Inferring chronological age from DNA methylation patterns of human teeth

American Journal of Physical Anthropology

Volumn 159, Issue 4, 2016, Pages 585-595

  Giuliani, Cristina ^a   Cilli, Elisabetta ^a   Bacalini, Maria Giulia ^a   Pirazzini, Chiara ^a   Sazzini, Marco ^a   Gruppioni, Giorgio ^a   Franceschi, Claudio ^a,b   Garagnani, Paolo ^a,c   Luiselli, Donata ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b IRCCS ISTITUTO DELLE SCIENZE NEUROLOGICHE DI BOLOGNA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

age estimation; DNA methylation; ELOVL2; teeth

Indexed keywords

ADOLESCENT; ADULT; AGE; AGED; CEMENTUM; DENTIN; DNA METHYLATION; HUMAN; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MODEL; STATISTICAL MODEL; TOOTH PULP; CHEMISTRY; DENTAL AGE ESTIMATION; GENETICS; ISOLATION AND PURIFICATION; MIDDLE AGED; PHYSICAL ANTHROPOLOGY; PROCEDURES; TOOTH; YOUNG ADULT;

ACYLTRANSFERASE; DNA; FATTY ACID ELONGASES;

ACETYLTRANSFERASES; ADOLESCENT; ADULT; AGE DETERMINATION BY TEETH; AGED; ANTHROPOLOGY, PHYSICAL; DNA; DNA METHYLATION; HUMANS; MIDDLE AGED; TOOTH; YOUNG ADULT;

EID: 84960260122     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22921     Document Type: Article

References (54)

