Palaeoproteomic investigation of an ancient human skeleton with abnormal deposition of dental calculus


  • Kilgore, L., Jurmain, R. & Van Gerven, D. Palaeoepidemiological patterns of trauma in a medieval Nubian skeletal population. Int. J. Osteoarchaeol. 7, 103–114 (1997).

    Article 

    Google Scholar 

  • Betsinger, T. K. & Smith, M. O. A singular case of advanced caries sicca in a pre-Columbian skull from East Tennessee. Int. J. Paleopathol. 24, 245–251 (2019).

    Article 
    PubMed 

    Google Scholar 

  • Tilley, L. & Oxenham, M. F. Survival against the odds: Modeling the social implications of care provision to seriously disabled individuals. Int. J. Paleopathol. 1, 35–42 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Milella, M., Zollikofer, C. P. E. & Ponce de León, M. S. Virtual reconstruction and geometric morphometrics as tools for paleopathology: A new approach to study rare developmental disorders of the skeleton. Anat. Rec. 298, 335–345 (2015).

    Article 

    Google Scholar 

  • Majander, K. et al. Ancient bacterial genomes reveal a high diversity of Treponema pallidum strains in early modern Europe. Curr. Biol. 30, 3788-3803.e10 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Andrades Valtueña, A. et al. Stone age Yersinia pestis genomes shed light on the early evolution, diversity, and ecology of plague. Proc. Natl. Acad. Sci. USA 119, e2116722119 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Akcalı, A. & Lang, N. P. Dental calculus: The calcified biofilm and its role in disease development. Periodontology 2000(76), 109–115 (2018).

    Article 

    Google Scholar 

  • Brothwell, D. R. Digging Up Bones: The Excavation, Treatment, and Study of Human Skeletal Remains (Cornell University Press, 1981).

    Google Scholar 

  • Gleize, Y., Castex, D., Chapoulie, R. & Duday, H. Analyse préliminaire et discussion sur la nature d’un dépôt dentaire très particulier. Bull. Mem. Soc. Anthropol. Paris 17, 5–12 (2005) ((in French)).

    Article 

    Google Scholar 

  • Hanihara, T., Ishida, H., Ohshima, N., Kondo, O. & Masuda, T. Dental calculus and other dental disease in a human skeleton of the Okhotsk Culture unearthed at Hamanaka-2 site, Rebun-Island, Hokkaido, Japan. Int. J. Osteoarchaeol. 4, 343–351 (1994).

    Article 

    Google Scholar 

  • Wright, S. L., Dobney, K. & Weyrich, L. S. Advancing and refining archaeological dental calculus research using multiomic frameworks. STAR Sci. Technol. Archaeol. Res. 7, 13–30 (2021).

    Google Scholar 

  • Radini, A. & Nikita, E. Beyond dirty teeth: Integrating dental calculus studies with osteoarchaeological parameters. Q. Int. 653-654, 3–18 (2022).

    Google Scholar 

  • Warinner, C. et al. Pathogens and host immunity in the ancient human oral cavity. Nat. Genet. 46, 336–344 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mackie, M. et al. Palaeoproteomic profiling of conservation layers on a 14th century Italian wall painting. Angew. Chem. Int. Ed Engl. 57, 7369–7374 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jersie-Christensen, R. R. et al. Quantitative metaproteomics of medieval dental calculus reveals individual oral health status. Nat. Commun. 9, 4744 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fotakis, A. K. et al. Multi-omic detection of Mycobacterium leprae in archaeological human dental calculus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190584 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Warinner, C. et al. Direct evidence of milk consumption from ancient human dental calculus. Sci. Rep. 4, 7104 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hendy, J. et al. A guide to ancient protein studies. Nat. Ecol. Evolut. 2, 791–799 (2018).

    Article 

    Google Scholar 

  • Jeong, C. et al. Bronze Age population dynamics and the rise of dairy pastoralism on the eastern Eurasian steppe. Proc. Natl. Acad. Sci. USA 115, E11248–E11255 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wilkin, S. et al. Dairying enabled early bronze age Yamnaya steppe expansions. Nature 598, 629–633 (2021).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Scorrano, G. et al. Genomic ancestry, diet and microbiomes of Upper Palaeolithic hunter-gatherers from San Teodoro cave. Commun. Biol. 5, 1262 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tang, L. et al. Paleoproteomic evidence reveals dairying supported prehistoric occupation of the highland Tibetan Plateau. Sci Adv 9, eadf0345 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ishida, H., Haniwara, T. & Kondo, O. Human Remains from the Hamanaka 2 Site, Rebun Island. Rebunto Hamanaka 2 Iseki Shutsudo No Jinkotsu (Daini/Yon Ji Chosa). Tsukuba Archaeological Studies/University of Tsukuba Prehistory and Archaeology Editorial Board. 89–108 (2002) (in Japanese).

