Dimorphic Mechanisms of Fragility in Diabetes Mellitus: the Role of Reduced Collagen Fibril Deformation.
advanced glycation end-products
bone quality
collagen deformation
cortical bone
diabetes mellitus
Journal
Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research
ISSN: 1523-4681
Titre abrégé: J Bone Miner Res
Pays: United States
ID NLM: 8610640
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
25
08
2022
received:
10
10
2021
accepted:
10
09
2022
pubmed:
17
9
2022
medline:
30
11
2022
entrez:
16
9
2022
Statut:
ppublish
Résumé
Diabetes mellitus (DM) is an emerging metabolic disease, and the management of diabetic bone disease poses a serious challenge worldwide. Understanding the underlying mechanisms leading to high fracture risk in DM is hence of particular interest and urgently needed to allow for diagnosis and treatment optimization. In a case-control postmortem study, the whole 12th thoracic vertebra and cortical bone from the mid-diaphysis of the femur from male individuals with type 1 diabetes mellitus (T1DM) (n = 6; 61.3 ± 14.6 years), type 2 diabetes mellitus (T2DM) (n = 11; 74.3 ± 7.9 years), and nondiabetic controls (n = 18; 69.3 ± 11.5) were analyzed with clinical and ex situ imaging techniques to explore various bone quality indices. Cortical collagen fibril deformation was measured in a synchrotron setup to assess changes at the nanoscale during tensile testing until failure. In addition, matrix composition was analyzed including determination of cross-linking and non-crosslinking advanced glycation end-products like pentosidine and carboxymethyl-lysine. In T1DM, lower fibril deformation was accompanied by lower mineralization and more mature crystalline apatite. In T2DM, lower fibril deformation concurred with a lower elastic modulus and tendency to higher accumulation of non-crosslinking advanced glycation end-products. The observed lower collagen fibril deformation in diabetic bone may be linked to altered patterns mineral characteristics in T1DM and higher advanced glycation end-product accumulation in T2DM. © 2022 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).
Substances chimiques
Glycation End Products, Advanced
0
Collagen
9007-34-5
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2259-2276Informations de copyright
© 2022 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).
Références
Lin X, Xu Y, Pan X, et al. Global, regional, and national burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Sci Rep. 2020;10(5):14790.
Alzaid A, de Guevara PL, Beillat M, Lehner V, Atanasov P. Burden of disease and costs associated with type 2 diabetes in emerging and established markets: systematic review analyses. Expert Rev Pharmacoecon Outcomes Res. 2021;21(4):785-798.
Guntur AJ, Rosen CJ. NIH public access. Endocr Pract. 2012;18(5):758-762.
Napoli N, Strotmeyer ES, Ensrud KE, et al. Fracture risk in diabetic elderly men: the MrOS study. Diabetologia. 2014;57(10):2057-2065.
Janghorbani M, Feskanich D, Willett WC, Hu F. Prospective study of diabetes and risk of hip fracture: the nurses' health study. Diabetes Care. 2006;29(7):1573-1578.
Jiao H, Xiao E, Graves DT. Diabetes and its effect on bone and fracture healing. Curr Osteoporos Rep. 2015;13(5):327-335.
Martinez-Laguna D, Nogues X, Abrahamsen B, et al. Excess of all-cause mortality after a fracture in type 2 diabetic patients: a population-based cohort study. Osteoporos Int. 2017;28(9):2573-2581.
Starup-Linde J, Hygum K, Harsløf T, Langdahl B. Type 1 diabetes and bone fragility: links and risks. Diabetes Metab Syndr Obes. 2019;12:2539-2547.
Russo GT, Giandalia A, Romeo EL, et al. Fracture risk in type 2 diabetes: current perspectives and gender differences. Int J Endocrinol. 2016;2016:1615735.
Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - a meta-analysis. Osteoporos Int. 2007;18(4):427-444.
Moayeri A, Mohamadpour M, Mousavi SF, Shirzadpour E, Mohamadpour S, Amraei M. Fracture risk in patients with type 2 diabetes mellitus and possible risk factors: a systematic review and meta-analysis. Ther Clin Risk Manag. 2017;13:455-468.
Patsch JM, Burghardt AJ, Yap SP, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res. 2013;28(2):313-324.
Shanbhogue VV, Hansen S, Frost M, et al. Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with type 1 diabetes mellitus. J Bone Miner Res. 2015;30(12):2188-2199.
Schwartz AV, Vittinghoff E, Bauer DC, et al. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA. 2011;305(21):2184-2192.
