Increase of Glucose Uptake in Human Bone Marrow With Increasing Exercise Intensity

in International Journal of Sport Nutrition and Exercise Metabolism
Restricted access

Purchase article

USD $24.95

Student 1 year subscription

USD $87.00

1 year subscription

USD $116.00

Student 2 year subscription

USD $165.00

2 year subscription

USD $215.00

Human bone marrow is a metabolically active tissue that responds to acute low-intensity exercise by having increased glucose uptake (GU). Here, the authors studied whether bone marrow GU increases more with increased exercise intensities. Femoral bone marrow GU was measured using positron emission tomography and [18F]-fluorodeoxyglucose in six healthy young men during cycling at intensities of 30% (low), 55% (moderate), and 75% (high) of maximal oxygen consumption on three separate days. Bone marrow GU at low was 17.2 µmol·kg−1·min−1 (range 9.0–25.4) and increased significantly (p = .003) at moderate (31.2 µmol·kg−1·min−1, 22.9–39.4) but was not significant from moderate to high (37.4 µmol·kg−1·min−1, 29.0–45.7, p = .26). Furthermore, the ratio between bone and muscle GU decreased from low to moderate exercise intensity (p < .01) but not (p = .99) from moderate to high exercise intensity. In conclusion, these results show that although the increase is not as large as observed in exercising skeletal muscle, GU in femoral bone marrow increases with increasing exercise intensity at least from low- to moderate-intensity effort, which may be important for bone and whole-body metabolic health.

Heinonen, Kemppainen, Knuuti, and Kalliokoski are with the Dept. of Clinical Physiology and Nuclear Medicine, University of Turku, Turku, Finland. Heinonen is with the Div. of Experimental Cardiology, Thoraxcenter, Erasmus MC University Medical Center, Rotterdam, The Netherlands. Kemppainen, and Knuuti are also with the Turku University Hospital. Fujimoto is with the Institute for Excellence in Higher Education, Tohoku University, Sendai, Japan.

Address author correspondence to Ilkka Heinonen at ilkka.heinonen@utu.fi.
International Journal of Sport Nutrition and Exercise Metabolism
Article Sections
References
  • BermeoS.GunaratnamK. & DuqueG. (2014). Fat and bone interactions. Current Osteoporosis Reports 12235242. PubMed ID: 24599601 doi:10.1007/s11914-014-0199-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ChenY.C.TraversR.L.WalhinJ.P.GonzalezJ.T.KoumanovF.BettsJ.A. & ThompsonD. (2017). Feeding influences adipose tissue responses to exercise in overweight men. American Journal of Physiology-Endocrinology and Metabolism 3138493. PubMed ID: 28292758 doi:10.1152/ajpendo.00006.2017

    • Crossref
    • Search Google Scholar
    • Export Citation
  • DykeJ.P. & AaronR.K. (2010). Noninvasive methods of measuring bone blood perfusion. Annals of the New York Academy of Sciences 119295102. PubMed ID: 20392223 doi:10.1111/j.1749-6632.2009.05376.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • FujimotoT.KemppainenJ.KalliokoskiK.K.NuutilaP.ItoM. & KnuutiJ. (2003). Skeletal muscle glucose uptake response to exercise in trained and untrained men. Medicine & Science in Sports & Exercise 35777783. PubMed ID: 12750587 doi:10.1249/01.MSS.0000065070.49295.C0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • GonzalezJ.T.RichardsonJ.D.ChowdhuryE.A.KoumanovF.HolmanG.D.CooperS. . . . BettsJ.A. (2018). Molecular adaptations of adipose tissue to 6 weeks of morning fasting vs. daily breakfast consumption in lean and obese adults. The Journal of Physiology 596609622. PubMed ID: 29193093 doi:10.1113/JP275113

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HamacherK.CoenenH.H & StöcklinG. (1986). Efficient stereospecific synthesis of no-carrier-added 2-[18F]-fluoro-2-deoxy-D-glucose using aminopolyether supported nucleophilic substitution. Journal of nuclear medicine: official publication Society of Nuclear Medicine 27(2) 235238. PubMed ID: 3712040

    • Search Google Scholar
    • Export Citation
  • HardouinP.MarieP.J. & RosenC.J. (2016). New insights into bone marrow adipocytes: Report from the first European meeting on Bone Marrow Adiposity (BMA 2015). Bone 93212215. PubMed ID: 26608519 doi:10.1016/j.bone.2015.11.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HardouinP.PansiniV. & CortetB. (2014). Bone marrow fat. Joint Bone Spine 81313319. PubMed ID: 24703396 doi:10.1016/j.jbspin.2014.02.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.BrothersR.M.KemppainenJ.KnuutiJ.KalliokoskiK.K. & CrandallC.G. (2011a). Local heating, but not indirect whole body heating, increases human skeletal muscle blood flow. Journal of Applied Physiology 111818824. PubMed ID: 21680875 doi:10.1152/japplphysiol.00269.2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.KalliokoskiK.K.HannukainenJ.C.DunckerD.J.NuutilaP. & KnuutiJ. (2014). Organ-specific physiological responses to acute physical exercise and long-term training in humans. Physiology 29421436. PubMed ID: 25362636 doi:10.1152/physiol.00067.2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.KemppainenJ.KaskinoroK.LangbergH.KnuutiJ.BoushelR.KjaerM. & KalliokoskiK.K. (2013a). Bone blood flow and metabolism in humans: Effect of muscular exercise and other physiological perturbations. Journal of Bone and Mineral Research 2810681074. PubMed ID: 23280932 doi:10.1002/jbmr.1833