  • Hudson, M. J. The perverse realities of change: World system incorporation and the Okhotsk culture of Hokkaido. J. Anthropol. Archaeol. 23, 290–308 (2004).

    Article 

    Google Scholar 

  • Naito, Y. I. et al. Dietary reconstruction of the Okhotsk Culture of Hokkaido, Japan, based on nitrogen composition of amino acids: Implications for correction of 14C marine reservoir effects on human bones. Radiocarbon 52, 671–681 (2010).

    Article 
    CAS 

    Google Scholar 

  • Tsutaya, T., Naito, Y. I., Ishida, H. & Yoneda, M. Carbon and nitrogen isotope analyses of human and dog diet in the Okhotsk culture: Perspectives from the Moyoro site, Japan. Anthropol. Sci. 122, 89–99 (2014).

    Article 

    Google Scholar 

  • Leipe, C. et al. Barley (Hordeum vulgare) in the Okhotsk culture (5th–10th century AD) of northern Japan and the role of cultivated plants in hunter–gatherer economies. PLoS One 12, e0174397 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ohshima, N. [Historical trends in caries frequency in archaeological human bones from Hokkaido, Japan] Hokkaido no kojinkotsu ni okeru ushokuhindo no jidaitekisuii. Anthropol. Sci. 104, 385–397 (1996) ((in Japanese)).

    Google Scholar 

  • Oxenham, M. F. & Matsumura, H. Oral and physiological paleohealth in cold adapted peoples: Northeast Asia, Hokkaido. Am. J. Phys. Anthropol. 135, 64–74 (2008).

    Article 
    PubMed 

    Google Scholar 

  • DeNiro, M. J. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317, 806–809 (1985).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • van Klinken, G. J. Bone collagen quality indicators for palaeodietary and radiocarbon measurements. J. Archaeol. Sci. 26, 687–695 (1999).

    Article 

    Google Scholar 

  • Junno, A. et al. Building a high-resolution chronology for northern Hokkaido—A case study of the Late Holocene Hamanaka 2 site on Rebun Island, Hokkaido (Japan). J. Archaeol. Sci. Rep. 36, 102867 (2021).

    Google Scholar 

  • Howland, M. R. et al. Expression of the dietary isotope signal in the compound-specific ?13C values of pig bone lipids and amino acids. Int. J. Osteoarchaeol. 13, 54–65 (2003).

    Article 

    Google Scholar 

  • Hedges, R. E. M., Clement, J. G., Thomas, C. D. L. & O’connell, T. C. Collagen turnover in the adult femoral mid-shaft: Modeled from anthropogenic radiocarbon tracer measurements. Am. J. Phys. Anthropol. 133, 808–816 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Okamoto, Y. et al. An Okhotsk adult female human skeleton (11th/12th century AD) with possible SAPHO syndrome from Hamanaka 2 site, Rebun Island, northern Japan. Anthropol. Sci. 124, 107–115 (2016).

    Article 

    Google Scholar 

  • van Doorn, N. L., Wilson, J., Hollund, H., Soressi, M. & Collins, M. J. Site-specific deamidation of glutamine: A new marker of bone collagen deterioration. Rapid Commun. Mass Spectrom. 26, 2319–2327 (2012).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Wilson, J., van Doorn, N. L. & Collins, M. J. Assessing the extent of bone degradation using glutamine deamidation in collagen. Anal. Chem. 84, 9041–9048 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mi, H., Muruganujan, A., Ebert, D., Huang, X. & Thomas, P. D. PANTHER version 14: More genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 47, D419–D426 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kashyap, D. R. et al. Peptidoglycan recognition proteins kill bacteria by inducing oxidative, thiol, and metal stress. PLoS Pathog. 10, e1004280 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dolińska, E. et al. The effect of nonsurgical periodontal therapy on HNP1-3 level in gingival crevicular fluid of chronic periodontitis patients. Arch. Immunol. Ther. Exp. 65, 355–361 (2017).

    Article 

    Google Scholar 

  • Oliveira, R. R. D. S. et al. Levels of candidate periodontal pathogens in subgingival biofilm. J. Dent. Res. 95, 711–718 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Curtis, M. A., Diaz, P. I. & Van Dyke, T. E. The role of the microbiota in periodontal disease. Periodontology 2000(83), 14–25 (2020).

    Article 

    Google Scholar 

  • Vielkind, P., Jentsch, H., Eschrich, K., Rodloff, A. C. & Stingu, C.-S. Prevalence of Actinomyces spp. in patients with chronic periodontitis. Int. J. Med. Microbiol. 305, 682–688 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Hasegawa, Y., Nagano, K. Porphyromonas gingivalis FimA and Mfa1 fimbriae: Current insights on localization, function, biogenesis, and genotype. Jpn Dent Sci Rev. 57, 190–200 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hayashi, F. et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099–1103 (2001).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Mahanonda, R. & Pichyangkul, S. Toll-like receptors and their role in periodontal health and disease. Periodontology 2000(43), 41–55 (2007).

