Advanced glycation end-products and bone fractures

wbldb

Vashishth, Deepak¹

Advanced glycation end-products and bone fractures

IBMS Bonekey. August 2009;6(8):268-278

©2009 International Bone & Mineral Society

Affiliations

¹Department of Biomedical Engineering, Center of Biotechnology & Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA
Abstract and keywords

Bone does not turn over uniformly, and becomes susceptible to post-translational modification by nonenzymatic glycation (NEG). NEG of bone causes the formation of advanced glycation end-products (AGEs) and this process is accelerated with aging, diabetes and antiresorptive postmenopausal osteoporosis therapy. Due to the elevated incidence of fracture associated with aging and diabetes, several studies have attempted to measure and evaluate AGEs as biomarkers for fracture risk. Here current methods of estimating AGEs in bone by liquid chromatography and fluorometric assay are summarized and the relationships between AGEs and fracture properties at whole bone, apparent tissue and matrix levels are discussed

Keywords: Advanced glycation end-products (AGEs); Bone; Mechanical properties; Non-enzymatic glycation; Pentosidine; Toughness
Links

DOI: 10.1138/20090390

PubMed: 27158323

PubMedCentral: PMC4856156

Cited Works (28)

Year	Entry
2007	Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. April 2007;40(4):1144-1151.
2005	Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM. Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone. December 2005;37(6):825-832.
2008	Allen MR, Gineyts E, Leeming DJ, Burr DB, Delmas PD. Bisphosphonates alter trabecular bone collagen cross-linking and isomerization in beagle dog vertebra. Osteoporos Int. March 2008;19(3):329-337.
2007	Nyman JS, Roy A, Tyler JH, Acuna RL, Gayle HJ, Wang X. Age‐related factors affecting the postyield energy dissipation of human cortical bone. J Orthop Res. May 2007;25(7):646-655.
2001	Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. February 2001;28(2):195-201.
1998	Bank RA, Bayliss MT, Lafeber FPJG, Maroudas A, Tekoppele JM. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage: the age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Biochem J. February 15, 1998;3301(1):345-351.
2002	Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone [published correction appears in Bone. 2003;32(1):107]. Bone. 2002;31(1):1-7.
1996	Garnero P, Sornay‐Rendu E, Chapuy M, Delmas PD. Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J Bone Miner Res. 1996;11(3):337-349.
1998	Bailey AJ, Paul RG, Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. December 1, 1998;106(1-2):1-56.
2005	Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A. Advanced glycation end products and bone loss during aging. Annals NY Acad Sci. 2005;1043:710-717.
2006	Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. October 2006;17(10):1514-1523.
2009	Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer DC; Health, Aging, and Body Composition Study. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab. July 2009;94(7):2380-2386.
1988	Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass as predictors of fracture in a prospective study. J Clin Invest. June 1988;81(6):1804-1809.
2006	Allen MR, Iwata K, Phipps R, Burr DB. Alterations in canine vertebral bone turnover, microdamage accumulation, and biomechanical properties following 1-year treatment with clinical treatment doses of risedronate or alendronate. Bone. October 2006;39(4):872-879.
2007	Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem. February 23, 2007;282(8):5691-5703.
1993	Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14(4):595-608.
1997	Saito M, Marumo K, Fujii K, Ishioka N. Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Ciochem. November 1, 1997;253(1):26-32.
2001	Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK. Bone indentation recovery time correlates with bond reforming time. Nature. December 13, 2001;414(6865):773-776.
2006	Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, Delmas PD, Bouxsein ML. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone. November 2006;39(5):1073-1079.
1984	Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. February 13, 1984;304(1121):509-518.
2009	Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. July 2009;20(6):887-894.
2008	Keaveny TM, Bouxsein ML. Theoretical implications of the biomechanical fracture threshold. J Bone Miner Res. October 2008;23(10):1541-1547.
1975	Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg. October 1975;57A(7):956-961.
2004	Vashishth D. Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. J Biomech. June 2004;37(6):943-946.
1998	Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone. March 1998;22(3):181-187.
2003	Akkus O, Polyakova‐Akkus A, Adar F, Schaffler MB. Aging of microstructural compartments in human compact bone. J Bone Miner Res. June 2003;18(6):1012-1019.
2006	Saito M, Fujii K, Marumo K. Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tiss Int. September 2006;79(3):160-168.
2006	Saito M, Fujii K, Soshi S, Tanaka T. Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos Int. July 2006;17(7):986-995.

