. Adipocyte. 2017;6(3):250-8. This paper provides evidence lipid uptake is required for osteoblasts in order to function properly.

  43. Tintut Y, Morony S, Demer LL. Hyperlipidemia promotes osteoclastic potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol. 2004;24(2):e6–10.

    Article  CAS  PubMed  Google Scholar 

  44. Oh SR, Sul OJ, Kim YY, Kim HJ, Yu R, Suh JH, Choi HS. Saturated fatty acids enhance osteoclast survival. J Lipid Res. 2010;51(5):892–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zoch ML, Abou DS, Clemens TL, Thorek DL, Riddle RC. In vivo radiometric analysis of glucose uptake and distribution in mouse bone. Bone Res. 2016;4:16004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. • Heinonen I, Kemppainen J, Fujimoto T, Knuuti J, Kalliokoski KK. Increase of glucose uptake in human bone marrow with increasing exercise intensity. Int J Sport Nutr Exerc Metab. 2019;29(3):254-8. Bone marrow adipose is often thought of only as an ectopic fat reservoir. This paper observed an increase in bone marrow glucose uptake in males exposed to moderate-intensity exercise compared to low-intensity exercise. This refutes the reservoir idea and shows a change in nutrient intake under increased energy demands.

  47. Heinonen I, Kemppainen J, Kaskinoro K, Langberg H, Knuuti J, Boushel R, Kjaer M, Kalliokoski KK. Bone blood flow and metabolism in humans: effect of muscular exercise and other physiological perturbations. J Bone Miner Res. 2013;28(5):1068–74.

    Article  CAS  PubMed  Google Scholar 

  48. Rojas JM, Bolze F, Thorup I, Nowak J, Dalsgaard CM, Skydsgaard M, Berthelsen LO, Keane KA, Søeborg H, Sjögren I, Jensen JT, Fels JJ, Offenberg HK, Andersen LW, Dalgaard M. The effect of diet-induced obesity on toxicological parameters in the polygenic Sprague-Dawley rat model. Toxicol Pathol. 2018;46(7):777–98.

    Article  CAS  PubMed  Google Scholar 

  49. Montalvany-Antonucci CC, Zicker MC, Ferreira AVM, Macari S, Ramos-Junior ES, Gomez RS, Pereira TSF, Madeira MFM, Fukada SY, Andrade I Jr, Silva TA. High-fat diet disrupts bone remodeling by inducing local and systemic alterations. J Nutr Biochem. 2018;59:93–103.

    Article  CAS  PubMed  Google Scholar 

  50. Montalvany-Antonucci CC, Duffles LF, de Arruda JAA, Zicker MC, de Oliveira S, Macari S, Garlet GP, Madeira MFM, Fukada SY, Andrade I Jr, Teixeira MM, Mackay C, Vieira AT, Vinolo MA, Silva TA. Short-chain fatty acids and FFAR2 as suppressors of bone resorption. Bone. 2019;125:112–21.

    Article  CAS  PubMed  Google Scholar 

  51. Silva MJ, Eekhoff JD, Patel T, Kenney-Hunt JP, Brodt MD, Steger-May K, Scheller EL, Cheverud JM. Effects of high-fat diet and body mass on bone morphology and mechanical properties in 1100 advanced intercross mice. J Bone Miner Res. 2019;34(4):711–25.

    Article  CAS  PubMed  Google Scholar 

  52. Wang Y, Dellatore P, Douard V, Qin L, Watford M, Ferraris RP, Lin T, Shapses SA. High fat diet enriched with saturated, but not monounsaturated fatty acids adversely affects femur, and both diets increase calcium absorption in older female mice. Nutr Res. 2016;36(7):742–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhan Q, Tian Y, Han L, Wang K, Wang J, Xue C. The opposite effects of Antarctic krill oil and arachidonic acid-rich oil on bone resorption in ovariectomized mice. Food Funct. 2020;11(8):7048–60.

    Article  CAS  PubMed  Google Scholar 

  54. Niu Y, Yang Z, Li X, Zhang W, Lu S, Zhang H, Chen X, Zhu L, Xing Y, Ning G, Qin L, Su Q. Association of osteoprotegerin with impaired glucose regulation and microalbuminuria: the REACTION study. BMC Endocr Disord. 2015;15:75.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Guntur AR, Gerencser AA, Le PT, DeMambro VE, Bornstein SA, Mookerjee SA, et al. Osteoblast-like MC3T3-E1 cells prefer glycolysis for ATP production but adipocyte-like 3T3-L1 cells prefer oxidative phosphorylation. J Bone Miner Res. 2018;33(6):1052–65.

    Article  CAS  PubMed  Google Scholar 

  56. Hahn TJ, Westbrook SL, Sullivan TL, Goodman WG, Halstead LR. Glucose transport in osteoblast-enriched bone explants: characterization and insulin regulation. J Bone Miner Res. 1988;3(3):359–65.