1. Adler CJ, Haak W, Donlon D, Cooper A., 2011. Survival and recovery of DNA from ancient teeth and bones. J Archaeol Sci 38: 956-964.
2. Aggarwal P, Saxena S, Bansal P., 2008. Incremental lines in root cementum of human teeth: an approach to their role in age estimation using polarizing microscopy. Indian J Dent Res off Publ Indian Soc Dent Res 19: 326-330.
3. Allentoft ME, Sikora M, Sjögren K-G, Rasmussen S, Rasmussen M, Stenderup J, Damgaard PB, Schroeder H, Ahlström T, Vinner L, Malaspinas A-S, Margaryan A, Higham T, Chivall D, Lynnerup N, Harvig L, Baron J, Della Casa P, Dąbrowski P, Duffy PR, Ebel AV, Epimakhov A, Frei K, Furmanek M, Gralak T, Gromov A, Gronkiewicz S, Grupe G, Hajdu T, Jarysz R, Khartanovich V, Khokhlov A, Kiss V, Kolář J, Kriiska A, Lasak I, Longhi C, McGlynn G, Merkevicius A, Merkyte I, Metspalu M, Mkrtchyan R, Moiseyev V, Paja L, Pálfi G, Pokutta D, Pospieszny Ł, Price TD, Saag L, Sablin M, Shishlina N, Smrčka V, Soenov VI, Szeverényi V, Tóth G, Trifanova SV, Varul L, Vicze M, Yepiskoposyan L, Zhitenev V, Orlando L, Sicheritz-Pontén T, Brunak S, Nielsen R, Kristiansen K, Willerslev E., 2015. Population genomics of Bronze Age Eurasia. Nature 522: 167-172.
4. AlQahtani SJ, Hector MP, Liversidge HM., 2014. Accuracy of dental age estimation charts: Schour and Massler, Ubelaker and the London Atlas. Am J Phys Anthropol 154: 70-78.
5. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, Mangino M, Zhai G, Zhang F, Valdes A, Shin SY, Dempster EL, Murray RM, Grundberg E, Hedman AK, Nica A, Small KS, MuTHER Consortium, Dermitzakis ET, McCarthy MI, Mill J, Spector TD, Deloukas P,. 2012. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet 8: e1002629.
6. Bocklandt S, Lin W, Sehl ME, Sánchez FJ, Sinsheimer JS, Horvath S, Vilain E., 2011. Epigenetic Predictor of Age. PLoS One 6: e14821.
7. Briggs AW, Meyer M, Krause J, Kircher M, Paabo S., 2010. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res 38: e87.
8. Briggs AW, Stenzel U, Johnson PLF, Green RE, Kelso J, Prüfer K, Meyer M, Krause J, Ronan MT, Lachmann M, Pääbo S., 2007. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci USA 104: 14616-14621.
9. Brooks S, Suchey JM., 1990. Skeletal age determination based on the os pubis: a comparison of the Acsádi-Nemeskéri and Suchey-Brooks methods. Hum Evol 5: 227-238.
10. Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R, Austin J, Cooper A., 2007. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Res 35: 5717-5728.
11. Canault M, Tellier E, Bonardo B, Mas E, Aumailley M, Juhan-Vague I, Nalbone G, Peiretti F., 2006. FHL2 interacts with both ADAM-17 and the cytoskeleton and regulates ADAM-17 localization and activity. J Cell Physiol 208: 363-372.
12. Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ., 2007. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res 35: e119.
13. 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.
14. Damgaard PB, Margaryan A, Schroeder H, Orlando L, Willerslev E, Allentoft ME., 2015. Improving access to endogenous DNA in ancient bones and teeth. Sci Rep 5: 11184.
15. Day K, Waite LL, Thalacker-Mercer A, West A, Bamman MM, Brooks JD, Myers RM, Absher D., 2013. Differential DNA methylation with age displays both common and dynamic features across human tissues that are influenced by CpG landscape. Genome Biol 14: R102.
16. Florath I, Butterbach K, Müller H, Bewerunge-Hudler M, Brenner H., 2014. Cross-sectional and longitudinal changes in DNA methylation with age: an epigenome-wide analysis revealing over 60 novel age-associated CpG sites. Hum Mol Genet 23: 1186-1201.
17. Franklin D., 2010. Forensic age estimation in human skeletal remains: current concepts and future directions. Leg Med Tokyo Jpn 12: 1-7.
