Transcript level of telomerase reverse-transcriptase (TERT) gene in the rainbow trout (Oncorhynchus mykiss) eggs with different developmental competence for gynogenesis.
Aquaculture
Fish reproduction
Gynogenesis
Maternal transcriptome
Telomerase
Telomeres
Journal
Journal of applied genetics
ISSN: 2190-3883
Titre abrégé: J Appl Genet
Pays: England
ID NLM: 9514582
Informations de publication
Date de publication:
26 Jun 2024
26 Jun 2024
Historique:
received:
23
01
2024
accepted:
18
06
2024
revised:
06
06
2024
medline:
26
6
2024
pubmed:
26
6
2024
entrez:
26
6
2024
Statut:
aheadofprint
Résumé
Expression of the telomerase reverse-transcriptase (TERT) gene and activity of telomerase have been reported in the somatic tissues and gonads in fish irrespective of their age and size. Nevertheless, little is known about TERT expression in the fish eggs. In the current study, the presence of the TERT transcripts was confirmed in the rainbow trout ovulated eggs before and after activation with nonirradiated and UV-irradiated (gynogenesis) sperm. Eggs originating from eight females had high and comparable quality expressed by similar hatching rates. However, survival of the gynogenetic larvae that hatched from eggs activated with UV-irradiated sperm and further exposed to the high hydrostatic pressure (HHP) shock for duplication of the maternal chromosomes varied between females from 2.1 ± 0.4 to 40.5 ± 2.2%. Increased level of TERT transcripts was observed in eggs originating from two females, and gametes from only one of them showed improved competence for gynogenesis (27.3 ± 1.9%). In turn, eggs from the female that exhibited the highest survival after gynogenetic activation were characterized by the lowest expression of the TERT gene. Telomerase in rainbow trout eggs may compensate erosion of the telomeres during early embryonic development; however, its upregulation does not assure better development after gynogenetic activation.
Identifiants
pubmed: 38922511
doi: 10.1007/s13353-024-00887-8
pii: 10.1007/s13353-024-00887-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Narodowe Centrum Nauki
ID : 2020/39/B/NZ9/00865
Informations de copyright
© 2024. The Author(s).
Références
Anchelin M, Murcia L, Alcaraz-Pérez F, García-Navarro EM, Cayuela ML (2011) Behaviour of telomere and telomerase during aging and regeneration in zebrafish. PLoS One 6:e16955
pubmed: 21347393
pmcid: 3036734
doi: 10.1371/journal.pone.0016955
Arai K (2001) Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197:205–228. https://doi.org/10.1016/S0044-8486(01)00588-9
doi: 10.1016/S0044-8486(01)00588-9
Betts DH, King WA (1999) Telomerase activity and telomere detection during early bovine development. Dev Genet 25:397–403
pubmed: 10570471
doi: 10.1002/(SICI)1520-6408(1999)25:4<397::AID-DVG13>3.0.CO;2-J
Billard R (1997) Utilisation d’un syst’eme tris-glycocolle pour tamponner le dilueurd’ins’emination pour truite. Bull Fr Piscic 264:102–112
Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573
pubmed: 1708110
doi: 10.1038/350569a0
Blackburn EH (2001) Switching and signalling at the telomere. Cell 106(6):661–673
pubmed: 11572773
doi: 10.1016/S0092-8674(01)00492-5
Blasco M, Rizen M, Greider CW, Hanahan D (1996) Differential regulation of telomerase activity and telomerase RNA during multi-stage tumorigenesis. Nat Genet 12:200–204
pubmed: 8563761
doi: 10.1038/ng0296-200
Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Wright WE (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352
pubmed: 9454332
doi: 10.1126/science.279.5349.349
Bolzan AD, Bianchi MS (2006) Telomeres, interstitial telomeric repeat sequences, and chromosomal aberrations. Mutat Res 612:189–214
pubmed: 16490380
doi: 10.1016/j.mrrev.2005.12.003
Chan SRWL, Blackburn EH (2004) Telomeres and telomerase. Phil Trans R Soc Lond B 359:109–122
doi: 10.1098/rstb.2003.1370
de Lange T (2002) Protection of mammalian telomeres. Oncogene 21:532–540
pubmed: 11850778
doi: 10.1038/sj.onc.1205080
Downs KP, Shen Y, Pasquali A, Beldorth I, Savage M, Gallier K, Garcia T, Booth RE, Walter RB (2012) Characterization of telomeres and telomerase expression in Xiphophorus. Comp Biochem Physiol C: Toxicol Pharmacol 155:89–94
pubmed: 21619941