    Article  CAS  PubMed  Google Scholar 

  57. Wei J, Shimazu J, Makinistoglu MP, Maurizi A, Kajimura D, Zong H, Takarada T, Iezaki T, Pessin JE, Hinoi E, Karsenty G. Glucose uptake and Runx2 synergize to orchestrate osteoblast differentiation and bone formation. Cell. 2015;161(7):1576–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Dirckx N, Tower RJ, Mercken EM, Vangoitsenhoven R, Moreau-Triby C, Breugelmans T, Nefyodova E, Cardoen R, Mathieu C, van der Schueren B, Confavreux CB, Clemens TL, Maes C. Vhl deletion in osteoblasts boosts cellular glycolysis and improves global glucose metabolism. J Clin Invest. 2018;128(3):1087–105.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Galaviz KI, Weber MB, Straus A, Haw JS, Narayan KMV, Ali MK. Global diabetes prevention interventions: a systematic review and network meta-analysis of the real-world impact on incidence, weight, and glucose. Diabetes Care. 2018;41(7):1526–34.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Pellegrini M, Cioffi I, Evangelista A, Ponzo V, Goitre I, Ciccone G, Ghigo E, Bo S. Effects of time-restricted feeding on body weight and metabolism. A systematic review and meta-analysis. Rev Endocr Metab Disord. 2020;21(1):17–33.

    Article  PubMed  Google Scholar 

  61. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292(14):1724–37.

    Article  CAS  PubMed  Google Scholar 

  62. Puzziferri N, Roshek TB 3rd, Mayo HG, Gallagher R, Belle SH, Livingston EH. Long-term follow-up after bariatric surgery: a systematic review. JAMA. 2014;312(9):934–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Maclean PS, Bergouignan A, Cornier MA, Jackman MR. Biologyʼs response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol. 2011;301(3):R581–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Jackman MR, Steig A, Higgins JA, Johnson GC, Fleming-Elder BK, Bessesen DH, MacLean PS. Weight regain after sustained weight reduction is accompanied by suppressed oxidation of dietary fat and adipocyte hyperplasia. Am J Physiol Regul Integr Comp Physiol. 2008;294(4):R1117–29.

    Article  CAS  PubMed  Google Scholar 

  65. MacLean PS, Blundell JE, Mennella JA, Batterham RL. Biological control of appetite: a daunting complexity. Obesity (Silver Spring). 2017;25(Suppl 1):S8–S16.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Schenk S, Harber MP, Shrivastava CR, Burant CF, Horowitz JF. Improved insulin sensitivity after weight loss and exercise training is mediated by a reduction in plasma fatty acid mobilization, not enhanced oxidative capacity. J Physiol. 2009;587(Pt 20):4949–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. MacLean PS, Higgins JA, Giles ED, Sherk VD, Jackman MR. The role for adipose tissue in weight regain after weight loss. Obes Rev. 2015;16(Suppl 1):45–54.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M. Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology. 2001;2(3):165–71.

    Article  CAS  PubMed  Google Scholar 

  69. Kricun ME. Red-yellow marrow conversion: its effect on the location of some solitary bone lesions. Skeletal Radiol. 1985;14(1):10–9.

    Article  CAS  PubMed  Google Scholar 

  70. Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, Zerhouni EA. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology. 1990;177(1):83–8.

    Article  CAS  PubMed  Google Scholar 

  71. Sieron D, Drakopoulos D, Loebelenz LI, Schroeder C, Ebner L, Obmann VC, et al. Correlation between fat signal ratio on T1-weighted MRI in the lower vertebral bodies and age, comparing 1.5-T and 3-T scanners. Acta Radiol Open. 2020;9(1):2058460120901517.

  72. • Suchacki KJ, Tavares AAS, Mattiucci D, Scheller EL, Papanastasiou G, Gray C, et al. Bone marrow adipose tissue is a unique adipose subtype with distinct roles in glucose homeostasis. Nat Commun. 2020;11(1):3097. This paper observed differences between bone marrow adipose tissue (BMA) and white and brown adipose tissue in glucose metabolism, thus providing support to the hypothesis of BMA contributing to whole body energy uptake.

  73. • Hussain MM, Mahley RW, Boyles JK, Lindquist PA, Brecht WJ, Innerarity TL. Chylomicron metabolism. Chylomicron uptake by bone marrow in different animal species. J Biol Chem. 1989;264(30):17931-8. This paper is one of the first studies that demonstrates chylomicron uptake into the bone marrow, providing evidence that bone is a metabolically active organ.

  74. Styner M, Pagnotti GM, McGrath C, Wu X, Sen B, Uzer G, Xie Z, Zong X, Styner MA, Rubin CT, Rubin J. Exercise decreases marrow adipose tissue through ss-oxidation in obese running mice. J Bone Miner Res. 2017;32(8):1692–702.

    Article  CAS  PubMed  Google Scholar 

  75. •• McGrath C, Sankaran JS, Misaghian-Xanthos N, Sen B, Xie Z, Styner MA, et al. Exercise degrades bone in caloric restriction, despite suppression of marrow adipose tissue (MAT). J Bone Miner Res. 2020;35(1):106-15. This paper observed increases in bone fatty acid uptake in calorie-restricted mice when compared to mice on a regular diet.

