Abstract
In recent decades, several methods based on biochemical and molecular changes caused by aging have been proposed to improve the accuracy of forensic age estimation. The present study aimed to measure changes in furosine and pentosidine, two markers of non-enzymatic glycation of proteins (NEGs), in human dentine and clavicle with aging, and to identify possible differences between turnover rates in different mineralized tissues. Furosine and pentosidine were quantified in 32 dentine samples from living donors between 14 and 80 years of age, and in a second group of samples consisting of a tooth and a piece of clavicle collected from the same cadaver (15 individuals aged 18 to 85 years). Furosine concentration was much higher than pentosidine concentration in the same tissue, although they were strongly correlated in both dentine and bone. A close relationship between furosine and/or pentosidine content and chronological age was found in both tissues (r > 0.93). Moreover, age estimation was more accurate when furosine or pentosidine content was determined in dentine, with specificity values for the tests higher than 82% in all age groups. In clavicle, furosine concentration and pentosidine concentration were much lower (2.6-fold and 3.1-fold, respectively) than in dentine from the same individuals. In conclusion, although the results show strong correlations between chronological age and furosine or pentosidine concentrations determined in mineralized tissues, there is still a need for further research with larger data sets, including patients with diabetes.
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Cunha E, Baccino E, Martrille L, Ramsthaler F, Prieto J, Schuliar Y, Lynnerup N, Cattaneo C (2009) The problem of aging human remains and living individuals: a review. Forensic Sci Int 193:1–13. https://doi.org/10.1016/j.forsciint.2009.09.008
Meissner C, Ritz-Timme S (2010) Molecular pathology and age estimation. Forensic Sci Int 203:34–43. https://doi.org/10.1016/j.forsciint.2010.07.010
Bekaert B, Kamalandua A, Zapico SC, van de Voorde W, Decorte R (2015) Improved age determination of blood and teeth samples using a selected set of DNA methylation markers. Epigenetics 10:922–930. https://doi.org/10.1080/15592294.2015.1080413
Márquez-Ruiz AB, González-Herrera L, Valenzuela A (2018) Usefulness of telomere length in DNA from human teeth for age estimation. Int J Legal Med 132:353–359. https://doi.org/10.1007/s00414-017-1595-5
Collins MJ, Nielsen-Marsh CM, Hiller J, Smith CI, Roberts JP, Prigodich RV, Wess TJ, Csapo J, Millard AR, Turner-Walker G (2002) The survival of organic matter in bone: a review. Archaeometry 44:383–394. https://doi.org/10.1111/1475-4754.t01-1-00071
Hedges REM (2002) Bone diagenesis: an overview of processes. Archaeometry 44:319–328. https://doi.org/10.1111/1475-4754.00064
Nicholson RA (2001) Taphonomic investigations. In: Brothwell DR, Pollard AM (eds) Handbook of archaeological science. Wiley, Chichester, pp 179–190
Kontopoulos I, Nystrom P, White L (2016) Experimental taphonomy: post-mortem microstructural modifications in Sus scrofa domesticus bone. Forensic Sci Int 266:320–328. https://doi.org/10.1016/j.forsciint.2016.06.024
Maurer AF, Person A, Tütken T, Amblard-Pison S, Ségalen L (2014) Bone diagenesis in arid environments: an intra-skeletal approach. Palaeogeogr Palaeoclimatol Palaeoecol 416:17–29. https://doi.org/10.1016/j.palaeo.2014.08.020
Nielsen-Marsh CM, Smith CI, Jans MME, Nord A, Kars H, Collins MJ (2007) Bone diagenesis in the European Holocene II: taphonomic and environmental considerations. J Archaeol Sci 34:1523–1531. https://doi.org/10.1016/J.JAS.2006.11.012
Stathopoulou ET, Psycharis V, Chryssikos GD, Gionis V, Theodorou G (2008) Bone diagenesis: new data from infrared spectroscopy and X-ray diffraction. Palaeogeogr Palaeoclimatol Palaeoecol 266:168–174. https://doi.org/10.1016/j.palaeo.2008.03.022
Ritz-Timme S, Cattaneo C, Collins MJ, Waite ER, Schütz HW, Kaatsch HJ, Borrman HIM (2000) Age estimation: the state of the art in relation to the specific demands of forensic practise. Int J Legal Med 113:129–136
