The effects of acute hyperinsulinemia on bone metabolism

Endocrine Connections

Volumn 4, Issue 3, 2015, Pages 155-162

  Ivaska, Kaisa K ^a   Heliövaara, Maikki K ^b   Ebeling, Pertti ^b   Bucci, Marco ^a   Huovinen, Ville ^a,c   Kalervo Vaananen H ^a   Nuutila, Pirjo ^a,c   Koistinen, Heikki A ^b,d  

^a UNIVERSITY OF TURKU   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c TURKU UNIVERSITY HOSPITAL   (Finland)

^d MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

Author keywords

Bone; Bone turnover markers; Hyperinsulinemic clamp; Insulin; Osteocalcin

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CARBOXY TERMINAL TELOPEPTIDE; INSULIN; OSTEOCALCIN; PROCOLLAGEN; TYPE I PROPEPTIDE PROCOLLAGEN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BONE METABOLISM; FEMALE; GLYCEMIC CONTROL; HUMAN; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; MALE; NORMAL HUMAN; OSTEOLYSIS; PRIORITY JOURNAL; VITAMIN BLOOD LEVEL;

EID: 84995619808     PISSN: None     EISSN: 20493614     Source Type: Journal    
DOI: 10.1530/EC-15-0022     Document Type: Article

References (45)

