Long-lived termite kings and queens activate telomerase in somatic organs

. 2021 Apr 28 ; 288 (1949) : 20210511. [epub] 20210421

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33878922

Kings and queens of termites, like queens of other advanced eusocial insects, are endowed with admirable longevity, which dramatically exceeds the life expectancies of their non-reproducing nest-mates and related solitary insects. In the quest to find the mechanisms underlying the longevity of termite reproductives, we focused on somatic maintenance mediated by telomerase. This ribonucleoprotein is well established for pro-longevity functions in vertebrates, thanks primarily to its ability of telomere extension. However, its participation in lifespan regulation of insects, including the eusocial taxa, remains understudied. Here, we report a conspicuous increase of telomerase abundance and catalytic activity in the somatic organs of primary and secondary reproductives of the termite Prorhinotermes simplex and confirm a similar pattern in two other termite species. These observations stand in contrast with the telomerase downregulation characteristic for most adult somatic tissues in vertebrates and also in solitary insects and non-reproducing castes of termites. At the same time, we did not observe caste-specific differences in telomere lengths that might explain the differential longevity of termite castes. We conclude that although the telomerase activation in termite reproductives is in line with the broadly assumed association between telomerase and longevity, its direct phenotypic impact remains to be elucidated.

Zobrazit více v PubMed

Keller L, Genoud M. 1997. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958-960. (10.1038/40130) DOI

Keller L. 1998. Queen lifespan and colony characteristics in ants and termites. Insectes Soc. 45, 235-246. (10.1007/s000400050084) DOI

Jemielity S, Chapuisat M, Parker JD, Keller L. 2005. Long live the queen: studying aging in social insects. Age 27, 241-248. (10.1007/s11357-005-2916-z) PubMed DOI PMC

Korb J, Thorne B. 2017. Sociality in termites. In Comparative social evolution (eds Rubenstein DR, Abbot P), pp. 124-153. Cambridge, UK: Cambridge University Press.

Lucas ER, Keller L. 2019. The co-evolution of longevity and social life. Funct. Ecol. 34, 76-87. (10.1111/1365-2435.13445) DOI

Negroni MA, Foitzik S, Feldmeyer B. 2019. Long-lived Temnothorax ant queens switch from investment in immunity to antioxidant production with age. Sci. Rep. 9, 7270. (10.1038/s41598-019-43796-1) PubMed DOI PMC

Oettler J, Schrempf A. 2016. Fitness and aging in Cardiocondyla obscurior ant queens. Curr. Opin. Insect Sci. 16, 58-63. (10.1016/j.cois.2016.05.010) PubMed DOI

Rueppell O, Aumer D, Moritz RFA. 2016. Ties between ageing plasticity and reproductive physiology in honey bees (Apis mellifera) reveal a positive relation between fecundity and longevity as consequence of advanced social evolution. Curr. Opin. Insect Sci. 16, 64-68. (10.1016/j.cois.2016.05.009) PubMed DOI PMC

Elsner D, Meusemann K, Korb J. 2018. Longevity and transposon defense, the case of termite reproductives. Proc. Natl Acad. Sci. USA 115, 5504-5509. (10.1073/pnas.1804046115) PubMed DOI PMC

Tasaki E, Mitaka Y, Nozaki T, Kobayashi K, Matsuura K, Iuchi Y. 2018. High expression of the breast cancer susceptibility gene BRCA1 in long-lived termite kings. Aging 10, 2668-2683. (10.18632/aging.101578) PubMed DOI PMC

Tasaki E, Kobayashi K, Matsuura K, Yoshihito I. 2018. Long-lived termite queens exhibit high Cu/Zn-superoxide dismutase activity. Oxidative Med. Cell. Longev. 2018, 5127251. (10.1155/2018/5127251) PubMed DOI PMC

Tasaki E, Kobayashi K, Matsuura K, Iuchi Y. 2017. An efficient antioxidant system in a long-lived termite queen. PLoS ONE 12, e0167412. (10.1371/journal.pone.0167412) PubMed DOI PMC

Autexier C, Lue NF. 2006. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493-517. (10.1146/annurev.biochem.75.103004.142412) PubMed DOI

Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW. 1996. Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18, 173-179. (10.1002/(SICI)1520-6408(1996)18:2<173::AID-DVG10>3.0.CO;2-3) PubMed DOI

Henriques CM, Carneiro MC, Tenente IM, Jacinto A, Ferreira MG. 2013. Telomerase is required for zebrafish lifespan. PLoS Genet. 9, e1003214. (10.1371/journal.pgen.1003214) PubMed DOI PMC

Fick LJ, Fick GH, Li Z, Cao E, Bao B, Heffelfinger D, Parker HG, Ostrander EA, Riabowol K. 2012. Telomere length correlates with life span of dog breeds. Cell Rep. 2, 1530-1536. (10.1016/j.celrep.2012.11.021) PubMed DOI

