vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-25-53vavilov-4675Research ArticleМОЛЕКУЛЯРНАЯ И КЛЕТОЧНАЯ БИОЛОГИЯMOLECULAR AND CELL BIOLOGYНеклассические модели животных для изучения роли теломер в процессах старения и долголетияUnconventional animal models to study the role of telomeres in aging and longevityСиморозЕ. В.SimorozE. V.

Федеральная территoрия «Сириус», Краснoдарский край

Sirius Federal Territory, Krasnodar region

ВасилевскаяЕ.VasilevskaJ.

Федеральная территoрия «Сириус», Краснoдарский край

Sirius Federal Territory, Krasnodar region

vasilevskaya.e@talantiuspeh.ruАракелянН. А.ArakelyanN. A.

Федеральная территoрия «Сириус», Краснoдарский край

Sirius Federal Territory, Krasnodar region

МанаховА. Д.ManakhovA. D.

Федеральная территoрия «Сириус», Краснoдарский край, Moсква

Sirius Federal Territory, Krasnodar region, Moscow

РогаевЕ. И.RogaevE. I.

Федеральная территoрия «Сириус», Краснoдарский край,

Шрус6ери, США

Sirius Federal Territory, Krasnodar region, Worcester, MA, USA

Научный центр генетики и наук o жизни, Научнo-технoлoгический университет «Сириус»РоссияResearch Center for Genetics and Life Sciences, Sirius University of Science and TechnologyRussian FederationНаучный центр генетики и наук o жизни, Научнo-технoлoгический университет «Сириус»; Институт o6щей генетики им. Н.И. Вавилoва Рoссийскoй академии наукРоссияResearch Center for Genetics and Life Sciences, Sirius University of Science and Technology; Vavilov Institute of General Genetics of the Russian Academy of SciencesRussian FederationНаучный центр генетики и наук o жизни, Научнo-технoлoгический университет «Сириус»; Mедицинская шкoла Чан Mассачусетскoгo университета, департамент психиатрииРоссияResearch Center for Genetics and Life Sciences, Sirius University of Science and Technology; Department of Psychiatry, UMass Chan Medical SchoolRussian Federation202520072025294496507Copyright © Симороз Е.В., Василевская Е., Аракелян Н.А., Манахов А.Д., Рогаев Е.И., 20252025Симороз Е.В., Василевская Е., Аракелян Н.А., Манахов А.Д., Рогаев Е.И.Simoroz E.V., Vasilevska J., Arakelyan N.A., Manakhov A.D., Rogaev E.I.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4675

Укoрoчение телoмер играет важную рoль в различных клетoчных прoцессах, связанных сo старением. Онo oграничивает прoдoлжительнoсть клетoчнoй прoлиферации и активирует механизмы, связанные с пoвреждением ДНК, чтo, в свoю oчередь, привoдит к репликативнoму старению. Укoрoчение телoмер oтражает 6иoлoгический, а не хрoнoлoгический вoзраст. Mеханизм вoсстанoвления длины телoмер oсуществляется с пoмoщью фермента телoмеразы. Однакo в этoм прoцессе неo6хoдимo сo6людать 6аланс, пoскoльку из6ытoчная активнoсть телoмеразы и чрезмернo длинные хрoмoсoмы мoгут привести к развитию oнкoлoгических за6oлеваний. Предпoлагается, чтo различия в пoтенциальнoй прoдoлжительнoсти жизни мoгут 6ыть связаны с вариациями в длине теломер у осо6ей одного возраста. Tем не менее последние исследования показывают, что длина теломер может служить лишь при6лизительной оценкой скорости старения и, вероятно, не является клинически значимым маркером риска возрастных за6олеваний и смертности. Вариации в длине теломер часто о6условлены не только возрастом, но и генетическими изменениями, факторами окружающей среды, а также мета6олически затратными процессами, такими как размножение и даже масса тела. Эти факторы могут спосо6ствовать ускоренной потере теломер у некоторых видов. Существует мнение, что для изучения роли длины теломер в контексте старения и долголетия классические модели, например мышь (Mus musculus) и крыса (Rattus norvegicus domestica), не оптимальны, поскольку продолжительность жизни этих животных и длина их теломер не сопоставимы с человеческими. Целесоо6разно использовать виды с 6олее длительным жизненным циклом. В данном о6зоре рассматривается степень корреляции между длиной теломер и долголетием в различных неклассических моделях долгоживущих животных, а также их пригодность для изучения молекулярных механизмов, приводящих к истощению теломер в контексте старения. Важно помнить, что вопрос о причинно-следственной связи длины теломер с продолжительностью жизни по-прежнему тре6ует дальнейшего исследования.