Eisenhauer KM, Gerstein RM, Chiu CP, Conti M, Hsueh AJ (1997) Telomerase activity in female and male rat germ cells undergoing meiosis and in early embryos. Biol Reprod 56:1120–1125
pubmed: 9160709
doi: 10.1095/biolreprod56.5.1120
Elmore LW, Norris MW, Sircar S, Bright AT, McChesney PA, Winn RN, Holt SE (2008) Upregulation of telomerase function during tissue regeneration. Exp Biol Med 233:958–967
doi: 10.3181/0712-RM-345
Flint J, Craddock CF, Villegas A, Bentley DP, Williams HJ, Galanello R, Cao A, Wood WG, Ayyub H, Higgs DR (1994) Healing of broken human chromosomes by the addition of telomeric repeats. Am J Hum Genet 55:505
pubmed: 7521575
pmcid: 1918405
Francis N, Gregg T, Owen R, Ebert T, Bodnar A (2006) Lack of age-associated telomere shortening in long- and short-lived species of sea urchins. FEBS Lett 580:4713–4717. https://doi.org/10.1016/j.febslet.2006.07.049
doi: 10.1016/j.febslet.2006.07.049
pubmed: 16876792
Franek R, Baloch AR, Kaspar V, Saito T, Fujimoto T, Arai K, Psenicka M (2020) Isogenic lines in fish - a critical review. Rev Aquac 12:1412–1434. https://doi.org/10.1111/raq.12389
doi: 10.1111/raq.12389
Greider CW, Blackburn EH (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337
pubmed: 2463488
doi: 10.1038/337331a0
Harel I, Benayoun BA, Machado B, Singh PP, Hu CK, Pech MF, Valenzano DR, Zhang E, Sharp SC, Artandi SE, Brunet AA (2015) Platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate. Cell 160:1013–1026
pubmed: 25684364
pmcid: 4344913
doi: 10.1016/j.cell.2015.01.038
Hartmann N, Reichwald K, Lechel A, Graf M, Kirschner J, Dorn A, Terzibasi E, Wellner J, Platzer M, Rudolph KL et al (2009) Telomeres shorten while TERT expression increases during ageing of the short-lived fish Nothobranchius furzeri. Mech Ageing Dev 130:290–296
pubmed: 19428446
doi: 10.1016/j.mad.2009.01.003
Hatakeyama H, Yamazaki H, Nakamura KI, Izumiyama-Shimomura N, Aida J, Suzuki H, Tsuchida S, Matsuura M, Takubo K, Ishikawa N (2016) Telomere attrition and restoration in the normal teleost Oryzias latipes are linked to growth rate and telomerase activity at each life stage. Aging 8:62–76
pubmed: 26789258
pmcid: 4761714
doi: 10.18632/aging.100873
Henriques CM, Carneiro MC, Tenente IM, Jacinto A, Ferreira MG (2013) Telomerase is required for zebrafish lifespan. PLoS Genet 9:e1003214
pubmed: 23349637
pmcid: 3547866
doi: 10.1371/journal.pgen.1003214
Jagiełło K, Dobosz S, Zalewski T, Polonis M, Ocalewicz K (2018) Developmental competence of eggs produced by rainbow trout doubled haploids (DHs) and generation of the clonal lines. Reprod Domest Anim 53:1176–1183
pubmed: 29956409
doi: 10.1111/rda.13223
Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456
pubmed: 8287796
doi: 10.1242/dev.119.2.447
Klapper W, Heidorn K, Kühne K, Parwaresch R, Krupp G (1998) Telomerase activity in ‘immortal’fish. FEBS Lett 434:409–412
pubmed: 9742964
doi: 10.1016/S0014-5793(98)01020-5
Komen H, Thorgaard GA (2007) Androgenesis, gynogenesis and the production of clones in fishes. Aquaculture 269:150–173
doi: 10.1016/j.aquaculture.2007.05.009
Komen J, Bongers ABJ, Richter CJJ, van Muiswinkel WB, Huisman EA (1991) Gynogenesis in common carp (Cyprinus carpio L.) II. The production of homozygous gynogenetic clones and F
doi: 10.1016/0044-8486(91)90015-Y
Koressaar T, Lepamets M, Kaplinski L, Raime K, Andreson R, Remm M (2018) Primer3_masker: integrating masking of template sequence with primer design software. Bioinformatics 34:1937–1938
pubmed: 29360956
doi: 10.1093/bioinformatics/bty036
Liu L, Blasco MA, Trimarchi JR, Keefe DL (2002) An essential role for functional telomeres in mouse germ cells during fertilization and early development. Dev Biol 249:74–84
pubmed: 12217319
doi: 10.1006/dbio.2002.0735
Liu L, Franco S, Spyropoulos B, Moens PB, Blasco MA, Keefe DL (2004) Irregular telomeres impair meiotic synapsis and recombination in mice. PNAS 101:6496–6501
pubmed: 15084742
pmcid: 404073
doi: 10.1073/pnas.0400755101
Liu S, Zhang Y, Zhou Z, Waldbieser G, Sun F, Lu J, Zhang J, Jiang Y, Zhang H, Wang X, Rajendran KV, Khoo L, Kucuktas H, Peatman E, Liu Z (2012) Efficient assembly and annotation of the transcriptome of catfish by RNA-seq analysis of a doubled haploid homozygote. BMC Genomics 13:595