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.KemppainenJ.KaskinoroK.PeltonenJ.E.BorraR.LindroosM.M. . . . KalliokoskiK.K. (2010a). Comparison of exogenous adenosine and voluntary exercise on human skeletal muscle perfusion and perfusion heterogeneity. Journal of Applied Physiology 108378386 . doi:10.1152/japplphysiol.00745.2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.KogaS.KalliokoskiK.K.MuschT.I. & PooleD.C. (2015). Heterogeneity of muscle blood flow and metabolism: Influence of exercise, aging and disease states. Exercise and Sport Sciences Reviews 43(3) 117124. PubMed ID: 25688763 doi:10.1249/JES.0000000000000044

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.NesterovS.V.KemppainenJ.FujimotoT.KnuutiJ. & KalliokoskiK.K. (2012). Increasing exercise intensity reduces heterogeneity of glucose uptake in human skeletal muscles. PLoS One 7e52191. PubMed ID: 23284929 doi:10.1371/journal.pone.0052191

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.NesterovS.V.KemppainenJ.NuutilaP.KnuutiJ.LaitioR. . . . KalliokoskiK.K. (2007). Role of adenosine in regulating the heterogeneity of skeletal muscle blood flow during exercise in humans. Journal of Applied Physiology 10320422048. PubMed ID: 17885025 doi:10.1152/japplphysiol.00567.2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.SaltinB.KemppainenJ.SipilaH.T.OikonenV.NuutilaP. . . . HellstenY. (2011b). Skeletal muscle blood flow and oxygen uptake at rest and during exercise in humans: a PET study with nitric oxide and cyclooxygenase inhibition. American Journal of Physiology-Heart and Circulatory Physiology 300H1510H1517. PubMed ID: 21257921 doi:10.1152/ajpheart.00996.2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.Wendelin-SaarenhoviM.KaskinoroK.KnuutiJ.ScheininM. & KalliokoskiK.K. (2013b). Inhibition of α-adrenergic tone disturbs the distribution of blood flow in the exercising human limb. American Journal of Physiology-Heart and Circulatory Physiology 305H163H172. PubMed ID: 23666670 doi:10.1152/ajpheart.00925.2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HeinonenI.H.KemppainenJ.KaskinoroK.PeltonenJ.E.BorraR.LindroosM. . . . KalliokoskiK.K. (2010b). Regulation of human skeletal muscle perfusion and its heterogeneity during exercise in moderate hypoxia. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 299R72R79. PubMed ID: 20427728 doi:10.1152/ajpregu.00056.2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HuovinenV.SaunavaaraV.KivirantaR.TarkiaM.HonkaH.StarkC. . . . ParkkolaR. (2014). Vertebral bone marrow glucose uptake is inversely associated with bone marrow fat in diabetic and healthy pigs: [(18)F]FDG-PET and MRI study. Bone 613338. PubMed ID: 24389418 doi:10.1016/j.bone.2013.12.022

    • Crossref
    • Search Google Scholar
    • Export Citation
  • KemppainenJ.FujimotoT.KalliokoskiK.K.ViljanenT.NuutilaP. & KnuutiJ. (2002). Myocardial and skeletal muscle glucose uptake during exercise in humans. The Journal of Physiology 542403412. PubMed ID: 12122141 doi:10.1113/jphysiol.2002.018135

    • Crossref
    • Search Google Scholar
    • Export Citation
  • KringsA.RahmanS.HuangS.LuY.CzernikP.J. & Lecka-CzernikB. (2012). Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone 50(2) 546552. PubMed ID: 21723971 doi:10.1016/j.bone.2011.06.016

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lecka-CzernikB. (2012). Marrow fat metabolism is linked to the systemic energy metabolism. Bone 50(2) 534539. PubMed ID: 21757043 doi:10.1016/j.bone.2011.06.032

    • Crossref
    • Search Google Scholar
    • Export Citation
  • StynerM.ThompsonW.R.GaliorK.UzerG.WuX.KadariS. . . . RubinJ. (2014). Bone marrow fat accumulation accelerated by high fat diet is suppressed by exercise. Bone 643946. PubMed ID: 24709686 doi:10.1016/j.bone.2014.03.044

    • Crossref
    • Search Google Scholar
    • Export Citation
  • VirtanenK.A.LonnrothP.ParkkolaR.PeltoniemiP.AsolaM.ViljanenT. . . . NuutilaP. (2002). Glucose uptake and perfusion in subcutaneous and visceral adipose tissue during insulin stimulation in nonobese and obese humans. The Journal of Clinical Endocrinology & Metabolism 8739023910. PubMed ID: 12161530 doi:10.1210/jcem.87.8.8761

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ZochM.L.AbouD.S.ClemensT.L.ThorekD.L. & RiddleR.C. (2016). In vivo radiometric analysis of glucose uptake and distribution in mouse bone. Bone Research 416004. PubMed ID: 27088042 doi:10.1038/boneres.2016.4

    • Crossref
    • Search Google Scholar
    • Export Citation
Article Metrics
All Time Past Year Past 30 Days
Abstract Views 61 61 20
Full Text Views 6 6 3
PDF Downloads 4 4 3
Altmetric Badge
PubMed
Google Scholar
Cited By