18. Friedrich FW, Reischmann S, Schwalm A, Unger A, Ramanujam D, Münch J, Müller OJ, Hengstenberg C, Galve E, Charron P, Linke WA, Engelhardt S, Patten M, Richard P, van der Velden J, Eschenhagen T, Isnard R, Carrier L., 2014. FHL2 expression and variants in hypertrophic cardiomyopathy. Basic Res Cardiol 109: 451.
19. Garagnani P, Bacalini MG, Pirazzini C, Gori D, Giuliani C, Mari D, Di Blasio AM, Gentilini D, Vitale G, Collino S, Rezzi S, Castellani G, Capri M, Salvioli S, Franceschi C., 2012. Methylation of ELOVL2 gene as a new epigenetic marker of age. Aging Cell 11: 1132-1134.
20. Gauthier J, Schutkowski H., 2013. Assessing the application of tooth cementum annulation relative to macroscopic aging techniques in an archeological sample. Homo 64: 42-57. doi: 10.1016/j.jchb.2012.11.001. Epub 2012 Dec 6. PubMed PMID: 23218650.
21. Gokhman D, Lavi E, Prüfer K, Fraga MF, Riancho JA, Kelso J, Pääbo S, Meshorer E, Carmel L., 2014. Reconstructing the DNA methylation maps of the Neandertal and the Denisovan. Science 344: 523-527.
22. Goldberg M, Smith AJ., 2004. Cells and extracellular matrices of dentin and pulp: a biological basis for repair and tissue engineering. Crit Rev Oral Biol Med off Publ Am Assoc Oral Biol 15: 13-27.
23. Gupta P, Kaur H, Shankari G S M, Jawanda MK, Sahi N., 2014. Human age estimation from tooth cementum and dentin. J Clin Diagn Res JCDR 8: ZC07-ZC10.
24. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, Klotzle B, Bibikova M, Fan J-B, Gao Y, Deconde R, Chen M, Rajapakse I, Friend S, Ideker T, Zhang K., 2013. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell 49: 359-367.
25. Higgins D, Austin JJ., 2013. Teeth as a source of DNA for forensic identification of human remains: a review. Sci Justice J Forensic Sci Soc 53: 433-441.
26. Higgins D, Kaidonis J, Townsend G, Hughes T, Austin JJ., 2013. Targeted sampling of cementum for recovery of nuclear DNA from human teeth and the impact of common decontamination measures. Investig Genet 4: 18.
27. Higgins D, Rohrlach AB, Kaidonis J, Townsend G, Austin JJ., 2015. Differential nuclear and mitochondrial DNA preservation in postmortem teeth with implications for forensic and ancient DNA studies. PloS One 10: e0126935.
28. Hillson S., 2005. Teeth. Cambridge: Cambridge University Press.
29. Hofreiter M, Jaenicke V, Serre D, von Haeseler A, Pääbo S., 2001. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res 29: 4793-4799.
30. Horvath S., 2013. DNA methylation age of human tissues and cell types. Genome Biol 14: R115.
31. Johansson A, Enroth S, Gyllensten U., 2013. Continuous Aging of the Human DNA Methylome Throughout the Human Lifespan. PLoS One 8: e67378.
32. Koch CM, Wagner W., 2011. Epigenetic-aging-signature to determine age in different tissues. Aging 3: 1018-1027.
33. Kvaal SI, Solheim T., 1995. Incremental lines in human dental cementum in relation to age. Eur J Oral Sci 103: 225-230.
34. Leonard AE, Kelder B, Bobik EG, Chuang L-T, Lewis CJ, Kopchick JJ, Mukerji P, Huang Y-S., 2002. Identification and expression of mammalian long-chain PUFA elongation enzymes. Lipids 37: 733-740.
35. Llamas B, Holland ML, Chen K, Cropley JE, Cooper A, Suter CM., 2012. High-resolution analysis of cytosine methylation in ancient DNA. PLoS One 7: e30226.
36. Malaver PC, Yunis JJ., 2003. Different dental tissues as source of DNA for human identification in forensic cases. Croat Med J 44: 306-309.
37. Marttila S, Kananen L, Häyrynen S, Jylhävä J, Nevalainen T, Hervonen A, Jylhä M, Nykter M, Hurme M., 2015. Ageing-associated changes in the human DNA methylome: genomic locations and effects on gene expression. BMC Genomics 16: 179. doi: 10.1186/s12864-015-1381-z
38. Meissner C, Ritz-Timme S., 2010. Molecular pathology and age estimation. Forensic Sci Int 203: 34-43.
39. Pedersen JS, Valen E, Velazquez AMV, Parker BJ, Rasmussen M, Lindgreen S, Lilje B, Tobin DJ, Kelly TK, Vang S, Andersson R, Jones PA, Hoover CA, Tikhonov A, Prokhortchouk E, Rubin EM, Sandelin A, Gilbert MTP, Krogh A, Willerslev E, Orlando L., 2014. Genome-wide nucleosome map and cytosine methylation levels of an ancient human genome. Genome Res 24: 454-466.