The progressive shortening of telomeres is significantly implicated in various cellular processes related to aging, including the limitation of cellular proliferative lifespan through the activation of DNA damage response pathways, ultimately leading to replicative senescence. Telomere shortening is considered an indicator of biological age rather than chronological age. The restoration of telomere length is mediated by the enzyme telomerase; however, it is crucial to maintain a balance in this process, as excessive telomerase activity and overly elongated chromosomes may increase the susceptibility of individuals to cancer. It has been proposed that variations in telomere length among individuals of the same chronological age may be associated with differences in potential lifespan. However, recent studies suggest that telomere length may serve only as a rough estimate of the aging process and is likely not a clinically relevant biomarker for age-related diseases or mortality risk. Furthermore, variations in telomere length are not solely determined by chronological age; rather, they are modulated by a multitude of factors, including genetic predispositions, environmental conditions, and heightened metabolic activities such as reproduction and body weight, which may lead to increased telomere attrition in certain species. It has been argued that traditional animal models, such as the mouse (Mus musculus) and the rat (Rattus norvegicus domestica), are suboptimal for investigating the relationship between telomere length and aging, as their lifespans and telomere lengths do not adequately reflect those of humans. Consequently, it is recommended to use long-lived species as they would provide a more appropriate framework for such research initiatives. This review aims to examine the correlation between telomere length and longevity in various non-traditional long-lived animal models, evaluating their suitability for investigating the molecular mechanisms underlying telomere attrition in the context of aging. Nevertheless, the question of whether telomere length is a causative factor or a consequence of longevity remains an area that necessitates further investigation.

