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      An insight into cancer palaeobiology: does the Mesozoic neoplasm support tissue organization field theory of tumorigenesis?

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          Abstract

          Background

          Neoplasms are common across the animal kingdom and seem to be a feature plesiomorphic for metazoans, related with an increase in somatic complexity. The fossil record of cancer complements our knowledge of the origin of neoplasms and vulnerability of various vertebrate taxa. Here, we document the first undoubted record of primary malignant bone tumour in a Mesozoic non-amniote. The diagnosed osteosarcoma developed in the vertebral intercentrum of a temnospondyl amphibian, Metoposaurus krasiejowensis from the Krasiejów locality, southern Poland.

          Results

          A wide array of data collected from gross anatomy, histology, and microstructure of the affected intercentrum reveals the tumour growth dynamics and pathophysiological aspects of the neoplasm formation on the histological level. The pathological process almost exclusively pertains to the periosteal part of the bone composed from a highly vascularised tissue with lamellar matrix. The unorganised arrangement of osteocyte lacunae observed in the tissue is characteristic for bone tissue types connected with static osteogenesis, and not for lamellar bone. The neoplastic bone mimics on the structural level the fast growing fibrolamellar bone, but on the histological level develops through a novel ossification type. The physiological process of bone remodelling inside the endochondral domain continued uninterrupted across the pathology of the periosteal part.

          Conclusions

          Based on the results, we discuss our case study’s consistence with the Tissue Organization Field Theory of tumorigenesis, which locates the causes of neoplastic transformations in disorders of tissue architecture.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12862-022-02098-3.

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          Most cited references55

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          Potential Mechanisms for Cancer Resistance in Elephants and Comparative Cellular Response to DNA Damage in Humans.

          Evolutionary medicine may provide insights into human physiology and pathophysiology, including tumor biology.
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            Peto's Paradox: evolution's prescription for cancer prevention.

            The evolution of multicellularity required the suppression of cancer. If every cell has some chance of becoming cancerous, large, long-lived organisms should have an increased risk of developing cancer compared with small, short-lived organisms. The lack of correlation between body size and cancer risk is known as Peto's paradox. Animals with 1000 times more cells than humans do not exhibit an increased cancer risk, suggesting that natural mechanisms can suppress cancer 1000 times more effectively than is done in human cells. Because cancer has proven difficult to cure, attention has turned to cancer prevention. In this review, similar to pharmaceutical companies mining natural products, we seek to understand how evolution has suppressed cancer to develop ultimately improved cancer prevention in humans.
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              Naturally occurring tumours in the basal metazoan Hydra.

              The molecular nature of tumours is well studied in vertebrates, although their evolutionary origin remains unknown. In particular, there is no evidence for naturally occurring tumours in pre-bilaterian animals, such as sponges and cnidarians. This is somewhat surprising given that recent computational studies have predicted that most metazoans might be prone to develop tumours. Here we provide first evidence for naturally occurring tumours in two species of Hydra. Histological, cellular and molecular data reveal that these tumours are transplantable and might originate by differentiation arrest of female gametes. Growth of tumour cells is independent from the cellular environment. Tumour-bearing polyps have significantly reduced fitness. In addition, Hydra tumours show a greatly altered transcriptome that mimics expression shifts in vertebrate cancers. Therefore, this study shows that spontaneous tumours have deep evolutionary roots and that early branching animals may be informative in revealing the fundamental mechanisms of tumorigenesis.
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                Author and article information

                Contributors
                dawid@surmik.pl
                Journal
                BMC Ecol Evol
                BMC Ecol Evol
                BMC Ecology and Evolution
                BioMed Central (London )
                2730-7182
                13 December 2022
                13 December 2022
                2022
                : 22
                : 143
                Affiliations
                [1 ]GRID grid.11866.38, ISNI 0000 0001 2259 4135, Institute of Earth Sciences, Faculty of Natural Sciences, , University of Silesia, ; Będzińska 60, 41-200 Sosnowiec, Poland
                [2 ]GRID grid.413454.3, ISNI 0000 0001 1958 0162, Institute of Paleobiology, , Polish Academy of Sciences, ; Twarda 51/55, 00-818 Warsaw, Poland
                [3 ]GRID grid.13276.31, ISNI 0000 0001 1955 7966, Institute of Animal Sciences, , Warsaw University of Life Sciences, ; Ciszewskiego 8, 02-786 Warsaw, Poland
                [4 ]GRID grid.10388.32, ISNI 0000 0001 2240 3300, Institute of Geosciences, Section Paleontology, , University of Bonn, ; Nussallee 8, 53115 Bonn, Germany
                [5 ]GRID grid.107891.6, ISNI 0000 0001 1010 7301, Institute of Biology, , University of Opole, ; Oleska 22, 45-052 Opole, Poland
                [6 ]GRID grid.11866.38, ISNI 0000 0001 2259 4135, Faculty of Exact and Technical Sciences, , University of Silesia, ; Będzińska 39, 41-200 Sosnowiec, Poland
                [7 ]GRID grid.420557.1, ISNI 0000 0001 2110 2178, Carnegie Museum of Natural History, ; 4400 Forbes Ave, Pittsburgh, PA 15215 USA
                Author information
                http://orcid.org/0000-0003-0121-9592
                http://orcid.org/0000-0002-4166-6963
                http://orcid.org/0000-0001-8329-0741
                http://orcid.org/0000-0001-5961-489X
                http://orcid.org/0000-0003-3575-5641
                http://orcid.org/0000-0003-1327-6615
                http://orcid.org/0000-0003-4932-7402
                Article
                2098
                10.1186/s12862-022-02098-3
                9746082
                36513967
                7b16b6a6-ce2b-4720-8a02-0121248eac34
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 7 November 2022
                : 8 December 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: 2019/32/C/NZ4/00150
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                neoplasm,mesozoic,paleopathology,comparative oncology
                neoplasm, mesozoic, paleopathology, comparative oncology

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