Hofbauer LC, Busse B, Eastell R, et al. Bone fragility in diabetes: novel concepts and clinical implications. Lancet Diabetes Endocrinol. 2022;10(3):207-220.
Zimmermann EA, Schaible E, Bale H, et al. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci U S A. 2011;108(35):14416-14421.
Gupta HS, Wagermaier W, Zickler GA, et al. Nanoscale deformation mechanisms in bone. Nano Lett. 2005;5(10):2108-2111.
Schwartz AV, Garnero P, Hillier TA, et al. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metabol. 2009;94(7):2380-2386.
Hunt HB, Torres AM, Palomino PM, et al. Altered tissue composition, microarchitecture, and mechanical performance in cancellous bone from men with type 2 diabetes mellitus. J Bone Miner Res. 2019;34(7):1191-1206.
Wölfel EM, Jähn-Rickert K, Schmidt FN, et al. Individuals with type 2 diabetes mellitus show dimorphic and heterogeneous patterns of loss in femoral bone quality. Bone. 2020;140(March):115556. https://doi.org/10.1016/j.bone.2020.115556.
Farlay D, Armas LAG, Gineyts E, Akhter MP, Recker RR, Boivin G. Nonenzymatic glycation and degree of mineralization are higher in bone from fractured patients with type 1 diabetes mellitus. J Bone Miner Res. 2016;31(1):190-195.
Karim L, Moulton J, van Vliet M, et al. Bone microarchitecture, biomechanical properties, and advanced glycation end-products in the proximal femur of adults with type 2 diabetes. Bone. 2018;114:32-39. https://doi.org/10.1016/j.bone.2018.05.030.
Thomas CJ, Cleland TP, Sroga GE, Vashishth D. Accumulation of carboxymethyl-lysine (CML) in human cortical bone. Bone. 2018;110:128-133.
Dhaliwal R, Ewing SK, Vashishth D, Semba RD, Schwartz AV. Greater carboxy-methyl-lysine is associated with increased fracture risk in type 2 diabetes. J Bone Miner Res. 2022;37(2):265-272.
Scheijen JLJM, Schalkwijk CG. Quantification of glyoxal, methylglyoxal and 3-deoxyglucosone in blood and plasma by ultra performance liquid chromatography tandem mass spectrometry: evaluation of blood specimen. Clin Chem Lab Med. 2014;52(1):85-91.
Tice MJL, Bailey S, Sroga GE, Gallagher EJ, Vashishth D. Non-obese mkr mouse model of type 2 diabetes reveals skeletal alterations in mineralization and material properties. JBMR Plus. 2022;6(2):e10583.
Holzer G, von Skrbensky G, Holzer LA, Pichl W. Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res. 2009;24(3):468-474.
Napoli N, Conte C, Eastell R, et al. Bone turnover markers do not predict fracture risk in type 2 diabetes. J Bone Miner Res. 2020;35(12):2363-2371.
Manavalan JS, Cremers S, Dempster DW, et al. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metabol. 2012;97(9):3240-3250.
Krakauer JC, McKenna MJ, Buderer NF, Sudhaker Rao D, Whitehouse FW, Parfitt MA. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7):775-782.
Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001;28(2):195-201.
Burghardt AJ, Issever AS, Schwartz AV, et al. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metabol. 2010;95(11):5045-5055.
Briggs AM, Wark JD, Kantor S, Fazzalari NL, Greig AM, Bennell KL. Bone mineral density distribution in thoracic and lumbar vertebrae: an ex vivo study using dual energy X-ray absorptiometry. Bone. 2006;38(2):286-288.
Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. 2010;47(3):519-528.
Zimmermann EA, Schaible E, Gludovatz B, et al. Intrinsic mechanical behavior of femoral cortical bone in young, osteoporotic and bisphosphonate- treated individuals in low- and high energy fracture conditions. Sci Rep. 2016;6:21072. https://doi.org/10.1038/srep21072.
Granke M, Does MD, Nyman JS. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int. 2015;97(3):292-307.
Lucksanasombool P, Higgs WAJ, Higgs RJED, Swain MV. Fracture toughness of bovine bone: influence of orientation and storage media. Biomaterials. 2001;22(23):3127-3132.
Hexemer A, Bras W, Glossinger J, et al. A SAXS/WAXS/GISAXS beamline with multilayer monochromator. J Phys Conf Ser. 2010;247:1-11.
Ilavsky J. Nika: software for two-dimensional data reduction. J Appl Crystallogr. 2012;45(2):324-328.
Roschger P, Fratzl P, Eschberger J, Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone. 1998;23(4):319-326.
