Glucocorticoid-induced insulin resistance in men is associated with suppressed undercarboxylated osteocalcin

Journal article


Parker, Lewan, Lin, Xuzhu, Garnham, Andrew, McConell, Glenn, Stepto, Nigel K., Hare, David L., Byrnes, Elizabeth, Ebeling, Peter R., Seeman, Ego, Brennan-Speranza, Tara C. and Levinger, Itamar. (2019) Glucocorticoid-induced insulin resistance in men is associated with suppressed undercarboxylated osteocalcin. Journal of Bone and Mineral Research. 34(1), pp. 49 - 58. https://doi.org/10.1002/jbmr.3574
AuthorsParker, Lewan, Lin, Xuzhu, Garnham, Andrew, McConell, Glenn, Stepto, Nigel K., Hare, David L., Byrnes, Elizabeth, Ebeling, Peter R., Seeman, Ego, Brennan-Speranza, Tara C. and Levinger, Itamar
Abstract

In mice, glucocorticoid‐induced insulin resistance occurs largely through impaired osteoblast function and decreased circulating undercarboxylated osteocalcin (ucOC). Whether these mechanisms contribute to glucocorticoid‐induced insulin resistance in humans has yet to be established. In addition, the effects of glucocorticoids on the exercise‐induced increase in circulating ucOC and insulin sensitivity are also unknown. We hypothesized that acute glucocorticoid treatment would lead to basal and postexercise insulin resistance in part through decreased circulating ucOC and ucOC‐mediated skeletal muscle protein signaling. Nine healthy men completed two separate cycling sessions 12 hours after ingesting either glucocorticoid (20 mg prednisolone) or placebo (20 mg Avicel). The homeostatic model assessment was used to assess basal insulin sensitivity and a 2‐hour euglycemic–hyperinsulinemic clamp was commenced 3 hours after exercise to assess postexercise insulin sensitivity. Serum ucOC and skeletal muscle protein signaling were measured. Single‐dose glucocorticoid ingestion increased fasting glucose (27%, p  < 0.01) and insulin (83%, p  < 0.01), and decreased basal insulin sensitivity (−47%, p  < 0.01). Glucocorticoids reduced insulin sensitivity after cycling exercise (−34%, p  < 0.01), reduced muscle GPRC6A protein content (16%, p  < 0.05), and attenuated protein phosphorylation of mTORSer2481, AktSer374, and AS160Thr642 (59%, 61%, and 50%, respectively; all p s < 0.05). Serum ucOC decreased (−24%, p  < 0.01) which correlated with lower basal insulin sensitivity (r  = 0.54, p  = 0.02), lower insulin sensitivity after exercise (r  = 0.72, p  < 0.05), and attenuated muscle protein signaling (r  = 0.48–0.71, p  < 0.05). Glucocorticoid‐induced basal and postexercise insulin resistance in humans is associated with the suppression of circulating ucOC and ucOC‐linked protein signaling in skeletal muscle. Whether ucOC treatment can offset glucocorticoid‐induced insulin resistance in human subjects requires further investigation. © 2018 American Society for Bone and Mineral Research.

Keywordsglucocorticoid metabolism; anti-inflammation; glycemic control; high-intensity interval exercise; insulin signaling
Year2019
JournalJournal of Bone and Mineral Research
Journal citation34 (1), pp. 49 - 58
PublisherJohn Wiley & Sons
ISSN0884-0431
Digital Object Identifier (DOI)https://doi.org/10.1002/jbmr.3574
Scopus EID2-s2.0-85053517542
Page range49 - 58
Research GroupMary MacKillop Institute for Health Research
Place of publicationUnited States of America
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Zebaze, Roger and Seeman, Ego. (2015) Cortical bone: A challenging geography. Journal of Bone and Mineral Research. 30(1), pp. 24 - 29. https://doi.org/10.1002/jbmr.2419
Regional heterogeneity in the configuration of the intracortical canals of the femoral shaft
Perilli, Egon, Bala, Yohann, Zebaze, Roger M., Reynolds, Karen J. and Seeman, Ego. (2015) Regional heterogeneity in the configuration of the intracortical canals of the femoral shaft. Calcified Tissue International. 97(4), pp. 327 - 335. https://doi.org/10.1007/s00223-015-0014-5
Changes in quality of life associated with fragility fractures : Australian arm of the International Cost and Utility Related to Osteoporotic Fractures Study (AusICUROS)
Abimanyi-Ochom, J., Watts, Jennifer, Borgstrom, F., Nicholson, Geoffrey, Shore-Lorenti, Catherine, Stuart, Amanda, Zhang, Y., Luliano, S., Seeman, Ego, Prince, Richard, March, Lyn, Winzenberg, T., Laslett, Laura, Duque, Gustavo, Ebeling, P. and Sanders, K. M.. (2015) Changes in quality of life associated with fragility fractures : Australian arm of the International Cost and Utility Related to Osteoporotic Fractures Study (AusICUROS). Osteoporosis International. 26(6), pp. 1781 - 1790. https://doi.org/10.1007/s00198-015-3088-z
