Relation of the protein glycation, oxidation and nitration to the osteocalcin level in obese subjects

• Authors: Urszula Razny , Joanna Goralska , Anna Zdzienicka , Danuta Fedak , Jinit Masania , Naila Rabbani , Paul Thornalley , Dorota Pawlica-Gosiewska , Katarzyna Gawlik , Aldona Dembinska-Kiec , Bogdan Solnica , Malgorzata Malczewska-Malec
• Languages of publication: EN

Abstracts

EN

Carboxylated osteocalcin (Gla-OC) contributes to the bone formation, whereas its undercarboxylated form (Glu-OC) takes part in the energy metabolism. In vitro studies had shown that treatment of osteoblast-like cells with advanced glycation end product-modified bovine serum resulted in reduced synthesis of collagen 1 and osteocalcin. The aim of this study was to find association between Gla-OC and markers of protein glycation, oxidation and nitration, as well as pro-inflammatory and antioxidant defense markers in obese subjects. Non-obese [(body mass index (BMI)<30 kg/m; n=34)] and obese subjects (30

Keywords

EN

advanced glycation end products; oxidative stress; obesity; osteocalcin

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2017
• Volume: 64
• Issue: 3
• Pages: 415-422

Dates

published

2017

received

2017-03-23

revised

2017-06-14

accepted

2017-06-19

(unknown)

2017-07-28

Contributors

author

Urszula Razny

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Joanna Goralska

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Anna Zdzienicka

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Danuta Fedak

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Jinit Masania

• Warwick Medical School University of Warwick, Clinical Sciences Research Laboratories, University Hospital, Coventry CV2 2DX, Warwick, United Kingdom

author

Naila Rabbani

• Warwick Medical School University of Warwick, Clinical Sciences Research Laboratories, University Hospital, Coventry CV2 2DX, Warwick, United Kingdom

author

Paul Thornalley

• Warwick Medical School University of Warwick, Clinical Sciences Research Laboratories, University Hospital, Coventry CV2 2DX, Warwick, United Kingdom

author

Dorota Pawlica-Gosiewska

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Katarzyna Gawlik

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Aldona Dembinska-Kiec

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Bogdan Solnica

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

author

Malgorzata Malczewska-Malec

• Department of Clinical Biochemistry, Jagiellonian University Medical College, Kraków, Poland