длина теломертеломеразастарениедолголетиенеклассические модели животныхtelomere lengthtelomeraseaginglongevityunconventional animal modelsThe research conducted by V.J. and A.N.A. was funded by the Sirius Federal Territory. Agreement 18-03, project MB-BFT-2403ReferencesAllsopp R.C., Chang E., Kashefi-Aazam M., Rogaev E.I., Piatyszek M.A., Shay J.W., Harley C.B. Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res. 1995; 220(1):194-200. doi 10.1006/excr.1995.1306Allsopp R.C., Chang E., Kashefi-Aazam M., Rogaev E.I., Piatyszek M.A., Shay J.W., Harley C.B. Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res. 1995; 220(1):194-200. doi 10.1006/excr.1995.1306Arai Y., Martin-Ruiz C.M., Takayama M., Abe Y., Takebayashi T., Koyasu S., Suematsu M., Hirose N., von Zglinicki T. Inflammation, but not telomere length, predicts successful ageing at extreme old age: a longitudinal study of semi-supercentenarians. EBioMedicine. 2015;2(10):1549-1558. doi 10.1016/j.ebiom.2015.07.029Arai Y., Martin-Ruiz C.M., Takayama M., Abe Y., Takebayashi T., Koyasu S., Suematsu M., Hirose N., von Zglinicki T. Inflammation, but not telomere length, predicts successful ageing at extreme old age: a longitudinal study of semi-supercentenarians. EBioMedicine. 2015;2(10):1549-1558. doi 10.1016/j.ebiom.2015.07.029Aramburu T., Plucinsky S., Skordalakes E. POT1-TPP1 telomere length regulation and disease. Comput Struct Biotechnol J. 2020;18:1939- 1946. doi 10.1016/j.csbj.2020.06.040Aramburu T., Plucinsky S., Skordalakes E. POT1-TPP1 telomere length regulation and disease. Comput Struct Biotechnol J. 2020;18:1939- 1946. doi 10.1016/j.csbj.2020.06.040Armstrong E., Boonekamp J. Does oxidative stress shorten telomeres in vivo? A meta-analysis. Ageing Res Rev. 2023;85:101854. doi 10.1016/j.arr.2023.101854Armstrong E., Boonekamp J. Does oxidative stress shorten telomeres in vivo? A meta-analysis. Ageing Res Rev. 2023;85:101854. doi 10.1016/j.arr.2023.101854Atzmon G., Cho M., Cawthon R.M., Budagov T., Katz M., Yang X., Siegel G., Bergman A., Huffman D.M., Schechter C.B., Wright W.E., Shay J.W., Barzilai N., Govindaraju D.R., Suh Y. Genetic variation in human telomerase is associated with telomere length in Ashkenazi centenarians. Proc Natl Acad Sci USA. 2010;107(1):1710-1717. doi 10.1073/pnas.0906191106Atzmon G., Cho M., Cawthon R.M., Budagov T., Katz M., Yang X., Siegel G., Bergman A., Huffman D.M., Schechter C.B., Wright W.E., Shay J.W., Barzilai N., Govindaraju D.R., Suh Y. Genetic variation in human telomerase is associated with telomere length in Ashkenazi centenarians. Proc Natl Acad Sci USA. 2010;107(1):1710-1717. doi 10.1073/pnas.0906191106Bartas M., Červeň J., Valková N., Volná A., Dobrovolná M., Šislerová L., Baldvinsson H., Pečinka P., Brázda V. RNA analysis of the longest living vertebrate Greenland shark revealed an abundance of LINE-like elements in its transcriptome. Czech Polar Rep. 2023;13(2):210-227. doi 10.5817/CPR2023-2-17Bartas M., Červeň J., Valková N., Volná A., Dobrovolná M., Šislerová L., Baldvinsson H., Pečinka P., Brázda V. RNA analysis of the longest living vertebrate Greenland shark revealed an abundance of LINE-like elements in its transcriptome. Czech Polar Rep. 2023;13(2):210-227. doi 10.5817/CPR2023-2-17Basova L., Begum S., Strahl J., Sukhotin A., Brey T., Philipp E., Abele D. Age-dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different lifespans. Aquat Biol. 2012;14(2):141-152. doi 10.3354/ab00387Basova L., Begum S., Strahl J., Sukhotin A., Brey T., Philipp E., Abele D. Age-dependent patterns of antioxidants in Arctica islandica from six regionally separate populations with different lifespans. Aquat Biol. 2012;14(2):141-152. doi 10.3354/ab00387Bernardes De Jesus B., Vera E., Schneeberger K., Tejera A.M., Ayuso E., Bosch F., Blasco M.A. Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer. EMBO Mol Med. 2012;4(8):691-704. doi 10.1002/emmm.201200245Bernardes De Jesus B., Vera E., Schneeberger K., Tejera A.M., Ayuso E., Bosch F., Blasco M.A. Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer. EMBO Mol Med. 2012;4(8):691-704. doi 10.1002/emmm.201200245Bowden T.J., Kraev I., Lange S. Extracellular vesicles and post-translational protein deimination signatures in haemolymph of the American lobster (Homarus americanus). Fish Shellfish Immunol. 2020; 106:79-102. doi 10.1016/j.fsi.2020.06.053Bowden T.J., Kraev I., Lange S. Extracellular vesicles and post-translational protein deimination signatures in haemolymph of the American lobster (Homarus americanus). Fish Shellfish Immunol. 2020; 106:79-102. doi 10.1016/j.fsi.2020.06.053Buddhachat K., Kriangwanich W., Kumoun I., Brown J.L., Chailangkarn S., Somgird C., Thitaram C., Prasitwattanaseree S., Nganvongpanit K. Telomeric attrition with increasing age in short- (Chihuahua dog) and long- (Asian elephant) life span animals. Kafkas Univ Vet Fak Derg. 2017;23(4):643-649. doi 10.9775/kvfd.2017.17504Buddhachat K., Kriangwanich W., Kumoun I., Brown J.L., Chailangkarn S., Somgird C., Thitaram C., Prasitwattanaseree S., Nganvongpanit K. Telomeric attrition with increasing age in short- (Chihuahua dog) and long- (Asian elephant) life span animals. Kafkas Univ Vet Fak Derg. 2017;23(4):643-649. doi 10.9775/kvfd.2017.17504Buddhachat K., Brown J.L., Kaewkool M., Poommouang A., Kaewmong P., Kittiwattanawong K., Nganvongpanit K. Life expectancy in marine mammals is unrelated to telomere length but is associated with body size. Front Genet. 