Dobberstein RC, Huppertz J, von Wurmb-Schwark N, Ritz-Timme S (2008) Degradation of biomolecules in artificially and naturally aged teeth: implications for age estimation based on aspartic acid racemization and DNA analysis. Forensic Sci Int 179:181–191. https://doi.org/10.1016/j.forsciint.2008.05.017
Klumb K, Matzenauer C, Reckert A, Lehmann K, Ritz-Timme S (2016) Age estimation based on aspartic acid racemization in human sclera. Int J Legal Med 130:207–211. https://doi.org/10.1007/s00414-015-1255-6
Butler WT (1992) Dentin extracellular matrix and dentinogenesis. Oper Dent Suppl 5:18–23
Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336. https://doi.org/10.1007/s00198-005-2035-9
Walters C, Eyre DR (1983) Collagen crosslinks in human dentin: increasing content of hydroxypyridinium residues with age. Calcif Tissue Int 35:401–405. https://doi.org/10.1007/BF02405067
Eyre DR, Dickson IR, Van Ness K (1988) Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J 252:495–500
Martin-de las Heras S, Valenzuela A, Villanueva E (1999) Deoxypyridinoline crosslinks in human dentin and estimation of age. Int J Legal Med 112:222–226
Singh R, Barden A, Mori T, Beilin L (2001) Advanced glycation end-products: a review. Diabetologia 44:129–146. https://doi.org/10.1007/s001250051591
Thorpe SR, Baynes JW (2003) Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 25:275–281. https://doi.org/10.1007/s00726-003-0017-9
Tessier FJ (2010) The Maillard reaction in the human body. The main discoveries and factors that affect glycation. Pathol Biol 58:214–219. https://doi.org/10.1016/j.patbio.2009.09.014
Dyer DG, Dunn JA, Thorpe SR et al (1992) Accumulation of Maillard reaction products in skin collagen in diabetes and aging. Ann N Y Acad Sci 663:421–422
Sell DR (1997) Ageing promotes the increase of early glycation Amadori product as assessed by ε-N-(2-furoylmethyl)-L-lysine (furosine) levels in rodent skin collagen. The relationship to dietary restriction and glycoxidation. Mech Ageing Dev 95:81–99. https://doi.org/10.1016/S0047-6374(97)01863-0
Panwar P, Butler GS, Jamroz A, Azizi P, Overall CM, Brömme D (2018) Aging-associated modifications of collagen affect its degradation by matrix metalloproteinases. Matrix Biol 65:30–44. https://doi.org/10.1016/j.matbio.2017.06.004
Verzijl N, DeGroot J, Oldehinkel E, et al (2000) Age-related accumulation of Maillard reaction products in human articular cartilage collagen. 350 Pt 2:381–387
Pilin A, Pudil FF, Bencko VV (2007) Changes in colour of different human tissues as a marker of age. Int J Legal Med 121:158–162. https://doi.org/10.1007/s00414-006-0136-4
Oimomi M, Igaki N, Hata F, Kitamura Y, Nishimoto S, Baba S, Maeda S (1989) Age- and diabetes-accelerated glycation in the human aorta. Arch Gerontol Geriatr 8:123–127. https://doi.org/10.1016/0167-4943(89)90056-3
Frye EB, Degenhardt TP, Thorpe SR, Baynes JW (1998) Role of the Maillard reaction in aging of tissue proteins: advanced glycation end product-dependent increase in imidazolium cross-links in human lens proteins. J Biol Chem 273:18714–18719. https://doi.org/10.1074/jbc.273.30.18714
Saito M, Marumo K, Fujii K, Ishioka N (1997) Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem 253:26–32. https://doi.org/10.1006/abio.1997.2350
Wang X, Shen X, Li X, Mauli Agrawal C (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7. https://doi.org/10.1016/S8756-3282(01)00697-4
Odetti P, Rossi S, Monacelli F et al (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717. https://doi.org/10.1196/annals.1333.082
Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM (2005) Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone 37:825–832. https://doi.org/10.1016/j.bone.2005.07.019
Dong XN, Qin A, Xu J, Wang X (2011) In situ accumulation of advanced glycation endproducts (AGEs) in bone matrix and its correlation with osteoclastic bone resorption. Bone 49:174–183. https://doi.org/10.1016/j.bone.2011.04.009
Miura J, Nishikawa K, Kubo M, Fukushima S, Hashimoto M, Takeshige F, Araki T (2014) Accumulation of advanced glycation end-products in human dentine. Arch Oral Biol 59:119–124. https://doi.org/10.1016/j.archoralbio.2013.10.012