Haussmann MF, Winkler DW, O'Reilly KM, Huntington CE, Nisbet ICT, Vleck CM. 2003. Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc. R. Soc. Lond. B 270, 1387-1392. (10.1098/rspb.2003.2385) PubMed DOI PMC

Salmon P, Nilsson JF, Watson H, Bensch S, Isaksson C. 2017. Selective disappearance of great tits with short telomeres in urban areas. Proc. R. Soc. B 284, 20171349. (10.1098/rspb.2017.1349) PubMed DOI PMC

Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. 2012. Telomere length in early life predicts lifespan. Proc. Natl Acad. Sci. USA 109, 1743-1748. (10.1073/pnas.1113306109) PubMed DOI PMC

Owen R, Sarkis S, Bodnar A. 2007. Developmental pattern of telomerase expression in the sand scallop, Euvola ziczac. Invertebr. Biol. 126, 40-45. (10.1111/j.1744-7410.2007.00074.x) DOI

Klapper W, Kühne K, Singh KK, Heidorn K, Parwaresch R, Krupp G. 1998. Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett. 439, 143-146. (10.1016/S0014-5793(98)01357-X) PubMed DOI

Seluanov A, Chen Z, Hine C, Sasahara THC, Ribeiro AACM, Catania KC, Presgraves DC, Gorbunova V. 2007. Telomerase activity coevolves with body mass not lifespan. Aging Cell 6, 45-52. (10.1111/j.1474-9726.2006.00262.x) PubMed DOI PMC

Raices M, Maruyama H, Dillin A, Karlseder J. 2005. Uncoupling of longevity and telomere length in C. elegans. PLoS Genet. 1, e30. (10.1371/journal.pgen.0010030) PubMed DOI PMC

Singhapol C, Pal D, Czapiewski R, Porika M, Nelson G, Saretzki GC. 2013. Mitochondrial telomerase protects cancer cells from nuclear DNA damage and apoptosis. PLoS ONE 8, e52989. (10.1371/journal.pone.0052989) PubMed DOI PMC

Ghosh A, et al. . 2012. Telomerase directly regulates NF-κB-dependent transcription. Nat. Cell Biol. 14, 1270-1281. (10.1038/ncb2621) PubMed DOI

Park JI, et al. . 2009. Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 460, 66-72. (10.1038/nature08137) PubMed DOI PMC

Saretzki G. 2014. Extra-telomeric functions of human telomerase: cancer, mitochondria and oxidative stress. Curr. Pharm. Design 20, 6386-6403. (10.2174/1381612820666140630095606) PubMed DOI

Mason JM, Randall TA, Frydrychova Capkova R. 2016. Telomerase lost? Chromosoma 125, 65-73. (10.1007/s00412-015-0528-7) PubMed DOI PMC

Jemielity S, Kimura M, Parker KM, Parker JD, Cao X, Aviv A, Keller L. 2007. Short telomeres in short-lived males: what are the molecular and evolutionary causes? Aging Cell 6, 225-233. (10.1111/j.1474-9726.2007.00279.x) PubMed DOI PMC

Korandová M, Krůček T, Vrbová K, Čapková Frydrychová R. 2014. Distribution of TTAGG-specific telomerase activity in insects. Chromosome Res. 22, 495-503. (10.1007/s10577-014-9436-6) PubMed DOI

Korandová M, Čapková Frydrychová R. 2016. Activity of telomerase and telomeric length in Apis mellifera. Chromosoma 125, 405-411. (10.1007/s00412-015-0547-4) PubMed DOI

Roisin Y. 1988. Morphology, development and evolutionary significance of the working stages in the caste system of Prorhinotermes (Insecta, Isoptera). Zoomorphology 107, 339-347. (10.1007/BF00312217) DOI

Monroy KJM, Meusemann K, Korb J. 2019. Long live the queen, the king and the commoner? Transcript expression differences between old and young in the termite Cryptotermes secundus. PLoS ONE 14, e0210371. (10.1371/journal.pone.0210371) PubMed DOI PMC

Bosoy D, Peng Y, Mian IS, Lue NF. 2003. Conserved N-terminal motifs of telomerase reverse transcriptase required for ribonucleoprotein assembly in vivo. J. Biol. Chem. 278, 3882-3890. (10.1074/jbc.M210645200) PubMed DOI

Banik SSR, Guo C, Smith AC, Margolis SS, Richardson DA, Tirado CA, Counter CM. 2002. C-terminal regions of the human telomerase catalytic subunit essential for in vivo enzyme activity. Mol. Cell Biol. 22, 6234-6246. (10.1128/MCB.22.17.6234-6246.2002) PubMed DOI PMC

