Echo of carcino-evo-devo. On the beneficial role of inherited tumors in the evolution of organisms

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Abstract

The analytical article critically examines some aspects of the theory of carcino-evo-devo, testing its strength, which is known to be useful for strengthening and improving both new and long-established ideas in the scientific world.

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About the authors

R. I. Ataullakhanov

State Scientific Center Institute of Immunology; Lomonosov Moscow State University

Author for correspondence.
Email: ravshan.ataullakhanov@gmail.com
Russian Federation, Moscow; Moscow

References

  1. Забежинский М.А., Полев Д.Е., Шилов Е.С. и др. Изучение развития “шапочек” на голове золотых рыбок // Рус. журн. “СПИД, рак и общественное здоровье”. 2010. Т. 14 (1). С. 21.
  2. Козлов А.П. Опухоли и эволюция // Вопр. онкол. 2008. Т. 54 (6). С. 695–705.
  3. Козлов А.П. Теория эволюционной роли наследуемых опухолей (carcino-evo-devo): история развития и современное состояние. Ч. 1. От общих принципов к гипотезе и от гипотезы к концепции // Успехи соврем. биол. 2024. Т. 144 (3). С. 249–264.
  4. Козлов А.П., Забежинский М.А., Попович И.Г. и др. Гиперпластические разрастания на коже головы золотых рыбок – сравнительно-онкологические аспекты // Вопр. онкол. 2012. Т. 58 (3). С. 387–393.
  5. Козлов А.П., Матюнина Е.А., Макашов А.А. База данных генов TSEEN Биомедицинского центра. Свидетельство о государственной регистрации базы данных № 2021621840. СПб., 2021.
  6. Круковская Л.Л., Полев Д.Е., Носова Ю.К. и др. Изучение экспрессии транскрипционного фактора BRACHYURY (T) в нормальных и опухолевых тканях человека // Вопр. онкол. 2008. Т. 54 (6). С. 739–743.
  7. Круковская Л.Л., Самусик Н.Д., Шилов Е.С. и др. Опухолеспецифическая экспрессия эволюционно нового гена PBOV1 // Вопр. онкол. 2010. Т. 56 (3). С. 327–332.
  8. Круковская Л.Л., Полев Д.Е., Курбатова Т.В. и др. Изучение опухолеспецифичности экспрессии некоторых эволюционно новых генов // Вопр. онкол. 2016. Т. 62 (3). С. 495–500.
  9. Полев Д., Носова Ю., Круковская Л. и др. Экспрессия транскриптов, соответствующих кластеру Hs.633957 в тканях и опухолях человека // Мол. биол. 2009. Т. 43 (1). С. 97–102.
  10. Полев Д.Е., Круковская Л.Л., Козлов А.П. Экспрессия локуса Hs.633957 в органах пищеварительной системы и опухолях человека // Вопр. онкол. 2011. Т. 57 (1). С. 48–49.
  11. Самусик Н.А., Галачьянц Ю.П., Козлов А.П. Сравнительно-геномный анализ опухолеспецифических транскрибируемых последовательностей человека // Рус. журн. “СПИД, рак и общественное здоровье”. 2007. Т. 10. С. 30–32.
  12. Самусик Н.А., Галачьянц Ю.П., Козлов А.П. Анализ эволюционной новизны последовательностей, экспрессирующихся в опухолях // Экол. генетика. 2009. Т. 7. С. 26–37.
  13. Шилов Е.С., Мурашев Б.В., Попович И.Г. и др. Возможная новая модель опухолей у рыб // Рус. журн. “СПИД, рак и общественное здоровье”. 2009. Т. 13 (2). С. 49–50.
  14. Alföldi J., Di Palma F., Grabherr M. et al. The genome of the green anole lizard and a comparative analysis with birds and mammals // Nature. 2011. V. 477 (7366). P. 587–591. https://doi.org/10.1038/nature10390
  15. Aparicio S., Chapman J., Stupka E. et al. Whole-genome shotgun assembly and analysis of the Fugu rubripes genome // Science. 2002. V. 297 (5585). P. 1301–1310. https://doi.org/10.1126/science.1072104
  16. Aury J.-M., Jaillon O., Duret L. et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia // Nature. 2006. V. 444 (7116). P. 171–178.
  17. Bagaev A., Kotlov N., Nomie K. et al. Conserved pan-cancer microenvironment subtypes predict response to immunotherapy // Cancer Cell. 2021. V. 39 (6). P. 845–865. e7. https://doi.org/10.1016/j.ccell.2021.04.014
  18. Berriman M., Haas B.J., LoVerde P.T. et al. The genome of the blood fluke Schistosoma mansoni // Nature. 2009. V. 460 (7253). P. 352–358. https://doi.org/10.1038/nature08160
  19. Blattner F.R., Plunkett G., Bloch C.A. et al. The complete genome sequence of Escherichia coli K-12 // Science. 1997. V. 277 (5331). P. 1453–1462. https://doi.org/10.1126/science.277.5331.1453
