Association between changes in bioactive osteocalcin and glucose homeostasis after biliopancreatic diversion.
Bariatric surgery
Biliopancreatic diversion
Bone remodeling markers
Glucose homeostasis
Uncarboxylated osteocalcin
Journal
Endocrine
ISSN: 1559-0100
Titre abrégé: Endocrine
Pays: United States
ID NLM: 9434444
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
07
02
2020
accepted:
04
05
2020
pubmed:
19
5
2020
medline:
22
6
2021
entrez:
19
5
2020
Statut:
ppublish
Résumé
Bone may regulate glucose homeostasis via uncarboxylated bioactive osteocalcin (ucOCN). This study explored whether changes in ucOCN and bone remodeling are associated with change in glucose homeostasis after biliopancreatic diversion (BPD). In this secondary exploratory analysis of a 1-year prospective observational study, 16 participants (11 men/5 women; 69% with type 2 diabetes; mean BMI 49.4 kg/m ucOCN was unchanged at 3 days but increased dramatically at 3 months (+257%) and 12 months (+498%). Change in ucOCN correlated significantly with change in CTX at 3 months (r = 0.62, p = 0.015) and 12 months (r = 0.64, p = 0.025) before adjustment for weight loss. It also correlated significantly with change in fasting insulin (r = -0.53, p = 0.035), HOMA-IR (r = -0.54, p = 0.033) and SI (r = 0.52, p = 0.041) at 3 days, and ADIPO-IR (r = -0.69, p = 0.003) and HbA The increase in ucOCN may be associated with the improvement in insulin resistance after BPD, independently of weight loss. These findings need to be confirmed in larger, less heterogeneous populations.
Identifiants
pubmed: 32419080
doi: 10.1007/s12020-020-02340-2
pii: 10.1007/s12020-020-02340-2
doi:
Substances chimiques
Blood Glucose
0
Insulin
0
Osteocalcin
104982-03-8
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Observational Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
526-535Subventions
Organisme : Canadian Diabetes Association
ID : NC-3-17-5232-CG
Pays : International
Organisme : CIHR
ID : MOP 97947
Pays : Canada
Organisme : CIHR
ID : MOP 133652
Pays : Canada
Références
G. Mingrone, S. Panunzi, A. De Gaetano, C. Guidone, A. Iaconelli, L. Leccesi, G. Nanni, A. Pomp, M. Castagneto, G. Ghirlanda, F. Rubino, Bariatric surgery versus conventional medical therapy for type 2 diabetes. N. Engl. J. Med. 366(17), 1577–1585 (2012). https://doi.org/10.1056/NEJMoa1200111
doi: 10.1056/NEJMoa1200111
pubmed: 22449317
H. Buchwald, R. Estok, K. Fahrbach, D. Banel, M.D. Jensen, W.J. Pories, J.P. Bantle, I. Sledge, Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am. J. Med. 122(3), 248–256.e245 (2009). https://doi.org/10.1016/j.amjmed.2008.09.041
doi: 10.1016/j.amjmed.2008.09.041
pubmed: 19272486
H. Buchwald, Y. Avidor, E. Braunwald, M.D. Jensen, W. Pories, K. Fahrbach, K. Schoelles, Bariatric surgery: a systematic review and meta-analysis. JAMA 292(14), 1724–1737 (2004). https://doi.org/10.1001/jama.292.14.1724
doi: 10.1001/jama.292.14.1724
pubmed: 15479938
C. Guidone, M. Manco, E. Valera-Mora, A. Iaconelli, D. Gniuli, A. Mari, G. Nanni, M. Castagneto, M. Calvani, G. Mingrone, Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes 55(7), 2025–2031 (2006). https://doi.org/10.2337/db06-0068
doi: 10.2337/db06-0068
pubmed: 16804072