2021;12:737860. doi 10.3389/fgene.2021.737860Buddhachat K., Brown J.L., Kaewkool M., Poommouang A., Kaewmong P., Kittiwattanawong K., Nganvongpanit K. Life expectancy in marine mammals is unrelated to telomere length but is associated with body size. Front Genet. 2021;12:737860. doi 10.3389/fgene.2021.737860Bythell J.C., Brown B.E., Kirkwood T.B.L. Do reef corals age? Biol Rev Camb Philos Soc. 2018;93(2):1192-1202. doi 10.1111/brv.12391Bythell J.C., Brown B.E., Kirkwood T.B.L. Do reef corals age? Biol Rev Camb Philos Soc. 2018;93(2):1192-1202. doi 10.1111/brv.12391Calado R.T., Dumitriu B. Telomere dynamics in mice and humans. Semin Hematol. 2013;50(2):165-174. doi 10.1053/j.seminhematol.2013.03.030Calado R.T., Dumitriu B. Telomere dynamics in mice and humans. Semin Hematol. 2013;50(2):165-174. doi 10.1053/j.seminhematol.2013.03.030Chusyd D.E., Ackermans N.L., Austad S.N., Hof P.R., Mielke M.M., Sherwood C.C., Allison D.B. Aging: what we can learn from elephants. Front Aging. 2021;2:726714. doi 10.3389/fragi.2021.726714Chusyd D.E., Ackermans N.L., Austad S.N., Hof P.R., Mielke M.M., Sherwood C.C., Allison D.B. Aging: what we can learn from elephants. Front Aging. 2021;2:726714. doi 10.3389/fragi.2021.726714Crawley J.A.H., Mumby H.S., Chapman S.N., Lahdenperä M., Mar K.U., Htut W., Thura Soe A., Aung H.H., Lummaa V. Is bigger better? The relationship between size and reproduction in female Asian elephants. J Evol Biol. 2017;30(10):1836-1845. doi 10.1111/jeb.13143Crawley J.A.H., Mumby H.S., Chapman S.N., Lahdenperä M., Mar K.U., Htut W., Thura Soe A., Aung H.H., Lummaa V. Is bigger better? The relationship between size and reproduction in female Asian elephants. J Evol Biol. 2017;30(10):1836-1845. doi 10.1111/jeb.13143Criscuolo F., Dobson F.S., Schull Q. The influence of phylogeny and life history on telomere lengths and telomere rate of change among bird species: a meta‐analysis. Ecol Evol. 2021;11(19):12908-12922. doi 10.1002/ece3.7931Criscuolo F., Dobson F.S., Schull Q. The influence of phylogeny and life history on telomere lengths and telomere rate of change among bird species: a meta‐analysis. Ecol Evol. 2021;11(19):12908-12922. doi 10.1002/ece3.7931Domínguez-de-Barros A., Sifaoui I., Borecka Z., Dorta-Guerra R., Lorenzo-Morales J., Castro-Fuentes R., Córdoba-Lanús E. An approach to the effects of longevity, sexual maturity, and reproduction on telomere length and oxidative stress in different Psittacidae species. Front Genet. 2023;14:1156730. doi 10.3389/fgene.2023.1156730Domínguez-de-Barros A., Sifaoui I., Borecka Z., Dorta-Guerra R., Lorenzo-Morales J., Castro-Fuentes R., Córdoba-Lanús E. An approach to the effects of longevity, sexual maturity, and reproduction on telomere length and oxidative stress in different Psittacidae species. Front Genet. 2023;14:1156730. doi 10.3389/fgene.2023.1156730Domínguez-de-Barros A., Sifaoui I., Dorta-Guerra R., Lorenzo-Morales J., Castro-Fuentes R., Córdoba-Lanús E. Telomere- and oxidative stress dynamics in Psittacidae species with different longevity trajectories. GeroScience. 2024. doi 10.1007/s11357-024-01397-5Domínguez-de-Barros A., Sifaoui I., Dorta-Guerra R., Lorenzo-Morales J., Castro-Fuentes R., Córdoba-Lanús E. Telomere- and oxidative stress dynamics in Psittacidae species with different longevity trajectories. GeroScience. 2024. doi 10.1007/s11357-024-01397-5Du C., Anderson A., Lortie M., Parsons R., Bodnar A. Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med. 2013;63:254-263. doi 10.1016/j.freeradbiomed.2013.05.023Du C., Anderson A., Lortie M., Parsons R., Bodnar A. Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med. 2013;63:254-263. doi 10.1016/j.freeradbiomed.2013.05.023Ebert T.A. Negative senescence in sea urchins. Exp Gerontol. 2019; 122:92-98. doi 10.1016/j.exger.2019.04.018Ebert T.A. Negative senescence in sea urchins. Exp Gerontol. 2019; 122:92-98. doi 10.1016/j.exger.2019.04.018Foley N.M., Hughes G.M., Huang Z., Clarke M., Jebb D., Whelan C.V., Petit E.J., … Kerth G., Rebelo H., Rodrigues L., Puechmaille S.J., Teeling E.C. Growing old, yet staying young: the role of telomeres in bats’ exceptional longevity. Sci Adv. 2018;4(2):eaao0926. doi 10.1126/sciadv.aao0926Foley N.M., Hughes G.M., Huang Z., Clarke M., Jebb D., Whelan C.V., Petit E.J., … Kerth G., Rebelo H., Rodrigues L., Puechmaille S.J., Teeling E.C. Growing old, yet staying young: the role of telomeres in bats’ exceptional longevity. Sci Adv. 2018;4(2):eaao0926. doi 10.1126/sciadv.aao0926Foley N.M., Petit E.J., Brazier T., Finarelli J.A., Hughes G.M., Touzalin F., Puechmaille S.J., Teeling E.C. Drivers of longitudinal telomere dynamics in a long‐lived bat species, Myotis myotis. Mol Ecol. 2020;29(16):2963-2977. doi 10.1111/mec.15395Foley N.M., Petit E.J., Brazier T., Finarelli J.A., Hughes G.M., Touzalin F., Puechmaille S.J., Teeling E.C. Drivers of longitudinal telomere dynamics in a long‐lived bat species, Myotis myotis. Mol Ecol. 2020;29(16):2963-2977. doi 10.1111/mec.15395Foote C.G., Daunt F., González-Solís J., Nasir L., Phillips R.A., Monaghan P. Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav Ecol. 2011;22(1): 156-161. doi 10.1093/beheco/arq178Foote C.G., Daunt F., González-Solís J., Nasir L., Phillips R.A., Monaghan P. Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav Ecol. 2011;22(1): 156-161. doi 10.1093/beheco/arq178Francis N., Gregg T., Owen R., Ebert T., Bodnar A. Lack of age‐associated telomere shortening in long‐ and short‐lived species of sea urchins. FEBS Lett. 2006;580(19):4713-4717. doi 10.1016/j.febslet.2006.07.049Francis N., Gregg T., Owen R., Ebert T., Bodnar A. Lack of age‐associated telomere shortening in long‐ and short‐lived species of sea urchins. FEBS Lett. 2006;580(19):4713-4717. doi 10.1016/j.febslet.2006.07.049Garg K.M., Lamba V., Sanyal A., Dovih P., Chattopadhyay B. Next generation sequencing revolutionizes organismal biology research in bats. J Mol Evol. 2023;91(4):391-404. doi 10.1007/s00239-023-10107-2Garg K.M., Lamba V., Sanyal A., Dovih P., Chattopadhyay B. Next generation sequencing revolutionizes organismal biology research in bats. J Mol Evol. 2023;91(4):391-404. doi 10.1007/s00239-023-10107-2Gomes N.M.V., Ryder O.A., Houck M.L., Charter S.J., Walker W., Forsyth N.R., Austad S.N., Venditti C., Pagel M., Shay J.W., Wright W.E. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell. 2011;10(5):761-768. doi 10.1111/j.1474-9726.2011.00718.xGomes N.M.V., Ryder O.A., Houck M.L., Charter S.J., Walker W., Forsyth N.R., Austad S.N., Venditti C., Pagel M., Shay J.W., Wright W.E. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell. 2011;10(5):761-768. doi 10.1111/j.1474-9726.2011.00718.xGruber H., Schaible R., Ridgway I.D., Chow T.T., Held C., Philipp E.E.R. Telomere-independent ageing in the longest-lived noncolonial animal, Arctica islandica. Exp Gerontol. 2014;51:38-45. doi 10.1016/j.exger.2013.12.014Gruber H., Schaible R., Ridgway I.D., Chow T.T., Held C., Philipp E.E.R. Telomere-independent ageing in the longest-lived noncolonial animal, Arctica islandica. Exp Gerontol. 2014;51:38-45. doi 10.1016/j.exger.2013.12.014Gruber H., Wessels W., Boynton P., Xu J., Wohlgemuth S., Leeuwenburgh C., Qi W., Austad S.N., Schaible R., Philipp E.E.R. Age-related cellular changes in the long-lived bivalve A. islandica. Age. 2015;37(5):90. doi 10.1007/s11357-015-9831-8Gruber H., Wessels W., Boynton P., Xu J., Wohlgemuth S., Leeuwenburgh C., Qi W., Austad S.N., Schaible R., Philipp E.E.R. Age-related cellular changes in the long-lived bivalve A. islandica. Age. 2015;37(5):90. doi 10.1007/s11357-015-9831-8Harper J.M., Holmes D.J. New perspectives on avian models for studies of basic aging processes. Biomedicines. 2021;9(6):649. doi 10.3390/biomedicines9060649Harper J.M., Holmes D.J. New perspectives on avian models for studies of basic aging processes. Biomedicines. 2021;9(6):649. doi 10.3390/biomedicines9060649Haussmann M.F., Winkler D.W., Huntington C.E., Nisbet I.C.T., Vleck C.M. Telomerase expression is differentially regulated in birds of differing life span. Ann NY Acad Sci. 2004;1019(1):186-190. doi 10.1196/annals.1297.029Haussmann M.F., Winkler D.W., Huntington C.E., Nisbet I.C.T., Vleck C.M. Telomerase expression is differentially regulated in birds of differing life span. Ann NY Acad Sci. 2004;1019(1):186-190. doi 10.1196/annals.1297.029Ineson K.M., O’Shea T.J., Kilpatrick C.W., Parise K.L., Foster J.T. Ambiguities in using telomere length for age determination in two North American bat species. J Mammal. 2020;101(4):958-969. doi 10.1093/jmammal/gyaa064Ineson K.M., O’Shea T.J., Kilpatrick C.W., Parise K.L., Foster J.T. Ambiguities in using telomere length for age determination in two North American bat species. J Mammal. 2020;101(4):958-969. doi 10.1093/jmammal/gyaa064Jenner L.P., Peska V., Fulnečková J., Sýkorová E. Telomeres and their neighbors. Genes. 2022;13(9):1663. doi 10.3390/genes13091663Jenner L.P., Peska V., Fulnečková J., Sýkorová E. Telomeres and their neighbors. Genes. 2022;13(9):1663. doi 10.3390/genes13091663Kirkwood T.B.L. Evolution of ageing. Nature. 1977;270(5635):301- 304. doi 10.1038/270301a0Kirkwood T.B.L. Evolution of ageing. Nature. 1977;270(5635):301- 304. doi 10.1038/270301a0Kirkwood T.B.L., Rose M.R. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci. 1991;332(1262):15-24. doi 10.1098/rstb.1991.0028Kirkwood T.B.L., Rose M.R. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci. 1991;332(1262):15-24. doi 10.1098/rstb.1991.0028Klapper W., Kühne K., Singh K.K., Heidorn K., Parwaresch R., Krupp G. Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett. 1998;439(1-2):143-146. doi 10.1016/S0014-5793(98)01357-XKlapper W., Kühne K., Singh K.K., Heidorn K., Parwaresch R., Krupp G. Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett. 1998;439(1-2):143-146. doi 10.1016/S0014-5793(98)01357-XKoliada A.K., Krasnenkov D.S., Vaiserman A.M. Telomeric aging: mitotic clock or stress indicator? Front Genet. 2015;6:82. doi 10.3389/fgene.2015.00082Koliada A.K., Krasnenkov D.S., Vaiserman A.M. Telomeric aging: mitotic clock or stress indicator? Front Genet. 2015;6:82. doi 10.3389/fgene.2015.00082Koopman H.N., Westgate A.J., Siders Z.A. Declining fecundity and factors affecting embryo quality in the American lobster (Homarus americanus) from the Bay of Fundy. Can J Fish Aquat Sci. 2015; 72(3):352-363. doi 10.1139/cjfas-2014-0277Koopman H.N., Westgate A.J., Siders Z.A. Declining fecundity and factors affecting embryo quality in the American lobster (Homarus americanus) from the Bay of Fundy. Can J Fish Aquat Sci. 2015; 72(3):352-363. doi 10.1139/cjfas-2014-0277Lagunas-Rangel F.A. Deciphering the whale’s secrets to have a long life. Exp Gerontol. 2021;151:111425. doi 10.1016/j.exger.2021.111425Lagunas-Rangel F.A. Deciphering the whale’s secrets to have a long life. Exp Gerontol. 2021;151:111425. doi 10.1016/j.exger.2021.111425Leonida S.R.L., Bennett N.C., Leitch A.R., Faulkes C.G. Patterns of telomere length with age in African mole-rats: new insights from quantitative fluorescence in situ hybridisation (qFISH). PeerJ. 2020;8:e10498. doi 10.7717/peerj.10498Leonida S.R.L., Bennett N.C., Leitch A.R., Faulkes C.G. Patterns of telomere length with age in African mole-rats: new insights from quantitative fluorescence in situ hybridisation (qFISH). PeerJ. 2020;8:e10498. doi 10.7717/peerj.10498Lin J., Epel E. Stress and telomere shortening: insights from cellular mechanisms. Ageing Res Rev. 2022;73:101507. doi 10.1016/j.arr.2021.101507Lin J., Epel E. Stress and telomere shortening: insights from cellular mechanisms. Ageing Res Rev. 2022;73:101507. doi 10.1016/j.arr.2021.101507Louzon M., Coeurdassier M., Gimbert F., Pauget B., De Vaufleury A. Telomere dynamic in humans and animals: review and perspectives in environmental toxicology. Environ Int. 2019;131:105025. doi 10.1016/j.envint.2019.105025Louzon M., Coeurdassier M., Gimbert F., Pauget B., De Vaufleury A. Telomere dynamic in humans and animals: review and perspectives in environmental toxicology. Environ Int. 2019;131:105025. doi 10.1016/j.envint.2019.105025Miller R.A., Harper J.M., Dysko R.C., Durkee S.J., Austad S.N. Longer life spans and delayed maturation in wild-derived mice. Exp Biol Med (Maywood). 2002;227(7):500-508. doi 10.1177/153537020222700715Miller R.A., Harper J.M., Dysko R.C., Durkee S.J., Austad S.N. Longer life spans and delayed maturation in wild-derived mice. Exp Biol Med (Maywood). 2002;227(7):500-508. doi 10.1177/153537020222700715Muñoz-Lorente M.A., Cano-Martin A.C., Blasco M.A. Mice with hyper-long telomeres show less metabolic aging and longer lifespans. Nat Commun. 2019;10(1):4723. doi 10.1038/s41467-019-12664-xMuñoz-Lorente M.A., Cano-Martin A.C., Blasco M.A. Mice with hyper-long telomeres show less metabolic aging and longer lifespans. Nat Commun. 2019;10(1):4723. doi 10.1038/s41467-019-12664-xNehmens M.C., Varney R.M., Janosik A.M., Ebert D.A. An exploratory study of telomere length in the deep-sea shark, Etmopterus granulosus. Front Mar Sci. 2021;8:642872. doi 10.3389/fmars.2021.642872Nehmens M.C., Varney R.M., Janosik A.M., Ebert D.A. An exploratory study of telomere length in the deep-sea shark, Etmopterus granulosus. Front Mar Sci. 2021;8:642872. doi 10.3389/fmars.2021.642872Nguyen T.H.D. Structural biology of human telomerase: progress and prospects. Biochem Soc Trans. 2021;49(5):1927-1939. doi 10.1042/BST20200042Nguyen T.H.D. Structural biology of human telomerase: progress and prospects. Biochem Soc Trans. 2021;49(5):1927-1939. doi 10.1042/BST20200042Nielsen J., Hedeholm R.B., Heinemeier J., Bushnell P.G., Christiansen J.S., Olsen J., Ramsey C.B., Brill R.W., Simon M., Steffensen K.F., Steffensen J.F. Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science. 2016;353(6300):702-704. doi 10.1126/science.aaf1703Nielsen J., Hedeholm R.B., Heinemeier J., Bushnell P.G., Christiansen J.S., Olsen J., Ramsey C.B., Brill R.W., Simon M., Steffensen K.F., Steffensen J.F. Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science. 