Milovanovic P, Zimmermann EA, Riedel C, et al. Multi-level characterization of human femoral cortices and their underlying osteocyte network reveal trends in quality of young, aged, osteoporotic and antiresorptive-treated bone. Biomaterials. 2015;45:46-55.
Schmidt FN, Zimmermann EA, Campbell GM, et al. Assessment of collagen quality associated with non-enzymatic cross-links in human bone using Fourier-transform infrared imaging. Bone. 2017;97:243-251. https://doi.org/10.1016/j.bone.2017.01.015.
Paschalis EP, Gamsjaeger S, Tatakis DN, Hassler N, Robins SP, Klaushofer K. Fourier transform infrared spectroscopic characterization of mineralizing type I collagen enzymatic trivalent cross-links. Calcif Tissue Int. 2014;96(1):18-29.
Paschalis EP, Mendelsohn R, Boskey AL. Infrared assessment of bone quality: a review. Clin Orthop Relat Res. 2011;469(8):2170-2178.
Arakawa S, Suzuki R, Kurosaka D, Ikeda R. Mass spectrometric quantitation of AGEs and enzymatic crosslinks in human cancellous bone. Sci Rep. 2020;10(18774):1-12.
Martens RJH, Broers NJH, Canaud B, et al. Relations of advanced glycation endproducts and dicarbonyls with endothelial dysfunction and low-grade inflammation in individuals with end-stage renal disease in the transition to renal replacement therapy: a cross- sectional observational study. PLoS One. 2019;14(8):e0221058.
Scheijen JLJM, van de Waarenburg MPH, Stehouwer CDA, Schalkwijk CG. Measurement of pentosidine in human plasma protein by a single-column high-performance liquid chromatography method with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci. 2009;877(7):610-614.
Viguet-Carrin S, Gineyts E, Bertholon C, Delmas PD. Simple and sensitive method for quantification of fluorescent enzymatic mature and senescent crosslinks of collagen in bone hydrolysate using single-column high performance liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci. 2009;877(1-2):1-7.
Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. 2017;13(4):208-219.
Janghorbani M, van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495-505.
Schwartz AV. Diabetes mellitus: does it affect bone? Calcif Tissue Int. 2003;73(6):515-519.
Gao H. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int J Fract. 2006;138(1-4):101-137.
Zimmermann EA, Riedel C, Schmidt FN, et al. Mechanical competence and bone quality develop during skeletal growth. J Bone Miner Res. 2019;34(8):1461-1472.
Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci U S A. 2006;103(47):17741-17746.
Acevedo C, Sylvia M, Schaible E, et al. Contributions of material properties and structure to increased bone fragility for a given bone mass in the UCD-T2DM rat model of type 2 diabetes. J Bone Miner Res. 2018;33(6):1066-1075.
Simmons ED, Pritzker KPH, Grynpas MD. Age-related changes in the human femoral cortex. J Orthoped Res. 1991;9(2):155-167.
Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195-214.
Saito M, Kida Y, Kato S, Marumo K. Diabetes, collagen, and bone quality. Curr Osteoporos Rep. 2014;12(2):181-188.
Nyman JS, Reyes M, Wang X. Effect of ultrastructural changes on the toughness of bone. Micron. 2005;36(7-8):566-582.
Sihota P, Yadav RN, Dhaliwal R, et al. Investigation of mechanical, material, and compositional determinants of human trabecular bone quality in type 2 diabetes. J Clin Endocrinol Metab. 2021;106(5):E2271-E2289.
Barzilay JI, Bůžková P, Zieman SJ, et al. Circulating levels of carboxy-methyl-lysine (CML) are associated with hip fracture risk: the cardiovascular health study. J Bone Miner Res. 2014;29(5):1061-1066.
Lamb LS, Alfonso H, Norman PE, et al. Advanced glycation end products and Esrage are associated with bone turnover and incidence of hip fracture in older men. J Clin Endocrinol Metab. 2018;103(11):4224-4231.
Valderrábano RJ, Linares MI. Diabetes mellitus and bone health: epidemiology, etiology and implications for fracture risk stratification. Clin Diabetes Endocrinol. 2018;4(9):1-8.
Rey C, Combes C, Drouet C, et al. Surface properties of biomimetic nanocrystalline apatites: applications in biomaterials. Progress in Crystal Growth and Characterization of Materials. 2014;60(3-4):63-73.
Piccoli A, Cannata F, Strollo R, et al. Sclerostin regulation, microarchitecture, and advanced glycation end-products in the bone of elderly women with type 2 diabetes. J Bone Miner Res. 2020;35(12):2415-2422.