A. Michaud, T. Grenier-Larouche, D. Caron-Dorval, S. Marceau, L. Biertho, S. Simard, D. Richard, A. Tchernof, A.C. Carpentier, Biliopancreatic diversion with duodenal switch leads to better postprandial glucose level and beta cell function than sleeve gastrectomy in individuals with type 2 diabetes very early after surgery. Metab.: Clin. Exp. 74, 10–21 (2017). https://doi.org/10.1016/j.metabol.2017.06.005
doi: 10.1016/j.metabol.2017.06.005
T. Grenier-Larouche, A.M. Carreau, A. Geloen, F. Frisch, L. Biertho, S. Marceau, S. Lebel, F.S. Hould, D. Richard, A. Tchernof, A.C. Carpentier, Fatty acid metabolic remodeling during type 2 diabetes remission after bariatric surgery. Diabetes 66(11), 2743–2755 (2017). https://doi.org/10.2337/db17-0414
doi: 10.2337/db17-0414
pubmed: 28835473
T. Grenier-Larouche, A.M. Carreau, A.C. Carpentier, Early metabolic improvement after bariatric surgery: the first steps toward remission of type 2 diabetes. Can. J. Diabetes 41(4), 418–425 (2017). https://doi.org/10.1016/j.jcjd.2016.10.013
doi: 10.1016/j.jcjd.2016.10.013
pubmed: 28318939
C.E. Plourde, T. Grenier-Larouche, D. Caron-Dorval, S. Biron, S. Marceau, S. Lebel, L. Biertho, A. Tchernof, D. Richard, A.C. Carpentier, Biliopancreatic diversion with duodenal switch improves insulin sensitivity and secretion through caloric restriction. Obesity 22(8), 1838–1846 (2014). https://doi.org/10.1002/oby.20771
doi: 10.1002/oby.20771
pubmed: 24760439
C. Koliaki, S. Liatis, C.W. le Roux, A. Kokkinos, The role of bariatric surgery to treat diabetes: current challenges and perspectives. BMC Endocr. Disord. 17(1), 50 (2017). https://doi.org/10.1186/s12902-017-0202-6
doi: 10.1186/s12902-017-0202-6
pubmed: 28797248
pmcid: 5553790
G. Karsenty, M. Ferron, The contribution of bone to whole-organism physiology. Nature 481(7381), 314–320 (2012). https://doi.org/10.1038/nature10763
doi: 10.1038/nature10763
pubmed: 22258610
P. Mera, M. Ferron, I. Mosialou, Regulation of energy metabolism by bone-derived hormones. Cold Spring Harbor Perspect. Med. (2017). https://doi.org/10.1101/cshperspect.a031666
N.K. Lee, H. Sowa, E. Hinoi, M. Ferron, J.D. Ahn, C. Confavreux, R. Dacquin, P.J. Mee, M.D. McKee, D.Y. Jung, Z. Zhang, J.K. Kim, F. Mauvais-Jarvis, P. Ducy, G. Karsenty, Endocrine regulation of energy metabolism by the skeleton. Cell 130(3), 456–469 (2007). https://doi.org/10.1016/j.cell.2007.05.047
doi: 10.1016/j.cell.2007.05.047
pubmed: 17693256
pmcid: 17693256
M. Ferron, E. Hinoi, G. Karsenty, P. Ducy, Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc. Natl Acad. Sci. USA 105(13), 5266–5270 (2008). https://doi.org/10.1073/pnas.0711119105
doi: 10.1073/pnas.0711119105
pubmed: 18362359
J. Lacombe, G. Karsenty, M. Ferron, In vivo analysis of the contribution of bone resorption to the control of glucose metabolism in mice. Mol. Metab. 2(4), 498–504 (2013). https://doi.org/10.1016/j.molmet.2013.08.004
doi: 10.1016/j.molmet.2013.08.004
pubmed: 24327965
pmcid: 3854996
J. Bonneau, G. Ferland, A.D. Karelis, E. Doucet, M. Faraj, R. Rabasa-Lhoret, M. Ferron, Association between osteocalcin gamma-carboxylation and insulin resistance in overweight and obese postmenopausal women. J. Diabetes Complicat. 31(6), 1027–1034 (2017). https://doi.org/10.1016/j.jdiacomp.2017.01.023
doi: 10.1016/j.jdiacomp.2017.01.023
pubmed: 28242268