2016;353(6300):702-704. doi 10.1126/science.aaf1703Olsen M.T., Robbins J., Bérubé M., Rew M.B., Palsbøll P.J. Utility of telomere length measurements for age determination of humpback whales. NAMMCO Sci Publ. 2014;10. doi 10.7557/3.3194Olsen M.T., Robbins J., Bérubé M., Rew M.B., Palsbøll P.J. Utility of telomere length measurements for age determination of humpback whales. NAMMCO Sci Publ. 2014;10. doi 10.7557/3.3194Polinski J.M., Kron N., Smith D.R., Bodnar A.G. Unique age-related transcriptional signature in the nervous system of the long-lived red sea urchin Mesocentrotus franciscanus. Sci Rep. 2020;10(1):9182. doi 10.1038/s41598-020-66052-3Polinski J.M., Kron N., Smith D.R., Bodnar A.G. Unique age-related transcriptional signature in the nervous system of the long-lived red sea urchin Mesocentrotus franciscanus. Sci Rep. 2020;10(1):9182. doi 10.1038/s41598-020-66052-3Polinski J.M., Zimin A.V., Clark K.F., Kohn A.B., Sadowski N., Timp W., Ptitsyn A., Khanna P., Romanova D.Y., Williams P., Greenwood S.J., Moroz L.L., Walt D.R., Bodnar A.G. The American lobster genome reveals insights on longevity, neural, and immune adaptations. Sci Adv. 2021;7(26):eabe8290. doi 10.1126/sciadv.abe8290Polinski J.M., Zimin A.V., Clark K.F., Kohn A.B., Sadowski N., Timp W., Ptitsyn A., Khanna P., Romanova D.Y., Williams P., Greenwood S.J., Moroz L.L., Walt D.R., Bodnar A.G. The American lobster genome reveals insights on longevity, neural, and immune adaptations. Sci Adv. 2021;7(26):eabe8290. doi 10.1126/sciadv.abe8290Polinski J.M., Castellano K.R., Buckley K.M., Bodnar A.G. Genomic signatures of exceptional longevity and negligible aging in the longlived red sea urchin. Cell Rep. 2024;43(4):114021. doi 10.1016/j.celrep.2024.114021Polinski J.M., Castellano K.R., Buckley K.M., Bodnar A.G. Genomic signatures of exceptional longevity and negligible aging in the longlived red sea urchin. Cell Rep. 2024;43(4):114021. doi 10.1016/j.celrep.2024.114021Puechmaille S.J., Frick W.F., Kunz T.H., Racey P.A., Voigt C.C., Wibbelt G., Teeling E.C. White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol Evol. 2011;26(11):570-576. doi 10.1016/j.tree.2011.06.013Puechmaille S.J., Frick W.F., Kunz T.H., Racey P.A., Voigt C.C., Wibbelt G., Teeling E.C. White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol Evol. 2011;26(11):570-576. doi 10.1016/j.tree.2011.06.013Roark E.B., Guilderson T.P., Dunbar R.B., Fallon S.J., Mucciarone D.A. Extreme longevity in proteinaceous deep-sea corals. Proc Natl Acad Sci USA. 2009;106(13):5204-5208. doi 10.1073/pnas.0810875106Roark E.B., Guilderson T.P., Dunbar R.B., Fallon S.J., Mucciarone D.A. Extreme longevity in proteinaceous deep-sea corals. Proc Natl Acad Sci USA. 2009;106(13):5204-5208. doi 10.1073/pnas.0810875106Rossiello F., Jurk D., Passos J.F., d’Adda Di Fagagna F. Telomere dysfunction in ageing and age-related diseases. Nat Cell Biol. 2022; 24(2):135-147. doi 10.1038/s41556-022-00842-xRossiello F., Jurk D., Passos J.F., d’Adda Di Fagagna F. Telomere dysfunction in ageing and age-related diseases. Nat Cell Biol. 2022; 24(2):135-147. doi 10.1038/s41556-022-00842-xRouan A., Pousse M., Tambutté E., Djerbi N., Zozaya W., Capasso L., Zoccola D., Tambutté S., Gilson E. Telomere dysfunction is associated with dark‐induced bleaching in the reef coral Stylophora pistillata. Mol Ecol. 2022;31(23):6087-6099. doi 10.1111/mec.16199Rouan A., Pousse M., Tambutté E., Djerbi N., Zozaya W., Capasso L., Zoccola D., Tambutté S., Gilson E. Telomere dysfunction is associated with dark‐induced bleaching in the reef coral Stylophora pistillata. Mol Ecol. 2022;31(23):6087-6099. doi 10.1111/mec.16199Rouan A., Pousse M., Djerbi N., Porro B., Bourdin G., Carradec Q., Hume B.C., … Furla P., Voolstra C.R., Forcioli D., Lombard F., Gilson E. Telomere DNA length regulation is influenced by seasonal temperature differences in short-lived but not in long-lived reef-building corals. Nat Commun. 2023;14(1):3038. doi 10.1038/s41467-023-38499-1Rouan A., Pousse M., Djerbi N., Porro B., Bourdin G., Carradec Q., Hume B.C., … Furla P., Voolstra C.R., Forcioli D., Lombard F., Gilson E. Telomere DNA length regulation is influenced by seasonal temperature differences in short-lived but not in long-lived reef-building corals. Nat Commun. 2023;14(1):3038. doi 10.1038/s41467-023-38499-1Sahm A., Bens M., Henning Y., Vole C., Groth M., Schwab M., Hoffmann S., Platzer M., Szafranski K., Dammann P. Higher gene expression stability during aging in long-lived giant mole-rats than in short-lived rats. Aging. 2018;10(12):3938-3956. doi 10.18632/aging.101683Sahm A., Bens M., Henning Y., Vole C., Groth M., Schwab M., Hoffmann S., Platzer M., Szafranski K., Dammann P. Higher gene expression stability during aging in long-lived giant mole-rats than in short-lived rats. Aging. 2018;10(12):3938-3956. doi 10.18632/aging.101683Sea Urchin Genome Sequencing Consortium; Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., … Okwuonu G., Parker D., Pu L.-L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science. 2006;314(5801):941-952. doi 10.1126/science.1133609Sea Urchin Genome Sequencing Consortium; Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., … Okwuonu G., Parker D., Pu L.-L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science. 2006;314(5801):941-952. doi 10.1126/science.1133609Seluanov A., Chen Z., Hine C., Sasahara T.H.C., Ribeiro A.A.C.M., Catania K.C., Presgraves D.C., Gorbunova V. Telomerase activity coevolves with body mass, not lifespan. Aging Cell. 2007;6(1): 45-52. doi 10.1111/j.1474-9726.2006.00262.xSeluanov A., Chen Z., Hine C., Sasahara T.H.C., Ribeiro A.A.C.M., Catania K.C., Presgraves D.C., Gorbunova V. Telomerase activity coevolves with body mass, not lifespan. Aging Cell. 2007;6(1): 45-52. doi 10.1111/j.1474-9726.2006.00262.xSergiev P.V., Artemov A.A., Prokhortchouk E.B., Dontsova O.A., Be rezkin G.V. Genomes of Strongylocentrotus franciscanus and Lytechinus variegatus: are there any genomic explanations for the two order of magnitude difference in the lifespan of sea urchins? Aging. 