  20. Blaxter M.L., De Ley P., Garey J.R. et al. A molecular evolutionary framework for the phylum Nematoda // Nature. 1998. V. 392 (6671). P. 71–75. https://pubmed.ncbi.nlm.nih.gov/9510248/
  21. Boissonnas A., Licata F., Poupel L. et al. CD8+ tumor-infiltrating T cells are trapped in the tumor-dendritic cell network // Neoplasia. 2013. V. 15 (1). P. 85–94. https://doi.org/10.1593/neo.121572
  22. Bult C.J., White O., Olsen G.J. et al. Complete genome sequence of the methanogenic archaeon Methanococcus jannaschii // Science. 1996. V. 273 (5278). P. 1058–1073. https://doi.org/10.1126/science.273.5278.1058
  23. Chapman J.A., Kirkness E.F., Simakov O. et al. The dynamic genome of Hydra // Nature. 2010. V. 464 (7288). P. 592–596. https://doi.org/10.1038/nature09660
  24. Clarke M., Lohan A.J., Liu B. et al. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling // Genome Biol. 2013. V. 14 (2). R11. https://doi.org/10.1186/gb-2013-14-2-r11
  25. Colbourne J.K., Pfrender M.E., Gilbert D. et al. The Daphnia pulex genome: a model for ecological genomics // Science. 2011. V. 331 (6017). P. 555–561. https://doi.org/10.1126/science.1197761
  26. Dobrynin P., Matyunina E., Malov S., Kozlov A. The novelty of human cancer/testis antigen encoding genes in evolution // Int. J. Genom. 2013. V. 2013. 105108.
  27. Eichinger L., Pachebat J.A., Glöckner G. et al. The genome of the social amoeba Dictyostelium discoideum // Nature. 2005. V. 435 (7038). P. 43–57. https://doi.org/10.1038/nature03481
  28. Eisen J.A., Coyne R.S., Wu M. et al. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote // PLoS Biol. 2006. V. 4 (9). e286. https://doi.org/10.1371/journal.pbio.0040286
  29. Evtushenko V.I., Barabitskaya O.V., Emeljanov A.V., Kozlov A.P. Estimation of the maximal expression of the rat genome and the complexity of tumor-specific transcripts // Abstr. of the First Intern. Conf. on Gene Regulation Oncogenesis, and AIDS. Loutráki, Greece, September 15–21, 1989.
  30. Galachyants Y., Kozlov A.P. CDD as a tool for discovery of specifically-expressed transcripts // Russ. J. “AIDS, Cancer and Related Problems”. 2009. V. 13 (2). P. 60–61.
  31. Gardner M.J., Hall N., Fung E. et al. Genome sequence of the human malaria parasite Plasmodium falciparum // Nature. 2002. V. 419 (6906). P. 498–511. https://doi.org/10.1038/nature01097
  32. Goffeau A., Barrell B.G., Bussey H. et al. Life with 6000 genes // Science. 1996. V. 274 (5287). P. 546–567. https://doi.org/10.1126/science.274.5287.546
  33. Grbić M., Bjelica A., Nagy Z.T. et al. The genome of Brachionus plicatilis // Nat. Commun. 2022. V. 13. 77. https://doi.org/10.1038/s41467-021-27778-8
  34. Green R.E., Krause J., Briggs A.W. et al. A draft sequence of the Neandertal genome // Science. 2010. V. 328 (5979). P. 710–722. https://doi.org/10.1126/science.1188021
  35. Gutekunst J., Andriantsoa R., Falckenhayn C. et al. Clonal genome evolution and rapid invasive spread of the marbled crayfish // Nat. Ecol. Evol. 2018. V. 2 (3). P. 567–573. 10.1038/s41559-018-0467-9' target='_blank'>https://doi: 10.1038/s41559-018-0467-9
  36. Han K., Li Z.F., Peng R. et al. Extraordinary expansion of a Sorangium cellulosum genome from an alkaline milieu // Sci. Rep. 2013. V. 3. 2101. https://pubmed.ncbi.nlm.nih.gov/23812535/
  37. Hellsten U., Harland R.M., Gilchrist M.J. et al. The genome of the Western clawed frog Xenopus tropicalis // Science. 2010. V. 328 (5978). P. 633–636. https://doi.org/10.1126/science.1183670
  38. Howe K., Clark M.D., Torroja C.F. et al. The zebrafish reference genome sequence and its relationship to the human genome // Nature. 2013. V. 496 (7446). P. 498–503. https://doi.org/10.1038/nature12111
  39. Inagaki K., Kunisho S., Takigawa H. et al. Role of tumor-associated macrophages at the invasive front in human colorectal cancer progression // Cancer Sci. V. 112 (7). P. 2692–2704. https://doi.org/10.1111/cas.14940
  40. International Chicken Genome Sequencing Consortium. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution // Nature. 2004. V. 432 (7018). P. 695–716. https://doi.org/10.1038/nature03154