U. Razny, D. Fedak, B. Kiec-Wilk, J. Goralska, A. Gruca, A. Zdzienicka, M. Kiec-Klimczak, B. Solnica, A. Hubalewska-Dydejczyk, M. Malczewska-Malec, Carboxylated and undercarboxylated osteocalcin in metabolic complications of human obesity and prediabetes. Diabetes/Metab. Res. Rev. 33(3), (2017). https://doi.org/10.1002/dmrr.2862
Y. Takashi, M. Koga, Y. Matsuzawa, J. Saito, M. Omura, T. Nishikawa, Undercarboxylated osteocalcin can predict insulin secretion ability in type 2 diabetes. J. Diabetes Investig. 8(4), 471–474 (2017). https://doi.org/10.1111/jdi.12601
doi: 10.1111/jdi.12601
pubmed: 27889949
pmcid: 5497042
Q. Guo, H. Li, L. Xu, S. Wu, H. Sun, B. Zhou, Undercarboxylated osteocalcin reverts insulin resistance induced by endoplasmic reticulum stress in human umbilical vein endothelial cells. Sci. Rep. 7(1), 46 (2017). https://doi.org/10.1038/s41598-017-00163-2
doi: 10.1038/s41598-017-00163-2
pubmed: 28246389
pmcid: 5427815
D.M. Liu, X.Z. Guo, H.J. Tong, B. Tao, L.H. Sun, H.Y. Zhao, G. Ning, J.M. Liu, Association between osteocalcin and glucose metabolism: a meta-analysis. Osteoporos. Int. 26(12), 2823–2833 (2015). https://doi.org/10.1007/s00198-015-3197-8
doi: 10.1007/s00198-015-3197-8
pubmed: 26089135
A.F. Turcotte, T. Grenier-Larouche, R.V. Ung, D. Simonyan, A.M. Carreau, A.C. Carpentier, F. Mac-Way, L. Michou, A. Tchernof, L. Biertho, S. Lebel, S. Marceau, C. Gagnon, Effects of biliopancreatic diversion on bone turnover markers and association with hormonal factors in patients with severe obesity. Obes. Surg. 29(3), 990–998 (2019). https://doi.org/10.1007/s11695-018-3617-x
doi: 10.1007/s11695-018-3617-x
pubmed: 30478790
J. Lacombe, O. Al Rifai, L. Loter, T. Moran, A.F. Turcotte, T. Grenier-Larouche, A. Tchernof, L. Biertho, A.C. Carpentier, D. Prud'homme, R. Rabasa-Lhoret, G. Karsenty, C. Gagnon, W. Jiang, M. Ferron, Measurement of bioactive osteocalcin in humans using a novel immunoassay reveals association with glucose metabolism and beta-cell function. Am. J. Physiol. Endocrinol. Metab. 318(3), E381–E391 (2020). https://doi.org/10.1152/ajpendo.00321.2019
doi: 10.1152/ajpendo.00321.2019
pubmed: 31935114
Standards of Medical Care in Diabetes, Abridged for Primary Care Providers. Clin. Diabetes Publ. Am. Diabetes Assoc. 35(1), 5–26 (2017). https://doi.org/10.2337/cd16-0067
L. Biertho, S. Lebel, S. Marceau, F.S. Hould, F. Julien, S. Biron, Biliopancreatic diversion with duodenal switch: surgical technique and perioperative care. Surg. Clin. N. Am. 96(4), 815–826 (2016). https://doi.org/10.1016/j.suc.2016.03.012
doi: 10.1016/j.suc.2016.03.012
pubmed: 27473803
D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28(7), 412–419 (1985)
doi: 10.1007/BF00280883
E. Sondergaard, A.E. Espinosa De Ycaza, M. Morgan-Bathke, M.D. Jensen, How to measure adipose tissue insulin sensitivity. J. Clin. Endocrinol. Metab. 102(4), 1193–1199 (2017). https://doi.org/10.1210/jc.2017-00047
doi: 10.1210/jc.2017-00047
pubmed: 28323973
pmcid: 5460729
A.C. Carpentier, F. Frisch, D. Cyr, P. Genereux, B.W. Patterson, R. Giguere, J.P. Baillargeon, On the suppression of plasma nonesterified fatty acids by insulin during enhanced intravascular lipolysis in humans. Am. J. Physiol. Endocrinol. Metab. 289(5), E849–E856 (2005). https://doi.org/10.1152/ajpendo.00073.2005
doi: 10.1152/ajpendo.00073.2005
pubmed: 15972273