2016;8(2):260-271. doi 10.18632/aging.100889Sergiev P.V., Artemov A.A., Prokhortchouk E.B., Dontsova O.A., Be rezkin G.V. Genomes of Strongylocentrotus franciscanus and Lytechinus variegatus: are there any genomic explanations for the two order of magnitude difference in the lifespan of sea urchins? Aging. 2016;8(2):260-271. doi 10.18632/aging.100889Smith A., Cook N., Cook K., Brown R., Woodgett R., Veron J., Saylor V. Field measurements of a massive Porites coral at Goolboodi (Orpheus Island), Great Barrier Reef. Sci Rep. 2021;11(1):15334. doi 10.1038/s41598-021-94818-wSmith A., Cook N., Cook K., Brown R., Woodgett R., Veron J., Saylor V. Field measurements of a massive Porites coral at Goolboodi (Orpheus Island), Great Barrier Reef. Sci Rep. 2021;11(1):15334. doi 10.1038/s41598-021-94818-wSmoom R., May C.L., Ortiz V., Tigue M., Kolev H.M., Rowe M., Reizel Y., Morgan A., Egyes N., Lichtental D., Skordalakes E., Kaestner K.H., Tzfati Y. Telomouse – a mouse model with humanlength telomeres generated by a single amino acid change in RTEL1. Nat Commun. 2023;14(1):6708. doi 10.1038/s41467-023-42534-6Smoom R., May C.L., Ortiz V., Tigue M., Kolev H.M., Rowe M., Reizel Y., Morgan A., Egyes N., Lichtental D., Skordalakes E., Kaestner K.H., Tzfati Y. Telomouse – a mouse model with humanlength telomeres generated by a single amino acid change in RTEL1. Nat Commun. 2023;14(1):6708. doi 10.1038/s41467-023-42534-6Terry D.F., Nolan V.G., Andersen S.L., Perls T.T., Cawthon R. Association of longer telomeres with better health in centenarians. J Gerontol A Biol Sci Med Sci. 2008;63(8):809-812. doi 10.1093/gerona/63.8.809Terry D.F., Nolan V.G., Andersen S.L., Perls T.T., Cawthon R. Association of longer telomeres with better health in centenarians. J Gerontol A Biol Sci Med Sci. 2008;63(8):809-812. doi 10.1093/gerona/63.8.809Tricola G.M., Simons M.J.P., Atema E., Boughton R.K., Brown J.L., Dearborn D.C., Divoky G., … Wheelwright N.T., Winkler D.W., Young R., Vleck C.M., Haussmann M.F. The rate of telomere loss is related to maximum lifespan in birds. Phil Trans R Soc B. 2018; 373(1741):20160445. doi 10.1098/rstb.2016.0445Tricola G.M., Simons M.J.P., Atema E., Boughton R.K., Brown J.L., Dearborn D.C., Divoky G., … Wheelwright N.T., Winkler D.W., Young R., Vleck C.M., Haussmann M.F. The rate of telomere loss is related to maximum lifespan in birds. Phil Trans R Soc B. 2018; 373(1741):20160445. doi 10.1098/rstb.2016.0445Tsuta H., Shinzato C., Satoh N., Hidaka M. Telomere shortening in the colonial coral Acropora digitifera during development. Zoolog Sci. 2014;31(3):129-134. doi 10.2108/zsj.31.129Tsuta H., Shinzato C., Satoh N., Hidaka M. Telomere shortening in the colonial coral Acropora digitifera during development. Zoolog Sci. 2014;31(3):129-134. doi 10.2108/zsj.31.129Vera E., Bernardes de Jesus B., Foronda M., Flores J.M., Blasco M.A. The rate of increase of short telomeres predicts longevity in mammals. Cell Rep. 2012;2(4):732-737. doi 10.1016/j.celrep.2012.08.023Vera E., Bernardes de Jesus B., Foronda M., Flores J.M., Blasco M.A. The rate of increase of short telomeres predicts longevity in mammals. Cell Rep. 2012;2(4):732-737. doi 10.1016/j.celrep.2012.08.023Yang W., Hu Y., Cui S. Fighting with aging: the secret for keeping health and longevity of naked mole rats. Aging Dis. 2024;16(1): 137-145. doi 10.14336/AD.2024.0109Yang W., Hu Y., Cui S. Fighting with aging: the secret for keeping health and longevity of naked mole rats. Aging Dis. 2024;16(1): 137-145. doi 10.14336/AD.2024.0109Young A.J. The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing. Phil Trans R Soc B. 2018; 373(1741):20160452. doi 10.1098/rstb.2016.0452Young A.J. The role of telomeres in the mechanisms and evolution of life-history trade-offs and ageing. Phil Trans R Soc B. 2018; 373(1741):20160452. doi 10.1098/rstb.2016.0452Zade N.H., Khattar E. POT1 mutations cause differential effects on telomere length leading to opposing disease phenotypes. J Cell Physiol. 2023;238(6):1237-1255. doi 10.1002/jcp.31034Zade N.H., Khattar E. POT1 mutations cause differential effects on telomere length leading to opposing disease phenotypes. J Cell Physiol. 2023;238(6):1237-1255. doi 10.1002/jcp.31034Zaug A.J., Goodrich K.J., Song J.J., Sullivan A.E., Cech T.R. Reconstitution of a telomeric replicon organized by CST. Nature. 2022; 608(7924):819-825. doi 10.1038/s41586-022-04930-8Zaug A.J., Goodrich K.J., Song J.J., Sullivan A.E., Cech T.R. Reconstitution of a telomeric replicon organized by CST. Nature. 2022; 608(7924):819-825. doi 10.1038/s41586-022-04930-8

The authors declare that there are no conflicts of interest present.