  41. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome // Nature. 2001. V. 409 (6822). P. 860–921. https://doi.org/10.1038/35057062
  42. Koonin E.V., Wolf Y.I. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world // Nucl. Acids Res. 2008. V. 36 (21). P. 6688–6719.
  43. Kozlov A.P. Evolution by tumor neofunctionalization: the role of tumors in the origin of new cell types, tissues and organs. Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo: Elsevier/Academic Press, 2014. 248 p.
  44. Kozlov A.P. The theory of carcino-evo-devo and its non-trivial predictions // Genes. 2022. V. 13 (1). 2347.
  45. Kozlov A.P., Emeljanov A.V., Barabitskaya O.V., Evtushenko V.I. The maximal expression of mammalian genome, the complexity of tumor-specific transcripts and the cloning of tumor-specific cDNAs // Abstr. of Annu. Meet. Spons. by Lab. of Tumor Cell Biol. Bethesda, Maryland: National Cancer Institute (U.S.), 1992.
  46. Kozlov A.P., Galachyants Y.P., Dukhovlinov I.V. et al. Evolutionarily new sequences expressed in tumors // Infect. Agent Cancer. 2006. V. 25. P. 1–8.
  47. Krukovskaja L.L., Baranova A., Tyezelova T. et al. Experimental study of human expressed sequences newly identified in silico as tumor specific // Tumor Biol. 2005. V. 26 (1). P. 17–24.
  48. Loftus B., Anderson I., Davies R. et al. The genome of the protist parasite Entamoeba histolytica // Nature. 2005. V. 433 (7028). P. 865–868. https://doi.org/10.1038/nature03828
  49. Miheecheva N., Postovalova E., Lyu Y. et al. Multiregional single-cell proteogenomic analysis of ccRCC reveals cytokine drivers of intratumor spatial heterogeneity // Cell Rep. 2022. V. 40 (7). 111180. https://doi.org/10.1016/j.celrep.2022.111180
  50. Navab R., Strumpf D., Bandarchi B. et al. Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer // PNAS USA. 2011. V. 108 (17). P. 7160–7165. https://doi.org/10.1073/pnas.1014506108
  51. Ota K.G., Kuratani S., Sato N. Hagfish embryology with reference to the evolution of the neural crest // Nat. Commun. 2011. V. 2. 1262. https://doi.org/10.1038/ncomms1262
  52. Palena C., Tsang K.Y., Fernando R.I. et al. The human T-box mesodermal transcription factor Brachyury is a candidate target for T-cell-mediated cancer immunotherapy // Clin. Cancer Res. 2007. V. 13 (8). P. 2471–2478.
  53. Polev D.E., Karnaukhova I.K., Krukovskaya L.L., Kozlov A.P. ELFN1-AS1: a novel primate gene with possible microRNA function expressed predominantly in human tumors // BioMed. Res. Internat. 2014. V. 2014. 398097.
  54. Putnam N.H., Srivastava M., Hellsten U. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization // Science. 2007. V. 317 (5834). P. 86–94. https://doi.org/10.1126/science.1139158
  55. Radtke A.J., Postovalova E., Varlamova A. et al. Multi-omic profiling of follicular lymphoma reveals changes in tissue architecture and enhanced stromal remodeling in high-risk patients // Cancer Cell. 2024. V. 42 (3). P. 444–463. https://doi.org/10.1016/j.ccell.2024.02.001
  56. Reich D., Green R.E., Kircher M. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia // Nature. 2010. V. 468 (7327). P. 1053–1060. https://doi.org/10.1038/nature09710
  57. Release M36 (GRCm39). https://www.gencodegenes.org/mouse/
  58. Release 47 (GRCh38.p14). https://www.gencodegenes.org/human/
  59. Rensch G., Warren W.C., Henson M.S. et al. Genomic architecture and evolution of the blue whale // Genome Biol. 2022. V. 23. P. 95. https://doi.org/10.1186/s13059-022-02695-9
  60. Samusik N., Galachyants Y., Kozlov A.P. Analysis of evolutionary novelty of tumor-specifically expressed sequences // Russ. J. Genet. Appl. Res. 2011. V. 1 (2). P. 138– 148.
  61. Samusik N., Krukovskaya L., Meln I. et al. PBOV1 is a human de novo gene with tumor-specific expression that is associated with a positive clinical outcome of cancer // PLoS One. 2013. V. 8 (2). e56162.
  62. Session A.M., Uno Y., Kwon T. et al. Genome evolution in the allotetraploid frog Xenopus laevis // Nature. 2016. V. 538 (7625). P. 336–343.
  63. Shaffer H.B., Minx P., Warren D.E. et al. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage // Genome Biol. 2013. V. 14 (3). R28. https://doi.org/10.1186/gb-2013-14-3-r28