1. Fukumoto S & Martin TJ. Bone as an endocrine organ. Trends in Endocrinology and Metabolism 2009 20 230-236. (doi:10.1016/j.tem. 2009.02.001).
2. Karsenty G & Ferron M. The contribution of bone to whole-organism physiology. Nature 2012 481 314-320. (doi:10.1038/nature10763).
3. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY et al. Endocrine regulation of energy metabolism by the skeleton. Cell 2007 130 456-469. (doi:10.1016/j.cell. 2007.05.047).
4. Ferron M, Hinoi E, Karsenty G & Ducy P. Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. PNAS 2008 105 5266-5270. (doi:10.1073/pnas.0711119105).
5. Hauschka PV, Lian JB, Cole DE & Gundberg CM. Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiological Reviews 1989 69 990-1047.
6. Hoang QQ, Sicheri F, Howard AJ & Yang DS. Bone recognition mechanism of porcine osteocalcin from crystal structure. Nature 2003 425 977-980. (doi:10.1038/nature02079).
7. PiM,Wu Y & Quarles LD. GPRC6A mediates responses to osteocalcin in β-cells in vitro and pancreas in vivo. Journal of Bone and Mineral Research 2011 26 1680-1683. (doi:10.1002/jbmr.390).
8. Wei J, Hanna T, Suda N, Karsenty G & Ducy P. Osteocalcin promotes β-cell proliferation during development and adulthood through Gprc6a. Diabetes 2014 63 1021-1031. (doi:10.2337/db13-0887).
9. Cornish J, Callon KE & Reid IR. Insulin increases histomorphometric indices of bone formation In vivo. Calcified Tissue International 1996 59 492-495. (doi:10.1007/BF00369216).
10. Thomas DM, Hards DK, Rogers SD, Ng KW & Best JD. Insulin receptor expression in bone. Journal of Bone and Mineral Research 1996 11 1312-1320. (doi:10.1002/jbmr.5650110916).
11. Thrailkill KM, Lumpkin CK Jr, Bunn RC, Kemp SF & Fowlkes JL. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues American Journal of Physiology. Endocrinology and Metabolism 2005 289 E735-E745. (doi:10.1152/ajpendo.00159.2005).
12. Hamann C, Kirschner S, Gunther KP & Hofbauer LC. Bone, sweet bone-osteoporotic fractures in diabetes mellitus. Nature Reviews. Endocrinology 2012 8 297-305. (doi:10.1038/nrendo.2011.233).
13. Pun KK, Lau P & Ho PW. The characterization, regulation, and function of insulin receptors on osteoblast-like clonal osteosarcoma cell line. Journal of Bone and Mineral Research 1989 4 853-862. (doi:10.1002/jbmr. 5650040610).
14. Martineau-Doize B, McKee MD, Warshawsky H & Bergeron JJ. In vivo demonstration by radioautography of binding sites for insulin in liver, kidney, and calcified tissues of the rat. Anatomical Record 1986 214 130-140. (doi:10.1002/ar.1092140205).
15. Fulzele K, DiGirolamo DJ, Liu Z, Xu J, Messina JL & Clemens TL. Disruption of the insulin-like growth factor type 1 receptor in osteoblasts enhances insulin signaling and action. Journal of Biological Chemistry 2007 282 25649-25658. (doi:10.1074/jbc.M700651200).
16. Thomas DM, Udagawa N, Hards DK, Quinn JM, Moseley JM, Findlay DM & Best JD. Insulin receptor expression in primary and cultured osteoclast-like cells. Bone 1998 23 181-186. (doi:10.1016/ S8756-3282(98)00095-7).
17. Avnet S, Perut F, Salerno M, Sciacca L & Baldini N. Insulin receptor isoforms are differently expressed during human osteoblastogenesis. Differentiation 2012 83 242-248. (doi:10.1016/j.diff.2012.02.002).
18. Zhang W, Shen X, Wan C, Zhao Q, Zhang L, ZhouQ & Deng L. Effects of insulin and insulin-like growth factor 1 on osteoblast proliferation and differentiation: differential signalling via Akt and ERK. Cell Biochemistry and Function 2012 30 297-302. (doi:10.1002/cbf.2801).
19. Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Bruning JC et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 2010 142 309-319. (doi:10.1016/j.cell.2010.06.002).
20. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P & Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 2010 142 296-308. (doi:10.1016/j.cell.2010.06.003).
21. Clemens TL & Karsenty G. The osteoblast: an insulin target cell controlling glucose homeostasis. Journal of Bone and Mineral Research 2011 26 677-680. (doi:10.1002/jbmr.321).
22. Booth SL, Centi A, Smith SR & Gundberg C. The role of osteocalcin in human glucose metabolism: marker or mediator? Nature Reviews. Endocrinology 2013 9 43-55. (doi:10.1038/nrendo.2012.201).
23. Booth SL, Centi AJ & Gundberg C. Bone as an endocrine organ relevant to diabetes. Current Diabetes Reports 2014 14 556. (doi:10.1007/s11892- 014-0556-3).
24. Motyl KJ, McCabe LR & Schwartz AV. Bone and glucose metabolism: a two-way street. Archives of Biochemistry and Biophysics 2010 503 2-10. (doi:10.1016/j.abb.2010.07.030).
25. Schwetz V, Pieber T & Obermayer-Pietsch B. The endocrine role of the skeleton: background and clinical evidence. European Journal of Endocrinology/European Federation of Endocrine Societies 2012 166 959-967. (doi:10.1530/EJE-12-0030).
26. Paldanius PM, Ivaska KK, Hovi P, Andersson S, Eriksson JG, Vaananen K, Kajantie E & Makitie O. Total and carboxylated osteocalcin associate with insulin levels in young adults born with normal or very low birth weight. PLoS ONE 2013 8 e63036. (doi:10.1371/journal.pone.0063036).