References

• Alikhani M, Alikhani Z, Boyd C, MacLellan CM, Raptis M, Liu R, Pischon N, Trackman PC, Gerstenfeld L, Graves DT (2007) Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40: 345-353.
• Alva AS, Gultekin SH, Baehrecke EH (2004) Autophagy in human tumors: cell survival or death? Cell Death Differ 11: 1046-1048. doi: 10.1038/sj.cdd.4401445.
• de Andrade IS, Zemdegs JC, Souza DA, Watanabe RL, Telles MM, Nascimento CM, Oyama LM, Ribeiro EB (2015) Diet-induced obesity impairs hypothalamic glucose sensing but not glucose hypothalamic extracellular levels, as measured by microdialysis. Nutr Diabetes 5: e162. doi: 10.1038/nutd.2015.1.
• Beisswenger BG, Delucia EM, Lapoint N, Sanford RJ, Beisswenger PJ (2005) Ketosis leads to increased methylglyoxal production on the Atkins diet. Ann N Y Acad Sci 1043: 201-210.
• Buetler TM, Leclerc E, Baumeyer A, Latado H, Newell J, Adolfsson O, Parisod V, Richoz J, Maurer S, Foata F, Piguet D, Junod S, Heizmann CW, Delatour T (2008) N(epsilon)-carboxymethyllysine-modified proteins are unable to bind to RAGE and activate an inflammatory response. Mol Nutr Food Res 52: 370-378. doi: 10.1002/mnfr.200700101.
• Cai Z, Yan LJ (2013) Protein oxidative modifications: beneficial roles in disease and health. J Biochem Pharmacol Res 1: 15-26.
• Dobler D, Ahmed N, Song LJ, Eboigbodin KE, Thornalley PJ (2006) Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes 55: 1961-1969. doi: 10.2337/db05-1634.
• Dowd TL, Rosen JF, Mints L, Gundberg CM (2001) The effect of Pb(2+) on the structure and hydroxyapatite binding properties of osteocalcin. Biochim Biophys Acta 1535: 153-163.
• Dowd TL, Rosen JF, Li L, Gundberg CM (2003) The three-dimensional structure of bovine calcium ion-bound osteocalcin using 1H NMR spectroscopy. Biochemistry 42: 7769-7779.
• Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100: 197-207.
• Erbersdobler HF, Faist V (2001) Metabolic transit of Amadori products. Nahrung 45: 177-181.
• Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G (2010) Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142: 296-308. doi: 10.1016/j.cell.2010.06.003.
• Ferron M, McKee MD, Levine RL, Ducy P, Karsenty G (2012) Intermittent injections of osteocalcin improve glucose metabolism and prevent type 2 diabetes in mice. Bone 50: 568-575. doi: 10.1016/j.bone.2011.04.017.
• Ferron M, Lacombe J (2014) Regulation of energy metabolism by the skeleton: osteocalcin and beyond. Arch Biochem Biophys 561: 137-146. doi: 10.1016/j.abb.2014.05.022.
• Forbes JM, Cowan SP, Andrikopoulos S, Morley AL, Ward LC, Walker KZ, Cooper ME, Coughlan MT (2013) Glucose homeostasis can be differentially modulated by varying individual components of a western diet. J Nutr Biochem 24: 1251-1257. doi: 10.1016/j.jnutbio.2012.09.009.
• Franke S, Rüster C, Pester J, Hofmann G, Oelzner P, Wolf G (2011) Advanced glycation end products affect growth and function of osteoblasts. Clin Exp Rheumatol 29: 650-660.
• Gaens KH, Goossens GH, Niessen PM, van Greevenbroek MM, van der Kallen CJ, Niessen HW, Rensen SS, Buurman WA, Greve JW, Blaak EE, van Zandvoort MA, Bierhaus A, Stehouwer CD, Schalkwijk CG (2014) Nε-(carboxymethyl)lysine-receptor for advanced glycation end product axis is a key modulator of obesity-induced dysregulation of adipokine expression and insulin resistance. arteriosclerosis. Arterioscler Thromb Vasc Biol 34: 1199-1208. doi: 10.1161/ATVBAHA.113.302281.
• Godfrey L, Yamada-Fowler N, Smith JA, Thornalley PJ, Rabbani N (2014) Arginine-directed glycation and decreased HDL plasma concentration and functionality. Nutr Diabetes 4: e134. doi: 10.1038/nutd.2014.3.
• Hauschka PV, Carr SA (1982) Calcium-dependent alpha-helical structure in osteocalcin. Biochemistry 21: 2538-2547.
• Hauschka PV, Lian JB, Cole DE, Gundberg CM (1989) Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev 69: 990-1047.
• Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2011) Serum undercarboxylated osteocalcin was inversely associated with plasma glucose level and fat mass in type 2 diabetes mellitus. Osteoporos Int 22: 187-194. doi: 10.1007/s00198-010-1184-7.
• Kanazawa I (2015) Osteocalcin as a hormone regulating glucose metabolism World J Diabetes 6: 1345-1354. doi: 10.4239/wjd.v6.i18.1345.