The effects of knee injury on skeletal muscle function, Na+-ATPase content, and isoform abundance
Perry, Ben D., Levinger, P, Morris, Hayden G., Petersen, Aaron C., Garnham, Andrew, Levinger, Itamar and McKenna, Michael J.. (2015) The effects of knee injury on skeletal muscle function, Na+-ATPase content, and isoform abundance. Physiological Reports. 3(2), pp. 1 - 14. https://doi.org/10.14814/phy2.12294
Genetic and environmental variances of bone microarchitecture and bone remodeling markers: A twin study
Bjornerem, Ashild, Bui, Q Minh, Wang, Xiaofang, Ghasem-Zadeh, Ali, Hopper, John L., Zebaze, Roger M. and Seeman, Ego. (2015) Genetic and environmental variances of bone microarchitecture and bone remodeling markers: A twin study. Journal of Bone and Mineral Research. 30(3), pp. 516 - 524. https://doi.org/10.1002/jbmr.2365
Bones material constituents and their contribution to bone strength in health, disease, and treatment
Bala, Y. and Seeman, Ego. (2015) Bones material constituents and their contribution to bone strength in health, disease, and treatment. Calcified Tissue International. 97(3), pp. 308 - 326. https://doi.org/10.1007/s00223-015-9971-y
A. Michael Parfitt: Enlightened scholar and revered mentor: May 10, 1930-May 18, 2015
Manolagas, Stavros C., Compston, Juliet, Rao, Sudhaker and Seeman, Ego. (2015) A. Michael Parfitt: Enlightened scholar and revered mentor: May 10, 1930-May 18, 2015. Journal of Bone and Mineral Research. 30(8), pp. 1349 - 1355. https://doi.org/10.1002/jbmr.2576
Co-administration of antiresorptive and anabolic agents: A missed opportunity
Seeman, Ego and Martin, T. John. (2015) Co-administration of antiresorptive and anabolic agents: A missed opportunity. Journal of Bone and Mineral Research. 30(5), pp. 753 - 764. https://doi.org/10.1002/jbmr.2496
The ABC of writing a grant proposal
Seeman, Ego. (2015) The ABC of writing a grant proposal. Osteoporosis International. 26(6), pp. 1665 - 1666. https://doi.org/10.1007/s00198-015-3085-2
Growth and age-related abnormalities in cortical structure and fracture risk
Seeman, Ego. (2015) Growth and age-related abnormalities in cortical structure and fracture risk. Endocrinology and Metabolism. 30(4), pp. 419 - 428. https://doi.org/10.3803/EnM.2015.30.4.419
Identification of MicroRNAs linked to regulators of muscle protein synthesis and regeneration in young and old skeletal muscle
Zacharewicz, Evelyn, Della Gatta, P. A., Reynolds, John, Garnham, Andrew, Crowley, Tamsyn, Russell, Andrew and Lamon, Séverine. (2014) Identification of MicroRNAs linked to regulators of muscle protein synthesis and regeneration in young and old skeletal muscle. PLoS ONE. 9(12), pp. 1 - 25. https://doi.org/10.1371/journal.pone.0114009
Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise
Stefanetti, Renae J., Zacharewicz, Evelyn, Della Gatta, Paul A., Garnham, Andrew, Russell, Aaron P. and Lamon, Séverine. (2014) Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Frontiers in Physiology. 5, pp. 1 - 10. https://doi.org/10.3389/fphys.2014.00030
High-resolution in vivo imaging of bone and joints: a window to microarchitecture
Geusens, P., Geusens, P., Chapurlat, Roland D., Chapurlat, Roland D., Schett, G., Ghasem-Zadeh, Ali, Ghasem-Zadeh, Ali, Seeman, Ego, De Jong, J. and Van Den Bergh, J.. (2014) High-resolution in vivo imaging of bone and joints: a window to microarchitecture. Nature Reviews Rheumatology. 10(5), pp. 304 - 313. https://doi.org/10.1038/nrrheum.2014.23
Effect of exercise training on skeletal muscle cytokine expression in the elderly
Della Gatta, Paul A., Garnham, Andrew P., Peake, Jonathan M. and Cameron-Smith, David. (2014) Effect of exercise training on skeletal muscle cytokine expression in the elderly. Brain, Behavior, and Immunity. 39, pp. 80 - 86. https://doi.org/10.1016/j.bbi.2014.01.006
A new method of segmentation of compact-appearing, transitional and trabecular compartments and quantification of cortical porosity from high resolution peripheral quantitative computed tomographic images
Zebaze, Roger M., Ghasem-Zadeh, Ali, Mbala, A. and Seeman, Ego. (2013) A new method of segmentation of compact-appearing, transitional and trabecular compartments and quantification of cortical porosity from high resolution peripheral quantitative computed tomographic images. Bone. 54(1), pp. 8 - 20. https://doi.org/10.1016/j.bone.2013.01.007
Teriparatide improves bone quality and healing of atypical femoral fractures associated with bisphosphonate therapy