40. Pilli E, Modi A, Serpico C, Achilli A, Lancioni H, Lippi B, Bertoldi F, Gelichi S, Lari M, Caramelli D., 2013. Monitoring DNA contamination in handled vs. directly excavated ancient human skeletal remains. PLoS One 8: e52524.
41. Pötsch L, Meyer U, Rothschild S, Schneider PM, Rittner C., 1992. Application of DNA techniques for identification using human dental pulp as a source of DNA. Int J Legal Med 105: 139-143.
42. Rakyan VK, Down TA, Thorne NP, Flicek P, Kulesha E, Gräf S, Tomazou EM, Bäckdahl L, Johnson N, Herberth M, Howe KL, Jackson DK, Miretti MM, Fiegler H, Marioni JC, Birney E, Hubbard TJP, Carter NP, Tavaré S, Beck S., 2008. An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Genome Res 18: 1518-1529.
43. Reynolds LM, Taylor JR, Ding J, Lohman K, Johnson C, Siscovick D, Burke G, Post W, Shea S, Jacobs DR Jr, Stunnenberg H, Kritchevsky SB, Hoeschele I, McCall CE, Herrington DM, Tracy RP, Liu Y,. 2014. Age-related variations in the methylome associated with gene expression in human monocytes and T cells. Nat Commun 5: 5366.
44. Roksandic M, Vlak D, Schillaci MA, Voicu D., 2009. Technical note: applicability of tooth cementum annulation to an archaeological population. Am J Phys Anthropol 140: 583-588. doi: 10.1002/ajpa.21136. PubMed PMID: 19639640.
45. Rönn T, Volkov P, Gillberg L, Kokosar M, Perfilyev A, Jacobsen AL, Jørgensen SW, Brøns C, Jansson PA, Eriksson KF, Pedersen O, Hansen T, Groop L, Stener-Victorin E, Vaag A, Nilsson E, Ling C., 2015. Impact of age, BMI and HbA1c levels on the genome-wide DNA methylation and mRNA expression patterns in human adipose tissue and identification of epigenetic biomarkers in blood. Hum Mol Genet 24: 3792-3813. doi: 10.1093/hmg/ddv124
46. Rudbeck L, Gilbert MTP, Willerslev E, Hansen AJ, Lynnerup N, Christensen T, Dissing J., 2005. mtDNA analysis of human remains from an early Danish Christian cemetery. Am J Phys Anthropol 128: 424-429.
47. Sarkar D., 2008. Lattice: multivariate data visualization with R. New York: Springer.
48. Saygin NE, Giannobile WV, Somerman MJ., 2000. Molecular and cell biology of cementum. Periodontol 2000 24: 73-98.
49. Shapiro B, Drummond AJ, Rambaut A, Wilson MC, Matheus PE, Sher AV, Pybus OG, Gilbert MTP, Barnes I, Binladen J, Willerslev E, Hansen AJ, Baryshnikov GF, Burns JA, Davydov S, Driver JC, Froese DG, Harington CR, Keddie G, Kosintsev P, Kunz ML, Martin LD, Stephenson RO, Storer J, Tedford R, Zimov S, Cooper A., 2004. Rise and fall of the Beringian Steppe Bison. Science 306: 1561-1565.
50. Smith O, Clapham AJ, Rose P, Liu Y, Wang J, Allaby RG., 2014. Genomic methylation patterns in archaeological barley show de-methylation as a time-dependent diagenetic process. Sci Rep 4: 5559.
51. Smith RW, Monroe C, Bolnick DA., 2015. Detection of Cytosine methylation in ancient DNA from five native american populations using bisulfite sequencing. PLoS One 10: e0125344. doi: 10.1371/journal.pone.0125344. eCollection 2015. PubMed PMID: 26016479; PubMed Central PMCID: PMC4445908.
52. Steegenga WT, Boekschoten MV, Lute C, Hooiveld GJ, de Groot PJ, Morris TJ, Teschendorff AE, Butcher LM, Beck S, Müller M., 2014. Genome-wide age-related changes in DNA methylation and gene expression in human PBMCs. Age Dordr Neth 36: 9648.
53. Zbiec-Piekarska R, Spólnicka M, Kupiec T, Makowska Ż, Spas A, Parys-Proszek A, Kucharczyk K, Płoski R, Branicki W., 2015. Examination of DNA methylation status of the ELOVL2 marker may be useful for human age prediction in forensic science. Forensic Sci Int Genet 14: 161-167.
54. Wittwer-Backofen U, Gampe I, Vaupel JJW., 2004. Tooth cementum annulation for age estimation: results from a large known-age validation study. Am J Phys Anthropol 123: 119-129.