Cited By (35)

Year	Entry
2013	Willett TL, Sutty S, Gaspar A, Avery N, Grynpas M. In vitro non-enzymatic ribation reduces post-yield strain accommodation in cortical bone. Bone. February 2013;52(2):611-622.
2018	Karim L, Moulton J, Van Vliet M, Velie K, Robbins A, Malekipour F, Abdeen A, Ayres D, Bouxsein ML. Bone microarchitecture, biomechanical properties, and advanced glycation end-products in the proximal femur of adults with type 2 diabetes. Bone. September 2018;114:32-39.
2020	Burr DB. Fifty years of bisphosphonates: what are their mechanical effects on bone? Bone. September 2020;138:115518.
2020	Taylor EA, Donnelly E. Raman and Fourier transform infrared imaging for characterization of bone material properties. Bone. October 2020;139:115490.
2022	LLabre JE, Sroga GE, Tice MJ, Vashishth D. Induction and rescue of skeletal fragility in a high-fat diet mouse model of type 2 diabetes: an in vivo and in vitro approach. Bone. March 2022;156:116302.
2023	Pendyala M, Stephen SJ, Vashishth D, Blaber EA, Chan DD. Loss of hyaluronan synthases impacts bone morphology, quality, and mechanical properties. Bone. July 2023;172:116779.
2016	Osterhoff G, Morgan EF, Shefelbine SJ, Karim L, McNamara LM, Augat P. Bone mechanical properties and changes with osteoporosis. Injury. June 2016;47(suppl 2):S11-S20.
2021	Maghami E, Josephson TO, Moore JP, Rezaee T, Freeman TA, Karim L, Najafi AR. Fracture behavior of human cortical bone: role of advanced glycation end-products and microstructural features. J Biomech. August 26, 2021;125:110600.
2010	Shane E, Burr D, Ebeling PR, Abrahamsen B, Adler RA, Brown TD, Cheung AM, Cosman F, Curtis JR, Dell R, Dempster D, Einhorn TA, Genant HK, Geusens P, Klaushofer K, Koval K, Lane JM, McKiernan F, McKinney R, Ng A, Nieves J, O'Keefe R, Papapoulos S, Sen HT, van der Meulen MCH, Weinstein RS, Whyte M. Atypical subtrochanteric and diaphyseal femoral fractures: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. November 2010;25(11):2267-2294.
2020	Kim SH, Yi S, Yi J, Kim YM, Won YJ. Chronic kidney disease increases the risk of hip fracture: a prospective cohort study in Korean adults. J Bone Miner Res. July 2020;35(7):1313-1321.
2020	Napoli N, Conte C, Eastell R, Ewing SK, Bauer DC, Strotmeyer ES, Black DM, Samelson EJ, Vittinghoff E, Schwartz AV. Bone turnover markers do not predict fracture risk in Type 2 diabetes. J Bone Miner Res. December 2020;35(12):2363-2371.
2022	Bailey S, Stadelmann MA, Zysset PK, Vashishth D, Alkalay RN. Influence of metastatic bone lesion type and tumor origin on human vertebral bone architecture, matrix quality, and mechanical properties. J Bone Miner Res. May 2022;37(5):896-907.
2022	Buettmann EG, Goldscheitter GM, Hoppock GA, Friedman MA, Suva LJ, Donahue HJ. Similarities between disuse and age-induced bone loss. J Bone Miner Res. August 2022;37(8):1417-1434.
2022	LLabre JE, Gil C, Amatya N, Lagalwar S, Possidente B, Vashishth D. Degradation of bone quality in a transgenic mouse model of Alzheimer′s disease. J Bone Miner Res. December 2022;37(12):2548-2565.
2015	Poundarik AA, Wu P-C, Evis Z, Sroga GE, Ural A, Rubin M, Vashishth D. A direct role of collagen glycation in bone fracture. J Mech Behav Biomed Mater. December 2015;52:120-130.