• Kaneshiro S, Ebina K, Shi K, Higuchi C, Hirao M, Okamoto M, Koizumi K, Morimoto T, Yoshikawa H, Hashimoto J (2014) IL-6 negatively regulates osteoblast differentiation through the SHP2/MEK2 and SHP2/Akt2 pathways in vitro. J Bone Miner Metab 32: 378-392. doi: 10.1007/s00774-013-0514-1.
• Keaney JF, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ; Framingham Study (2003) Obesity and systemic oxidative stress clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 23: 434-439.
• Korda M, Kubant R, Patton S, Malinski T (2008) Leptin-induced endothelial dysfunction in obesity. Am J Physiol Heart Circ Physiol 295: H1514-H1521. doi: 10.1152/ajpheart.00479.2008.
• Kruger MC, Booth CL, Coad J, Schollum LM, Kuhn-Sherlock B, Shearer MJ (2006) Effect of calcium fortified milk supplementation with or without vitamin K on biochemical markers of bone turnover in premenopausal women. Nutrition 22: 1120-1128.
• 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 (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130: 456-469.
• Li SY, Liu Y, Sigmon VK, McCort A, Ren J (2005) High-fat diet enhances visceral advanced glycation end products, nuclear O-Glc-Nac modification, p38 mitogen-activated protein kinase activation and apoptosis. Diabetes Obes Metab 7: 448-454. doi: 10.1111/j.1463-1326.2004.00387.x.
• Lontchi-Yimagou E, Sobngwi E, Matsha TE, Kengne AP (2013) Diabetes mellitus and inflammation. Curr Diab Rep 13: 435-444. doi: 10.1007/s11892-013-0375-y.
• Mari A, Pacini G, Murphy E, Ludvik B, Nolan JJ (2001) A model-based method for assessing insulin sensitivity from the oral glucose tolerance test. Diabetes Care 24: 539-548.
• Masania J, Malczewska-Malec M, Razny U, Goralska J, Zdzienicka A, Kiec-Wilk B, Gruca A, Stancel-Mozwillo J, Dembinska-Kiec A, Rabbani N, Thornalley PJ (2016) Dicarbonyl stress in clinical obesity. Glycoconj J 33: 581-589. doi: 10.1007/s10719-016-9692-0.
• Matusik P, Prokopowicz Z, Norek B, Olszanecka-Glinianowicz M, Chudek J, Malecka-Tendera E (2005) Oxidative/Antioxidative status in obese and sport trained children: a comparative study. Biomed Res Int 2015: 315747. doi: 10.1155/2015/315747.
• Meng HZ, Zhang WL, Liu F, Yang MW (2015) Advanced glycation end products affect osteoblast proliferation and function by modulating autophagy via the receptor of advanced glycation end products/raf protein/mitogen-activated protein kinase/extracellular signal-regulated kinase kinase/extracellular signal-regulated kinase (RAGE/Raf/MEK/ERK) pathway. J Biol Chem 290: 28189-28199. doi: 10.1074/jbc.M115.669499.
• Mercer N, Ahmed H, Etcheverry SB, Vasta GR, Cortizo AM (2007) Regulation of advanced glycation end product (AGE) receptors and apoptosis by AGEs in osteoblast-like cells. Mol Cell Biochem 306: 87-94.
• Molnár D, Decsi T, Koletzko B (2004) Reduced antioxidant status in obese children with multimetabolic syndrome. Int J Obes Relat Metab Disord 28: 1197-1202. doi: 10.1038/sj.ijo.0802719.
• Nikolajczyk BS, Jagannathan-Bogdan M, Shin H, Gyurko R (2011) State of the union between metabolism and the immune system in type 2 diabetes. Genes Immun 12: 239-250. doi: 10.1038/gene.2011.1.
• Niedowicz DM, Daleke DL (2005) The role of oxidative stress in diabetic complications. Cell Biochem Biophys 43: 289-330.
• Olusi S (2002) Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans. Int J Obes Relat Metab Disord 26: 1159-1164.
• Osta B, Benedetti G, Miossec P (2014) Classical and paradoxical effects of TNF-a on bone homeostasis. Front Immunol 5: 48. doi: 10.3389/fimmu.2014.00048.
• Pi M, Chen L, Huang MZ, Zhu W, Ringhofer B, Luo J, Christenson L, Li B, Zhang J, Jackson PD, Faber P, Brunden KR, Harrington JJ, Quarles LD (2008) GPRC6A null mice exhibit osteopenia, feminization and metabolic syndrome. PLoS One 3: e3858. doi: 10.1371/journal.pone.0003858.
• Pi M, Wu Y, Quarles LD (2011) GPRC6A mediates responses to osteocalcin in β-cells in vitro and pancreas in vivo. J Bone Miner Res 26: 1680-1683. doi: 10.1002/jbmr.390.
• Platini F, Pérez-Tomás R, Ambrosio S, Tessitore L (2010) Understanding autophagy in cell death control. Curr Pharm Des 16: 101-113.