  64. Simakov O., Marletaz F., Cho S.J. et al. Insights into bilaterian evolution from three spiralian genomes // Nature. 2013. V. 493 (7433). P. 526–531. https://doi.org/10.1038/nature12368
  65. Smith J.J., Kuraku S., Holt C. et al. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution // Nat. Gen. 2013. V. 45 (4). P. 415–421. https://doi.org/10.1038/ng.2568
  66. Srivastava M., Simakov O., Chapman J. et al. The Amphimedon queenslandica genome and the evolution of animal complexity // Nature. 2010. V. 466 (7307). P. 720–726. https://doi.org/10.1038/nature09201
  67. Streicher J.W. The genome sequence of the common frog, Rana temporaria Linnaeus 1758 // Wellcome Open Res. 2021. V. 6. 286. https://doi.org/10.12688/wellcomeopenres.17296.1
  68. The C. elegans sequencing consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology // Science. 1998. V. 282 (5396). P. 2012–2018. https://doi.org/10.1126/science.282.5396.2012
  69. The Chimpanzee sequencing and analysis consortium. Initial sequence of the chimpanzee genome and comparison with the human genome // Nature. 2005. V. 437 (7055). P. 69–87. https://doi.org/10.1038/nature04072
  70. Venkatesh B., Kirkness E.F., Loh Y.H.E. et al. Elephant shark genome provides unique insights into gnathostome evolution // Nature. 2014. V. 505 (7482). P. 174–179. https://doi.org/10.1038/nature12826
  71. Warren W.C., Krestov G., Castoe T.A. et al. Genome analysis of the grey mouse lemur (Microcebus murinus) // Genome Res. 2005. V. 15 (12). P. 1749–1760. https://doi.org/10.1101/gr.3309705
  72. Warren W.C., Clayton D.F., Ellegren H. et al. The genome of a songbird // Nature. 2010. V. 464 (7289). P. 757–762. https://doi.org/10.1038/nature08819
  73. Waterston R.H., Lindblad-Toh K., Birney E. et al. Initial sequencing and comparative analysis of the mouse genome // Nature. 2002. V. 420 (6915). P. 520–562. https://doi.org/10.1038/nature01262
  74. Zaitsev A., Chelushkin M., Dyikanov D. et al. Precise reconstruction of the TME using bulk RNA-seq and a machine learning algorithm trained on artificial transcriptomes // Canc. Cell. 2022. V. 40 (8). P. 879–894. https://doi.org/10.1016/j.ccell.2022.07.006
  75. Zhang G., Fang X., Guo X. et al. The oyster genome reveals stress adaptation and complexity of shell formation // Nature. 2012. V. 490 (7418). P. 49–54. https://doi.org/10.1038/nature11413
  76. Zhang Y.E., Long M. New genes contribute to genetic and phenotypic novelties in human evolution // Curr. Opin. Genet. Dev. 2014. V. 29. P. 90–96.

Supplementary files

Supplementary Files
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2. Fig. 1. Genome sizes of prokaryotes and unicellular eukaryotes.

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3. Fig. 2. Number of protein-coding genes in prokaryotes and unicellular eukaryotes.

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4. Fig. 3. Genome size of unicellular and multicellular eukaryotes.

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5. Fig. 4. Number of protein-coding genes in unicellular and multicellular eukaryotes.

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6. Fig. 5. Genome size changes in the progressive evolution of multicellular organisms.

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7. Fig. 6. Number of protein-coding genes in the progressive evolution of multicellular organisms.

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8. Fig. 7. Increase in the proportion of non-coding genome in organism evolution.

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9. Fig. 8. Photographs of talus bones from the ankle joints of five individual sheep.

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10. Fig. 9. Morphogenesis – creation of form (explanation in the text): a – pile of building materials; b – finished house built from these materials.

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11. Fig. 10. Non-malignant cells of the tumor microenvironment: a – colorectal cancer-associated macrophages. [...] (from: Inagaki et al., 2021, modified)

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