Shinno Y, Ishimoto T, Saito M, Uemura R, Arino M, Marumo K, Nakano T, Hayashi M (2016) Comprehensive analyses of how tubule occlusion and advanced glycation end-products diminish strength of aged dentin. Sci Rep 6:19849. https://doi.org/10.1038/srep19849
Greis F, Reckert A, Fischer K, Ritz-Timme S (2018) Analysis of advanced glycation end products (AGEs) in dentine: useful for age estimation? Int J Legal Med 132:799–805. https://doi.org/10.1007/s00414-017-1671-x
Simm A, Wagner J, Gursinsky T, Nass N, Friedrich I, Schinzel R, Czeslik E, Silber RE, Scheubel RJ (2007) Advanced glycation endproducts: a biomarker for age as an outcome predictor after cardiac surgery? Exp Gerontol 42:668–675. https://doi.org/10.1016/j.exger.2007.03.006
Guerra-Hernandez E, Corzo N (1996) Furosine determination in baby cereals by ion-pair reversed-phase liquid chromatography. Cereal Chem 73:729–731
Resmini P, Pellegrino L (1991) Analysis of food heat damage by direct HPLC of furosine. Int Cromatography Lab 6:7–11
Delgado T, Corzo N, Santa-María G, Jimeno ML, Olano A (1992) Determination of furosine in milk samples by ion-pair reversed phase liquid chromatography. Chromatographia 33:374–376. https://doi.org/10.1007/BF02275921
Takahashi M, Hoshino H, Kushida K, Inoue T (1995) Direct measurement of crosslinks, pyridinoline, deoxypyridinoline, and pentosidine, in the hydrolysate of tissues using high-performance liquid chromatography. Anal Biochem 232:158–162. https://doi.org/10.1006/abio.1995.0002
Jamall IS, Finelli VN, Que Hee SS (1981) A simple method to determine nanogram levels of 4-hydroxyproline in biological tissues. Anal Biochem 112:70–75. https://doi.org/10.1016/0003-2697(81)90261-X
Nkhumeleni FS, Raubenheimer EJ, Dauth J, van Heerden WFP, Smith PD, Pitout MJ (1992) Amino acid composition of dentine in permanent human teeth. Arch Oral Biol 37:157–158. https://doi.org/10.1016/0003-9969(92)90012-W
Kleter GA, Damen JJM, Buijs MJ, Ten Cate JM (1998) Modification of amino acid residues in carious dentin matrix. J Dent Res 77:488–495. https://doi.org/10.1177/00220345980770030801
Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JWJ, Lafeber FPJG, Baynes JW, TeKoppele JM (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275:39027–39031. https://doi.org/10.1074/jbc.M006700200
Ohtani S (1998) Rate of aspartic acid racemization in bone. Am J Forensic Med Pathol 19:284–287. https://doi.org/10.1097/00000433-199809000-00017
Sroga GE, Siddula A, Vashishth D (2015) Glycation of human cortical and cancellous bone captures differences in the formation of Maillard reaction products between glucose and ribose. PLoS One 10:e0117240. https://doi.org/10.1371/journal.pone.0117240
Schleicher E, Wieland OH (1986) Kinetic analysis of glycation as a tool for assessing the half-life of proteins. BBA-Gen. Subjects 884:199–205. https://doi.org/10.1016/0304-4165(86)90244-8
Senatus LM, Schmidt AM (2017) The AGE-RAGE Axis: implications for age-associated arterial diseases. Front Genet 8:187. https://doi.org/10.3389/fgene.2017.00187
Acknowledgments
This research was funded by Project PM97-0182 from the Ministry of Education of Spain. The authors acknowledge Dr. Paula Rodríguez-Bouzas of the Department of Statistics, University of Granada, Spain, for her assistance with statistical studies, and K. Shashok for improving the use of English in the manuscript.
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The protocols to collect samples from human subjects were approved by the corresponding Ethics Committees for Human Research of the University of Granada (Spain) and the University of Copenhagen (Denmark), and the study was conducted in accordance with the ethical standards laid down by the Declaration of Helsinki.
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Valenzuela, A., Guerra-Hernández, E., Rufián-Henares, J.Á. et al. Differences in non-enzymatic glycation products in human dentine and clavicle: changes with aging. Int J Legal Med 132, 1749–1758 (2018). https://doi.org/10.1007/s00414-018-1908-3
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DOI: https://doi.org/10.1007/s00414-018-1908-3