27. Lu C, Ivaska KK, Alen M, Wang Q, Tormakangas T, Xu L, Wiklund P, Mikkola TM, Pekkala S, Tian H et al. Serum osteocalcin is not associated with glucose but is inversely associated with leptin across generations of nondiabetic women. Journal of Clinical Endocrinology and Metabolism 2012 97 4106-4114. (doi:10.1210/jc.2012-2045).
28. GundbergCM, Lian JB&Booth SL. Vitamin K-dependent carboxylation of osteocalcin: friend or foe? Advances in Nutrition 2012 3 149-157. (doi:10.3945/an.112.001834).
29. DeFronzo RA, Tobin JD & Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. American Journal of Physiology 1979 237 E214-E223.
30. Clowes JA, Robinson RT, Heller SR, Eastell R & Blumsohn A. Acute changes of bone turnover and PTH induced by insulin and glucose: euglycemic and hypoglycemic hyperinsulinemic clamp studies. Journal of Clinical Endocrinology and Metabolism 2002 87 3324-3329. (doi:10.1210/jcem.87.7.8660).
31. Basu R, Peterson J, Rizza R & Khosla S. Effects of physiological variations in circulating insulin levels on bone turnover in humans. Journal of Clinical Endocrinology and Metabolism 2011 96 1450-1455. (doi:10.1210/ jc.2010-2877).
32. Levinger I, Jerums G, Stepto NK, Parker L, Serpiello FR, McConell GK, Anderson M, Hare DL, Byrnes E, Ebeling PR et al. The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men. Journal of Bone and Mineral Research 2014 29 2571-2576. (doi:10.1002/jbmr.2285).
33. Heliovaara MK, Teppo AM, Karonen SL, Tuominen JA & Ebeling P. Plasma IL-6 concentration is inversely related to insulin sensitivity, and acute-phase proteins associate with glucose and lipid metabolism in healthy subjects. Diabetes, Obesity & Metabolism 2005 7 729-736. (doi:10.1111/j.1463-1326.2004.00463.x).
34. Koistinen HA, Remitz A, Gylling H, Miettinen TA, Koivisto VA & Ebeling P. Dyslipidemia and a reversible decrease in insulin sensitivity induced by therapy with 13-cis-retinoic acid. Diabetes/Metabolism Research and Reviews 2001 17 391-395. (doi:10.1002/dmrr.222).
35. Kakonen SM, Hellman J, Karp M, Laaksonen P, Obrant KJ, Vaananen HK, Lovgren T & Pettersson K. Development and evaluation of three immunofluorometric assays that measure different forms of osteocalcin in serum. Clinical Chemistry 2000 46 332-337.
36. Paldanius PM, Ivaska KK, Hovi P, Andersson S, Vaananen HK, Kajantie E & Makitie O. The effect of oral glucose tolerance test on serum osteocalcin and bone turnover markers in young adults. Calcified Tissue International 2012 90 90-95. (doi:10.1007/s00223-011-9551-8).
37. Hellman J, Kakonen SM, Matikainen MT, Karp M, Lovgren T, Vaananen HK & Pettersson K. Epitope mapping of nine monoclonal antibodies against osteocalcin: combinations into two-site assays affect both assay specificity and sample stability. Journal of Bone and Mineral Research 1996 11 1165-1175. (doi:10.1002/jbmr.5650110816).
38. Gundberg CM, Nieman SD, Abrams S & Rosen H. Vitamin K status and bone health: an analysis of methods for determination of undercarboxylated osteocalcin. Journal of Clinical Endocrinology and Metabolism 1998 83 3258-3266. (doi:10.1210/jcem.83.9.5126).
39. Buday B, Pach FP, Literati-Nagy B, Vitai M, Vecsei Z & Koranyi L. Serum osteocalcin is associated with improved metabolic state via adiponectin in females versus testosterone in males. Gender specific nature of the bone-energy homeostasis axis. Bone 2013 57 98-104. (doi:10.1016/j. bone.2013.07.018).
40. Andrews NA. Skeletal regulation of glucose metabolism: challenges in translation from mouse to man. IBMS BoneKEy 2013 10 Article number: 353. (doi:10.1038/bonekey.2013.87).
41. Viljakainen H, Ivaska KK, Paldanius P, Lipsanen-Nyman M, Saukkonen T, Pietilainen KH, Andersson S, Laitinen K & Makitie O. Suppressed bone turnover in obesity: a link to energy metabolism? A case-control study Journal of Clinical Endocrinology and Metabolism 2014 99 2155-2163. (doi:10.1210/jc.2013-3097).
42. Nissen A, Christensen M, Knop FK, Vilsboll T, Holst JJ & Hartmann B. Glucose-dependent insulinotropic polypeptide inhibits bone resorption in humans. Journal of Clinical Endocrinology and Metabolism 2014 99 E2325-E2329. (doi:10.1210/jc.2014-2547).
43. Henriksen DB, Alexandersen P, Hartmann B, Adrian CL, Byrjalsen I, Bone HG, Holst JJ & Christiansen C. Four-month treatment with GLP-2 significantly increases hip BMD: a randomized, placebo-controlled, dose-ranging study in postmenopausal women with low BMD. Bone 2009 45 833-842. (doi:10.1016/j.bone.2009.07.008).
44. Dienelt A & zur Nieden NI. Hyperglycemia impairs skeletogenesis from embryonic stem cells by affecting osteoblast and osteoclast differentiation. Stem Cells and Development 2011 20 465-474. (doi:10.1089/scd. 2010.0205).
45. Polgreen LE, Jacobs DR Jr, Nathan BM, Steinberger J, Moran A & Sinaiko AR. Association of osteocalcin with obesity, insulin resistance, and cardiovascular risk factors in young adults. Obesity 2012 20 2194-2201. (doi:10.1038/oby.2012.108).