    Article 

    Google Scholar 

  • Kim, C. et al. Immunotherapy targeting toll-like receptor 2 alleviates neurodegeneration in models of synucleinopathy by modulating α-synuclein transmission and neuroinflammation. Mol. Neurodegener. 13, 43 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rath, C. B. et al. Flagellin glycoproteomics of the periodontitis associated pathogen Selenomonas sputigena reveals previously not described O-glycans and rhamnose fragment rearrangement occurring on the glycopeptides. Mol. Cell. Proteom. 17, 721–736 (2018).

    Article 
    CAS 

    Google Scholar 

  • Tanner, A., Maiden, M. F., Macuch, P. J., Murray, L. L. & Kent, R. L. Jr. Microbiota of health, gingivitis, and initial periodontitis. J. Clin. Periodontol. 25, 85–98 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kopeckova, M., Pavkova, I. & Stulik, J. Diverse localization and protein binding abilities of glyceraldehyde-3-phosphate dehydrogenase in pathogenic bacteria: The key to its multifunctionality?. Front. Cell. Infect. Microbiol. 10, 89 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mackie, M. et al. Preservation of the metaproteome: Variability of protein preservation in ancient dental calculus. Sci. Technol. Archaeol. Res. 3, 74–86 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Velsko, I. M. et al. Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage. Microbiome 7, 102 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Socransky, S. S. & Haffajee, A. D. Periodontal microbial ecology. Periodontology 2000(38), 135–187 (2005).

    Article 

    Google Scholar 

  • Lieverse, A. R. Diet and the aetiology of dental calculus. Int. J. Osteoarchaeol. 9, 219–232 (1999).

  • Miyake, M., Iwasaki, A., Saito, H., Ohbayashi, Y. & Nagahata, S. A case of a giant dental calculus suspected to be a neoplastic lesion. Jpn. J. Oral Maxillofac. Surg. 50, 442–445 (2004).

    Article 

    Google Scholar 

  • Iwama, R. et al. A case of giant dental calculus in a patient with centronuclear myopathy. Spec. Care Dent. 43. 481–485 (2022).

    Article 

    Google Scholar 

  • Gupta, V. K., Paul, S. & Dutta, C. Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front. Microbiol. 8, 1162 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sawafuji, R., Saso, A., Suda, W., Hattori, M. & Ueda, S. Ancient DNA analysis of food remains in human dental calculus from the Edo period, Japan. PLoS One 15, e0226654 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Fagernäs, Z. et al. Understanding the microbial biogeography of ancient human dentitions to guide study design and interpretation. FEMS Microbes 3, xtac006 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hughes, C. S. et al. Single-pot, solid-phase-enhanced sample preparation for proteomics experiments. Nat. Protoc. 14, 68–85 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Palmer, K. S. et al. Comparing the use of magnetic beads with ultrafiltration for ancient dental calculus proteomics. J. Proteome Res. 20, 1689–1704 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sawafuji, R. et al. Proteomic profiling of archaeological human bone. R Soc. Open Sci. 4, 161004 (2017).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nunoura, T. et al. A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science 359, 559–563 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Ogura, K. et al. Potential biomarker proteins for aspiration pneumonia detected by shotgun proteomics using buccal mucosa samples: A cross-sectional case–control study. Clin. Proteom. 20, 9 (2023).

    Article 
    CAS 

    Google Scholar 

  • Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301–2319 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Chen, T. et al. The Human Oral Microbiome Database: A web accessible resource for investigating oral microbe taxonomic and genomic information. Database 2010, baq013 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tsutaya, T., Gakuhari, T., Asahara, A. & Yoneda, M. Isotopic comparison of gelatin extracted from bone powder with that from bone chunk and development of a framework for comparison of different extraction methods. J. Archaeol. Sci. Rep. 11, 99–105 (2017).

    Google Scholar 

  • Heaton, T. J. et al. Marine20—The marine radiocarbon age calibration curve (0–55,000 cal BP). Radiocarbon 62, 779–820 (2020).

    Article 
    CAS 

    Google Scholar 

  • Reimer, P. J. et al. The IntCal20 northern hemisphere radiocarbon age calibration curve (0–55 cal kBP). Radiocarbon 62, 725–757 (2020).

    Article 
    CAS 

    Google Scholar 

  • Yoneda, M. et al. Radiocarbon marine reservoir ages in the western Pacific estimated by pre-bomb molluscan shells. Nucl. Instrum. Methods Phys. Res. B 259, 432–437 (2007).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Ramsey, C. B. Radiocarbon calibration and analysis of stratigraphy: The OxCal Program. Radiocarbon 37, 425–430 (1995).

    Article 

    Google Scholar 

  • Perez-Riverol, Y. et al. The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 



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