2013	Karim L, Tang SY, Sroga GE, Vashishth D. Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone. Osteoporos Int. September 2013;24(9):2441-2447.
2022	Senwar B. Bone Material Quality, Structure, and Functional Relationships Contribute to Bone Strength and Toughness [Master's thesis]. University of Colorado; 2022.
2017	Matheny JB. Interactions Between Bone Remodeling and Microdamage in Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; August 2017.
2018	Torres AM. Fatigue Behavior of Cancellous Bone, Microdamage Accumulation, and Biologically Inspired Cellular Solids [PhD thesis]. Ithaca, NY: Cornell University; August 2018.
2020	Taylor EA. Validation and Implementation of Vibrational Spectroscopic Measures of Bone Composition [PhD thesis]. Ithaca, NY: Cornell University; December 2020.
2021	Tobolsky V. Energy Allocation to Adolescent Skeletal Growth: Impacts of Insulin and Physical Activity [PhD thesis]. Cambridge, MA: Harvard University; April 2021.
2016	Hammond MA. The Influence of Collagen Crosslinking and Treadmill Exercise on the Mechanics, Composition, and Morphology of Bone At Multiple Length Scales [PhD thesis]. Purdue University; May 2016.
2011	Karim L. The Biomolecular Basis of Bone Fracture [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; November 2011.
2014	Bradke BS. The Role of Cortical and Cancellous Bone Quality on Vertebral Fragility [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; April 2014.
2016	Bailey SM. The Role of Extra-Cellular Matrix Proteins and Post-Translational Modifications on Bone Fracture [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; September 2016.
2022	Pendyala M. The Interplay Between Mechanics and Joint Health: A Focus on Hyaluronan and Inflammation [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; December 2022.
2022	Tice MJL. Loss and Modulation of Bone Matrix and Fragility During Diabetes Mellitus [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; May 2022.
2021	Frank M. Mechanical Characterization of Individual Trabeculae [PhD thesis]. Vienna University of Technology; February 2021.
2012	Hardisty MR. Not Tough Enough: Why Bone Turns Pale When it Feels Stressed [PhD thesis]. Davis, CA: Davis, University of California; 2012.
2022	Schurman CA. The Role of TGFβ Mediated Osteocytic Perilacunar/canalicular Remodeling in Age-Related Bone Fragility [PhD thesis]. San Francisco, University of California; 2022.
2019	Aaronson JD. Effects of Hyperglycemia and Advanced Glycation End Products on Novel Ocy454 Osteocytes [Master's thesis]. University of Massachusetts at Dartmouth; May 2019.
2021	Hays MR. Effects of Metformin on Advanced Glycation End Product Formation in Bone Under Hyperglycemic Conditions [Master's thesis]. University of Massachusetts at Dartmouth; May 2021.
2022	Rezaee T. Effect of Clinically Relevant Alterations of Mineral and Protein on Bone Biomechanics [PhD thesis]. University of Massachusetts at Dartmouth; May 2022.
2021	Romanowicz GE. The Role of Collagen Cross-Linking in Craniofacial and Long Bone Mineralization and Healing [PhD thesis]. University of Michigan; 2021.
2020	Singleton RC. A Study of Aging in Male Cortical Bone Using Nanoindentation [PhD thesis]. Knoxville, University of Tennessee; August 2020.