Chiang, Cherie Ying, Zebaze, Roger M.D., Ghasem-Zadeh, Ali, Iuliano-Burns, Sandra, Hardidge, Andrew and Seeman, Ego. (2013) Teriparatide improves bone quality and healing of atypical femoral fractures associated with bisphosphonate therapy. Bone. 52(1), pp. 360 - 365. https://doi.org/10.1016/j.bone.2012.10.006
Effect of exercise on the skeletal muscle proteome in patients with type 2 diabetes
Hussey, Sophie E., Sharoff, Carrie G., Garnham, Andrew, Yi, Zhengping, Bowen, Benjamin P., Mandarino, Lawrence J. and Hargreaves, Mark. (2013) Effect of exercise on the skeletal muscle proteome in patients with type 2 diabetes. Medicine and Science in Sports and Exercise. 45(6), pp. 1069 - 1076. https://doi.org/10.1249/MSS.0b013e3182814917
Preexercise aminoacidemia and muscle protein synthesis after resistance exercise
Burke, Louise, Hawley, John, Ross, M, Moore, Daniel, Phillips, S, Slater, G, Stellingwerff, T, Tipton, K, Garnham, A and Coffey, Vernon. (2012) Preexercise aminoacidemia and muscle protein synthesis after resistance exercise. Medicine and Science in Sports and Exercise. 44(10), pp. 1968 - 1977. https://doi.org/10.1249/MSS.0b013e31825d28fa
Early inflammatory and myogenic responses to resistance exercise in the elderly
Mathers, Jessica L., Farnfield, Michelle M., Garnham, Andrew P., Caldow, Marissa K., Cameron-Smith, David and Peake, Jonathan M.. (2012) Early inflammatory and myogenic responses to resistance exercise in the elderly. Muscle & Nerve. 46(3), pp. 407 - 412. https://doi.org/10.1002/mus.23317
Evaluation of the MAIIA dipstick test to detect recombinant human erythropoietin in plasma
Ashenden, Michael, Sharpe, Ken, Garnham, Andrew and Gore, Christopher J.. (2012) Evaluation of the MAIIA dipstick test to detect recombinant human erythropoietin in plasma. Journal of Pharmaceutical and Biomedical Analysis. 67-68, pp. 123 - 128. https://doi.org/10.1016/j.jpba.2012.04.025
Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion
Farnfield, Michelle M., Breen, Leigh, Carey, Kate A., Garnham, Andrew and Cameron-Smith, David. (2012) Activation of mTOR signalling in young and old human skeletal muscle in response to combined resistance exercise and whey protein ingestion. Applied Physiology, Nutrition and Metabolism. 37(1), pp. 21 - 30. https://doi.org/10.1139/H11-132
Predictors of new and severe vertebral fractures: Results from the HoRIZoN Pivotal Fracture Trial
Wustrack, R., Seeman, Ego, Bucci-Rechtweg, C. and Burch, S.. (2012) Predictors of new and severe vertebral fractures: Results from the HoRIZoN Pivotal Fracture Trial. Osteoporosis International. 23(1), pp. 53 - 58. https://doi.org/10.1007/s00198-011-1664-4
Low muscle glycogen concentration does not suppress the anabolic response to resistance exercise
Camera, Donny, West, D, Burd, N, Phillips, S, Garnham, A, Hawley, John and Coffey, Vernon. (2012) Low muscle glycogen concentration does not suppress the anabolic response to resistance exercise. Journal of Applied Physiology. 113(2), pp. 206 - 214. https://doi.org/10.1152/japplphysiol.00395.2012
Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints
Coffey, Vernon, Moore, Daniel, Burd, N, Rerecich, T, Stellingwerff, T, Garnham, A, Phillips, S and Hawley, John. (2011) Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. European Journal of Applied Physiology. 111(7), pp. 1473 - 1483. https://doi.org/10.1007/s00421-010-1768-0
The effect of acute exercise on undercarboxylated osteocalcin in obese men
Levinger, Itamar, Zebaze, Roger M., Jeru, G., Hare, David L., Selig, Steve and Seeman, Ego. (2011) The effect of acute exercise on undercarboxylated osteocalcin in obese men. Osteoporosis International. 22(5), pp. 1621 - 1626. https://doi.org/10.1007/s00198-010-1370-7
Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men
Trenerry, Marissa K., Della Gatta, Paul A., Larsen, Amy E., Garnham, Andrew P. and Cameron-Smith, David. (2011) Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men. Muscle & Nerve. 43(3), pp. 385 - 392. https://doi.org/10.1002/mus.21875
Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men
Trenerry, Melissa K., Della Gatta, Paul A., Larson, Amy E. and Garnham, Andrew P.. (2011) Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men. Muscle & Nerve. 43(3), pp. 385 - 392. https://doi.org/10.1002/mus.21875
Vitamin D status and musculoskeletal health in adolescent male ballet dancers a pilot study
Ducher, Gaele, Kukuljan, Sonja, Hill, B., Garnham, Andrew P., Nowson, Carol A., Kimlin, M. G. and Cook, Jill. (2011) Vitamin D status and musculoskeletal health in adolescent male ballet dancers a pilot study. Journal of Dance Medicine and Science. 15(3), pp. 99 - 107.