  76. Spurny M, Jiang Y, Sowah SA, Schubel R, Nonnenmacher T, Bertheau R, et al. Changes in bone marrow fat upon dietary-induced weight loss. Nutrients. 2020;12(5).

  77. Scheller EL, Khoury B, Moller KL, Wee NK, Khandaker S, Kozloff KM, et al. Changes in skeletal integrity and marrow adiposity during high-fat diet and after weight loss. Front Endocrinol (Lausanne). 2016;7:102.

  78. Bosy-Westphal A, Later W, Schautz B, Lagerpusch M, Goele K, Heller M, Glüer CC, Müller MJ. Impact of intra- and extra-osseous soft tissue composition on changes in bone mineral density with weight loss and regain. Obesity (Silver Spring). 2011;19(7):1503–10.

    Article  PubMed  Google Scholar 

  79. Kim TY, Schwartz AV, Li X, Xu K, Black DM, Petrenko DM, Stewart L, Rogers SJ, Posselt AM, Carter JT, Shoback DM, Schafer AL. Bone marrow fat changes after gastric bypass surgery are associated with loss of bone mass. J Bone Miner Res. 2017;32(11):2239–47.

    Article  CAS  PubMed  Google Scholar 

  80. Bredella MA, Greenblatt LB, Eajazi A, Torriani M, Yu EW. Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone. 2017;95:85–90.

    Article  PubMed  Google Scholar 

  81. Bredella MA, Fazeli PK, Miller KK, Misra M, Torriani M, Thomas BJ, Ghomi RH, Rosen CJ, Klibanski A. Increased bone marrow fat in anorexia nervosa. J Clin Endocrinol Metab. 2009;94(6):2129–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Levental KR, Surma MA, Skinkle AD, Lorent JH, Zhou Y, Klose C, et al. Omega-3 polyunsaturated fatty acids direct differentiation of the membrane phenotype in mesenchymal stem cells to potentiate osteogenesis. Sci Adv. 2017;3(11):eaao1193.

  83. Al Saedi A, C AG, D EM, Hayes A, Duque G. Rapamycin affects palmitate-induced lipotoxicity in osteoblasts by modulating apoptosis and autophagy. J Gerontol A Biol Sci Med Sci. 2020;75(1):58-63.

  84. Jackman MR, Kramer RE, MacLean PS, Bessesen DH. Trafficking of dietary fat in obesity-prone and obesity-resistant rats. Am J Physiol Endocrinol Metab. 2006;291(5):E1083–91.

    Article  CAS  PubMed  Google Scholar 

  85. Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, Clemens TL. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010;142(2):309–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Jansson JO, Palsdottir V, Hagg DA, Schele E, Dickson SL, Anesten F, et al. Body weight homeostat that regulates fat mass independently of leptin in rats and mice. Proc Natl Acad Sci U S A. 2018;115(2):427–32.

    Article  CAS  PubMed  Google Scholar 

  87. Ohlsson C, Gidestrand E, Bellman J, Larsson C, Palsdottir V, Hagg D, et al. Increased weight loading reduces body weight and body fat in obese subjects - a proof of concept randomized clinical trial. EClinicalMedicine. 2020;22:100338.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Turner RT, Branscum AJ, Wong CP, Iwaniec UT, Morey-Holton E. Studies in microgravity, simulated microgravity and gravity do not support a gravitostat. J Endocrinol. 2020;247(3):273–82.

    Article  PubMed  Google Scholar 

  89. Foright RM, Presby DM, Sherk VD, Kahn D, Checkley LA, Giles ED, Bergouignan A, Higgins JA, Jackman MR, Hill JO, MacLean PS. Is regular exercise an effective strategy for weight loss maintenance? Physiol Behav. 2018;188:86–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

NIH KL2 TR002534 (VS), ASBMR Rising Star Award (VS)

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Authors and Affiliations

  1. Department of Mechanical Engineering, University of Colorado Denver, Denver, CO, USA

    Beatriz Bermudez & R. Dana Carpenter

  2. Department of Orthopedics, University of Colorado Anschutz Medical Campus, Aurora, CO, USA

    Beatriz Bermudez, Toru Ishii & Vanessa D. Sherk

  3. Department of Surgery, Johns Hopkins University, Baltimore, MD, USA

    Yuan-Haw Wu

  4. Division of Translational and Clinical Sciences, Center for Scientific Review, National Institutes of Health, Bethesda, MD, USA

    Vanessa D. Sherk

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  1. Beatriz Bermudez
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  2. Toru Ishii
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  5. Vanessa D. Sherk
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This article was prepared while Vanessa Sherk, PhD, was employed at the University of Colorado. The opinions expressed in this article are the authors’ own and do not reflect the view of the National Institutes of Health, the Department of Health and Human Services, or the United States government.

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Bermudez, B., Ishii, T., Wu, YH. et al. Energy Balance and Bone Health: a Nutrient Availability Perspective. Curr Osteoporos Rep 21, 77–84 (2023). https://doi.org/10.1007/s11914-022-00765-4

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