A. Carpentier, S.D. Mittelman, B. Lamarche, R.N. Bergman, A. Giacca, G.F. Lewis, Acute enhancement of insulin secretion by FFA in humans is lost with prolonged FFA elevation. Am. J. Physiol. 276(6 Pt 1), E1055–E1066 (1999)
pubmed: 10362618
R.N. Bergman, M. Ader, K. Huecking, G. Van Citters, Accurate assessment of beta-cell function: the hyperbolic correction. Diabetes 51(Suppl 1), S212–S220 (2002)
doi: 10.2337/diabetes.51.2007.S212
S.E. Kahn, The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 46(1), 3–19 (2003). https://doi.org/10.1007/s00125-002-1009-0
doi: 10.1007/s00125-002-1009-0
pubmed: 12637977
M. Ferron, J. Lacombe, Regulation of energy metabolism by the skeleton: osteocalcin and beyond. Arch. Biochem. Biophysics 561, 137–146 (2014). https://doi.org/10.1016/j.abb.2014.05.022
doi: 10.1016/j.abb.2014.05.022
A. Diaz-Lopez, M. Bullo, M. Juanola-Falgarona, M.A. Martinez-Gonzalez, R. Estruch, M.I. Covas, F. Aros, J. Salas-Salvado, Reduced serum concentrations of carboxylated and undercarboxylated osteocalcin are associated with risk of developing type 2 diabetes mellitus in a high cardiovascular risk population: a nested case-control study. J. Clin. Endocrinol. Metab. 98(11), 4524–4531 (2013). https://doi.org/10.1210/jc.2013-2472
doi: 10.1210/jc.2013-2472
pubmed: 24037881
K. Mori, M. Emoto, K. Motoyama, E. Lee, S. Yamada, T. Morioka, Y. Imanishi, T. Shoji, M. Inaba, Undercarboxylated osteocalcin does not correlate with insulin resistance as assessed by euglycemic hyperinsulinemic clamp technique in patients with type 2 diabetes mellitus. Diabetol. Metab. Syndr. 4(1), 53 (2012). https://doi.org/10.1186/1758-5996-4-53
doi: 10.1186/1758-5996-4-53
pubmed: 23249601
pmcid: 3565869
R. Saucedo, G. Rico, G. Vega, L. Basurto, L. Cordova, R. Galvan, M. Hernandez, E. Puello, A. Zarate, Osteocalcin, under-carboxylated osteocalcin and osteopontin are not associated with gestational diabetes mellitus but are inversely associated with leptin in non-diabetic women. J. Endocrinol. Investig. 38(5), 519–526 (2015). https://doi.org/10.1007/s40618-014-0220-4
doi: 10.1007/s40618-014-0220-4
M. Ferron, J. Wei, T. Yoshizawa, A. Del Fattore, R.A. DePinho, A. Teti, P. Ducy, G. Karsenty, Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142(2), 296–308 (2010). https://doi.org/10.1016/j.cell.2010.06.003
doi: 10.1016/j.cell.2010.06.003
pubmed: 20655470
pmcid: 2910411
B. Lee, J. Shao, Adiponectin and energy homeostasis. Rev. Endocr. Metab. Disord. 15(2), 149–156 (2014). https://doi.org/10.1007/s11154-013-9283-3
doi: 10.1007/s11154-013-9283-3
pubmed: 24170312
pmcid: 4006341
R. Ye, P.E. Scherer, Adiponectin, driver or passenger on the road to insulin sensitivity? Mol. Metab. 2(3), 133–141 (2013). https://doi.org/10.1016/j.molmet.2013.04.001
doi: 10.1016/j.molmet.2013.04.001
pubmed: 24049728
pmcid: 3773837
X. Wu, H. Motoshima, K. Mahadev, T.J. Stalker, R. Scalia, B.J. Goldstein, Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 52(6), 1355–1363 (2003)
doi: 10.2337/diabetes.52.6.1355
J.J. Cao, Effects of obesity on bone metabolism. J. Orthop. Surg. Res. 6, 30 (2011). https://doi.org/10.1186/1749-799x-6-30
doi: 10.1186/1749-799x-6-30
pubmed: 21676245
pmcid: 3141563
B.A. Gower, K. Casazza, Divergent effects of obesity on bone health. J. Clin. Densitom. 16(4), 450–454 (2013). https://doi.org/10.1016/j.jocd.2013.08.010