Teriparatide therapy for osteonecrosis of the jaw REPLY
Cheung, Ada S. and Seeman, Ego. (2011) Teriparatide therapy for osteonecrosis of the jaw REPLY. New England Journal of Medicine. 364, pp. 1081 - 1082. https://doi.org/10.1056/NEJMc1100730
Current markers of the Athlete Blood Passport do not flag microdose EPO doping
Ashenden, Michael, Gough, Clare E., Garnham, Andrew, Gore, Christopher J. and Sharpe, Ken. (2011) Current markers of the Athlete Blood Passport do not flag microdose EPO doping. European Journal of Applied Physiology. 111(9), pp. 2307 - 2314. https://doi.org/10.1007/s00421-011-1867-6
Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes
Hussey, Sophie E., McGee, S. L., Garnham, Andrew, Wentworth, John M., Jeukendrup, A. E. and Hargreaves, M.. (2011) Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes. Diabetes, Obesity and Metabolism. 13(10), pp. 959 - 962. https://doi.org/10.1111/j.1463-1326.2011.01426.x
Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen : Experimental Physiology-Research Paper
Yeo, W, McGee, S, Carey, A, Paton, C, Garnham, A, Hargreaves, M and Hawley, John. (2010) Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen : Experimental Physiology-Research Paper. Experimental Physiology. 95(2), pp. 351 - 358. https://doi.org/10.1113/expphysiol.2009.049353
Cytokine responses to carbohydrate ingestion during recovery from exercise-induced muscle injury
Ross, M, Halson, Shona, Suzuki, K, Garnham, A, Hawley, John, Cameron-Smith, David and Peake, J. (2010) Cytokine responses to carbohydrate ingestion during recovery from exercise-induced muscle injury. Journal of Interferon and Cytokine Research. 30(5), pp. 329 - 337. https://doi.org/10.1089/jir.2009.0079
Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle
Coffey, Vernon Glenn, Jemiolo, Bozena, Edge, Johann, Garnham, Andrew P., Trappe, Scott W. and Hawley, John Alan. (2009) Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle. American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 297(5), pp. 1441 - 1451. https://doi.org/10.1152/ajpregu.00351.2009
Festschrift to honor Professor Pierre D. Delmas
Seeman, E., Lindsay, R. and Kanis, J. A.. (2009) Festschrift to honor Professor Pierre D. Delmas. Osteoporosis International. 20(Supplement 3), pp. S231 - S233. https://doi.org/10.1007/s00198-008-0811-z
Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle
Coffey, Vernon Glenn, Pilegaard, Henriette, Garnham, Andrew P., O'Brien, Brendan J. and Hawley, John Alan. (2009) Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. Journal of Applied Physiology. 106(4), pp. 1187 - 1197. https://doi.org/10.1152/japplphysiol.91221.2008
Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens
Yeo, Wee Kian, Paton, Carl D., Garnham, Andrew P., Burke, Louise M., Carey, Andrew L. and Hawley, John Alan. (2008) Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. Journal of Applied Physiology. 105(5), pp. 1462 - 1470. https://doi.org/10.1152/japplphysiol.90882.2008
Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans
Yeo, Wee Kian, Lessard, Sarah J., Chen, Zhi-Ping, Garnham, Andrew P., Burke, Louise, Rivas, Donato A., Kemp, Bruce Ernest and Hawley, John Alan. (2008) Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. Journal of Applied Physiology. 105(5), pp. 1519 - 1526. https://doi.org/10.1152/japplphysiol.90540.2008
Bone fragility in men - Where are we?
Seeman, Ego, Bianchi, Georges, Khosla, Sundeep, Kanis, John and Orwoll, E. (2006) Bone fragility in men - Where are we? Osteoporosis International. 17(11), pp. 1577 - 1583. https://doi.org/10.1007/s00198-006-0160-8