• Price PA, Rice JS, Williamson MK (1994) Conserved phosphorylation of serines in the Ser-X-Glu/Ser(P) sequences of the vitamin K-dependent matrix Gla protein from shark, lamb, rat, cow, and human. Protein Science 3: 822-830.
• Rabbani N, Godfrey L, Xue M, Shaheen F, Geoffrion M, Milne R, Thornalley PJ (2011) Glycation of LDL by methylglyoxal increases arterial atherogenicity. a possible contributor to increased risk of cardiovascular disease in diabetes. Diabetes 60: 1973-1980. doi: 10.2337/db11-0085.
• Rabbani N, Thornalley PJ (2012) Glycation research in amino acids: a place to call home. Amino Acids 42: 1087-109.
• Rabbani N, Shaheen F, Anwar A, Masania J, Thornalley PJ (2014) Assay of methylglyoxal-derived protein and nucleotide AGEs. Biochem Soc Trans 42: 511-517. doi: 10.1042/BST20140019.
• Rabbani N, Xue M, Thornalley PJ (2016) Methylglyoxal-induced dicarbonyl stress in aging and disease: first steps towards glyoxalase 1-based treatments. Clin Sci 130: 1677-1696. doi: 10.1042/CS20160025.
• Ramasamy R, Yan SF, Schmidt AM (2012) The diverse ligand repertoire of the receptor for advanced glycation endproducts and pathways to the complications of diabetes. Vascul Pharmacol 57: 160-167. doi: 10.1016/j.vph.2012.06.004.
• Razny U, Fedak D, Kiec-Wilk B, Goralska J, Gruca A, Zdzienicka A, Kiec-Klimczak M, Solnica B, Hubalewska-Dydejczyk A, Malczewska-Malec M (2017) Carboxylated and undercarboxylated osteocalcin in metabolic complications of human obesity and prediabetes. Diabetes Metab Res Rev 33 10.1002/dmrr.2862.
• Sandu O, Song K, Cai W, Zheng F, Uribarri J, Vlassara H (2005) Insulin resistance and type 2 diabetes in high-fat-fed mice are linked to high glycotoxin intake. Diabetes 54: 2314-2319.
• Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111: 305-317.
• Tanaka K, Yamaguchi T, Kaji H, Kanazawa I, Sugimoto T (2013) Advanced glycation end products suppress osteoblastic differentiation of stromal cells by activating endoplasmic reticulum stress. Biochem Biophys Res Commun 438: 463-467. doi: 10.1016/j.bbrc.2013.07.126.
• Tanaka K, Yamaguchi T, Kanazawa I, Sugimoto T (2015) Effects of high glucose and advanced glycation end products on the expressions of sclerostin and RANKL as well as apoptosis in osteocyte-like MLO-Y4-A2 cells. Biochem Biophys Res Commun 461: 193-199. doi: 10.1016/j.bbrc.2015.02.091.
• Thornalley PJ, Langborg A, Minhas HS (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 344: 109-116.
• Thornalley PJ, Rabbani N (2014) Detection of oxidized and glycated proteins in clinical samples using mass spectrometry - A user's perspective. Biochim Biophys Acta 1840: 818–829. doi: 10.1016/j.bbagen.2013.03.025.
• Unoki KH, Yamagishi S, Takeuchi M, Bujo H, Saito Y (2010) Pyridoxamine, an inhibitor of advanced glycation end product (AGE) formation ameliorates insulin resistance in obese, type 2 diabetic mice. Protein Pept Lett 17: 1177-1181. doi: 10.2174/092986610791760423.
• Wannamethee SG, Tchernova J, Whincup P, Lowe G, Kelly A, Rumley A, Wallace AM, Sattar N (2007) Plasma leptin: associations with metabolic, inflammatory and haemostatic risk factors for cardiovascular disease. Atherosclerosis 191: 418-426.
• Wei J, Hanna T, Suda N, Karsenty G, Ducy P (2014) Osteocalcin promotes β-cell proliferation during development and adulthood through Gprc6a. Diabetes 63: 1021-1031. doi: 10.2337/db13-0887.
• Weinberg E, Maymon T, Weinreb M (2014) AGEs induce caspase-mediated apoptosis of rat BMSCs via TNFalpha production and oxidative stress. J Mol Endocrinol 52: 67-76. doi: 10.1530/JME-13-0229.
• Xue M, Weickert MO, Qureshi S, Kandala NB, Anwar A, Waldron M, Shafie A, Messenger D, Fowler M, Jenkins G, Rabbani N, Thornalley PJ (2016) Improved glycemic control and vascular function in overweight and obese subjects by glyoxalase 1 inducer formulation Diabetes 65: 2282-2294. doi: 10.2337/db16-0153.
• Yamamoto T, Ozono K, Miyauchi A, Kasayama S, Kojima Y, Shima M, Okada S (2001) Role of advanced glycation end products in adynamic bone disease in patients with diabetic nephropathy. Am J Kidney Dis 38: S161-S164.
• Zhong ZM, Bai L, Chen JT (2009) Advanced oxidation protein products inhibit proliferation and differentiation of rat osteoblast-like cells via NF-kappaB pathway. Cell Physiol Biochem 24: 105-114. doi: 10.1159/000227818.

Identifiers

DOI

10.18388/abp.2017_1627