doi: 10.1016/j.jocd.2013.08.010
pubmed: 24063845
pmcid: 5321047
A.L. Evans, M.A. Paggiosi, R. Eastell, J.S. Walsh, Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J. Bone Miner. Res. 30(5), 920–928 (2015). https://doi.org/10.1002/jbmr.2407
doi: 10.1002/jbmr.2407
pubmed: 25400253
J.S. Walsh, T. Vilaca, Obesity, type 2 diabetes and bone in adults. Calcif. Tissue Int. 100(5), 528–535 (2017). https://doi.org/10.1007/s00223-016-0229-0
doi: 10.1007/s00223-016-0229-0
pubmed: 28280846
pmcid: 5394147
J. Wei, M. Ferron, C.J. Clarke, Y.A. Hannun, H. Jiang, W.S. Blaner, G. Karsenty, Bone-specific insulin resistance disrupts whole-body glucose homeostasis via decreased osteocalcin activation. J. Clin. Investig. 124(4), 1–13 (2014). https://doi.org/10.1172/jci72323
doi: 10.1172/jci72323
pubmed: 24642469
C. Gagnon, A.L. Schafer, Bone health after bariatric surgery. JBMR 2(3), 121–133 (2018). https://doi.org/10.1002/jbm4.10048
doi: 10.1002/jbm4.10048
C. Rousseau, S. Jean, P. Gamache, S. Lebel, F. Mac-Way, L. Biertho, L. Michou, C. Gagnon, Change in fracture risk and fracture pattern after bariatric surgery: nested case-control study. BMJ (Clin. Res. ed.) 354, i3794 (2016). https://doi.org/10.1136/bmj.i3794
doi: 10.1136/bmj.i3794
E.W. Yu, M. Wewalka, S.A. Ding, D.C. Simonson, K. Foster, J.J. Holst, A. Vernon, A.B. Goldfine, F. Halperin, Effects of gastric bypass and gastric banding on bone remodeling in obese patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 101(2), 714–722 (2016). https://doi.org/10.1210/jc.2015-3437
doi: 10.1210/jc.2015-3437
pubmed: 26600045
R. Basu, J. Peterson, R. Rizza, S. Khosla, Effects of physiological variations in circulating insulin levels on bone turnover in humans. J. Clin. Endocrinol. Metab. 96(5), 1450–1455 (2011). https://doi.org/10.1210/jc.2010-2877
doi: 10.1210/jc.2010-2877
pubmed: 21325461
pmcid: 3085206
M.M. Weivoda, C.K. Chew, D.G. Monroe, J.N. Farr, E.J. Atkinson, J.R. Geske, B. Eckhardt, B. Thicke, M. Ruan, A.J. Tweed, L.K. McCready, R.A. Rizza, A. Matveyenko, M. Kassem, T.L. Andersen, A. Vella, M.T. Drake, B.L. Clarke, M.J. Oursler, S. Khosla, Identification of osteoclast-osteoblast coupling factors in humans reveals links between bone and energy metabolism. Nat. Commun. 11(1), 87 (2020). https://doi.org/10.1038/s41467-019-14003-6
doi: 10.1038/s41467-019-14003-6
pubmed: 31911667
pmcid: 6946812
I. Mosialou, S. Shikhel, J.M. Liu, A. Maurizi, N. Luo, Z. He, Y. Huang, H. Zong, R.A. Friedman, J. Barasch, P. Lanzano, L. Deng, R.L. Leibel, M. Rubin, T. Nickolas, W. Chung, L.M. Zeltser, K.W. Williams, J.E. Pessin, S. Kousteni, MC4R-dependent suppression of appetite by bone-derived lipocalin 2. Nature 543(7645), 385–390 (2017). https://doi.org/10.1038/nature21697
doi: 10.1038/nature21697
pubmed: 28273060
pmcid: 5975642
S. Costantini, C. Conte, Bone health in diabetes and prediabetes. World J. Diabetes 10(8), 421–445 (2019). https://doi.org/10.4239/wjd.v10.i8.421
doi: 10.4239/wjd.v10.i8.421
pubmed: 31523379
pmcid: 6715571
F. Gossiel, H. Altaher, D.M. Reid, C. Roux, D. Felsenberg, C.C. Gluer, R. Eastell, Bone turnover markers after the menopause: T-score approach. Bone 111, 44–48 (2018). https://doi.org/10.1016/j.bone.2018.03.016
doi: 10.1016/j.bone.2018.03.016
pubmed: 29551751