Lai AG, Pouchkina-Stantcheva N, Di Donfrancesco A, Kildisiute G, Sahu S, Aboobaker AA.. 2017. The protein subunit of telomerase displays patterns of dynamic evolution and conservation across different metazoan taxa. BMC Evol. Biol. 17, 107. (10.1186/s12862-017-0949-4) PubMed DOI PMC

Terrapon N, et al. . 2014. Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5, 3636. (10.1038/ncomms4636) PubMed DOI

Harrison MC, et al. . 2018. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nat. Ecol. Evol. 2, 557-566. (10.1038/s41559-017-0459-1) PubMed DOI PMC

Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR. 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567. (10.1126/science.276.5312.561) PubMed DOI

Jakob S, Schroeder P, Lukosz M, Buchner N, Spyridopoulos I, Altschmied J, Haendeler J. 2008. Nuclear protein tyrosine phosphatase Shp-2 is one important negative regulator of nuclear export of telomerase reverse transcriptase. J. Biol. Chem. 283, 33 155-33 161. (10.1074/jbc.M805138200) PubMed DOI PMC

Drosopoulos WC, Prasad VR. 2007. The active site residue Valine 867 in human telomerase reverse transcriptase influences nucleotide incorporation and fidelity. Nucleic Acids Res. 35, 1155-1168. (10.1093/nar/gkm002) PubMed DOI PMC

Avin BA, Umbricht CB, Zeiger MA. 2016. Human telomerase reverse transcriptase regulation by DNA methylation, transcription factor binding and alternative splicing (Review). Int. J. Oncol. 49, 2199-2205. (10.3892/ijo.2016.3743) PubMed DOI PMC

Tan TC, Rahman R, Jaber-Hijazi F, Felix DA, Chen C, Louis EJ, Aboobaker A. 2012. Telomere maintenance and telomerase activity are differentially regulated in asexual and sexual worms. Proc. Natl Acad. Sci. USA 109, 4209-4214. (10.1073/pnas.1118885109) PubMed DOI PMC

Bernhofer M, Goldberg T, Wolf S, Ahmed M, Zaugg J, Boden M, Rost B. 2018. NLSdb—major update for database of nuclear localization signals and nuclear export signals. Nucleic Acids Res. 46, D503-D508. (10.1093/nar/gkx1021) PubMed DOI PMC

Izard JW, Kendall DA. 1994. Signal peptides: exquisitely designed transport promoters. Mol. Microbiol. 13, 765-773. (10.1111/j.1365-2958.1994.tb00469.x.) PubMed DOI

Kuznetsova V, Grozeva S, Gokhman V. 2020. Telomere structure in insects: a review. J. Zool. Syst. Evol. Res. 58, 127-158. (10.1111/jzs.12332) DOI

Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fujiwara H. 1993. Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol. Cell Biol. 13, 1424-1432. (10.1128/mcb.13.3.1424) PubMed DOI PMC

Sahara K, Marec F, Traut W. 1999. TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 7, 449-460. (10.1023/A:1009297729547) PubMed DOI

Frydrychová R, Grossmann P, Trubac P, Vitkova M, Marec FE. 2004. Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47, 163-178. (10.1139/g03-100) PubMed DOI

Mohan KN, Rani BS, Kulashreshta PS, Kadandale JS. 2011. Characterization of TTAGG telomeric repeats, their interstitial occurrence and constitutively active telomerase in the mealybug Planococcus lilacinus (Homoptera; Coccoidea). Chromosoma 120, 165-175. (10.1007/s00412-010-0299-0) PubMed DOI

Sasaki T, Fujiwara H. 2000. Detection and distribution patterns of telomerase activity in insects. Eur. J. Biochem. 267, 3025-3031. (10.1046/j.1432-1033.2000.01323.x) PubMed DOI

Koubová J, Jehlík T, Kodrík D, Sábová M, Šima P, Sehadová H, Závodská R, Frydrychová Čapková R. 2019. Telomerase activity is upregulated in the fat bodies of pre-diapause bumblebee queens (Bombus terrestris). Insect Biochem. Mol. Biol. 115, 103241. (10.1016/j.ibmb.2019.103241) PubMed DOI

Nozaki T, Matsuura K. 2016. Termite queens have disproportionately more DNA in their fat body cells: reproductive division of labor and endoreduplication. Entomol. Sci. 19, 67-71. (10.1111/ens.12156) DOI

Nozaki T, Matsuura K. 2019. Evolutionary relationship of fat body endoreduplication and queen fecundity in termites. Ecol. Evol. 9, 11 684-11 694. (10.1002/ece3.5664) PubMed DOI PMC

Tasaki E, Sakurai H, Nitao M, Matsuura K, Iuchi Y. 2017. Uric acid, an important antioxidant contributing to survival in termites. PLoS ONE 12, e0179426. (10.1371/journal.pone.0179426) PubMed DOI PMC

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.c.5368978

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...