pubmed: 23127152
pmcid: 3582483
doi: 10.1186/1471-2164-13-595
Liu L, Bailey SM, Okuka M, Muñoz P, Li C, Zhou L, …, Keefe DL (2007) Telomere lengthening early in development. Nat Cell Biol 9:1436–1441
Liu Y, Zhao H, Shao F, Zhang Y, Nie H, Zhang J, …, Lu F (2023) Remodeling of maternal mRNA through poly(A) tail orchestrates human oocyte-to-embryo transition. Nat Struct Mol Biol 30:200–215
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Lund TC, Glass TJ, Tolar J, Blazar BR (2009) Expression of telomerase and telomere length are unaffected by either age or limb regeneration in Danio rerio. PLoS One 4:e7688
pubmed: 19893630
pmcid: 2766636
doi: 10.1371/journal.pone.0007688
Mantell LL, Greider CW (1994) Telomerase activity in germline and embryonic cells of Xenopus. EMBO 13:3211–3217
doi: 10.1002/j.1460-2075.1994.tb06620.x
Michalik O, Dobosz S, Zalewski T, Sapota M, Ocalewicz K (2015) Induction of gynogenetic and androgenetic haploid and doubled haploid development in the brown trout (Salmo trutta Linnaeus 1758). Reprod Domest Anim 50:256–262
pubmed: 25601334
doi: 10.1111/rda.12480
Naruse K, Ijiri K, Shima A, Egami N (1985) The production of cloned fish in the Medaka (Oryzias latipes). J Exp Zool 236:335–341
pubmed: 4086988
doi: 10.1002/jez.1402360311
Nergadze SG, Santagostino MA, Salzano A, Mondello C, Giulotto E (2007) Contribution of telomerase RNA retrotranscription to DNA double-strand break repair during mammalia genome evolution. Genome Biol 8(12):R260
pubmed: 18067655
pmcid: 2246262
doi: 10.1186/gb-2007-8-12-r260
Ocalewicz K (2023) Quality of fish eggs and production of androgenetic and gynogenetic doubled haploids (DHs). Fish Physiol Biochem 1:11
Ocalewicz K, Babiak I, Dobosz S, Nowaczyk J, Goryczko K (2004) The stability of telomereless chromosome fragments in adult androgenetic rainbow trout. J Exp Biol 207:2229–2236
pubmed: 15159428
doi: 10.1242/jeb.01007
Ocalewicz K, Dobosz S, Kuzminski H (2012) Distribution of telomeric DNA sequences on the X-radiation-induced chromosome fragments in the genome of androgenetic brook trout (Salvelinus fontinalis, Mitchill 1814). Cytogenet Genome Res 137:1–6
pubmed: 22777065
doi: 10.1159/000339330
Ocalewicz K, Gurgul A, Pawlina-Tyszko K, Szmatoła T, Jasielczuk I, Bugno-Poniewierska M, Dobosz S (2019) Induced androgenetic development in rainbow trout and transcriptome analysis of irradiated eggs. Sci Rep 9:8084
pubmed: 31147623
pmcid: 6542805
doi: 10.1038/s41598-019-44568-7
Ocalewicz K, Gurgul A, Polonis M, Dobosz S (2020) Preliminary identification of candidate genes related to survival of gynogenetic rainbow trout (Oncorhynchus mykiss) based on comparative transcriptome analysis. Animals 10:1326
pubmed: 32751994
pmcid: 7459965
doi: 10.3390/ani10081326
Panasiak L, Dobosz S, Ocalewicz K (2020) Telomere dynamics in the diploid and triploid rainbow trout (Oncorhynchus Mykiss) assessed by Q-FISH analysis. Genes 11:786
pubmed: 32668770
pmcid: 7397301
doi: 10.3390/genes11070786
Panasiak L, Kuciński M, Hliwa P, Pomianowski K, Ocalewicz K (2023) Telomerase activity in somatic tissues and ovaries of diploid and triploid rainbow trout (Oncorhynchus mykiss) females. Cells 12:1772. https://doi.org/10.3390/cells12131772
doi: 10.3390/cells12131772
pubmed: 37443805
pmcid: 10340188
Pandian TJ, Koteeswaran R (1998) Ploidy induction and sex control in fish. Hydrobiologia 384:167–243
doi: 10.1023/A:1003332526659
Pedram M, Sprung CN, Gao Q, Lo AW, Reynolds GE, Murnane JP (2006) Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol Cell Biol 26:1865–1878
pubmed: 16479005
pmcid: 1430234
doi: 10.1128/MCB.26.5.1865-1878.2006
Peterson DR, Mok HOL, Au DWT (2015) Modulation of telomerase activity in fish muscle by biological and environmental factors. Comp Biochem Physiol C: Toxicol Pharmacol 178:51–59
pubmed: 26400776
Pfennig F, Kind B, Zieschang F, Busch M, Gutzeit HO (2008) Tert expression and telomerase activity in gonads and somatic cells of the Japanese medaka (Oryzias latipes). Dev Growth Differ 50:131–141
pubmed: 18312429
doi: 10.1111/j.1440-169X.2008.00986.x
Polonis M, Fujimoto T, Dobosz S, Zalewski T, Ocalewicz K (2018) Genome incompatibility between rainbow trout (Oncorhynchus mykiss) and sea trout (Salmo trutta) and induction of the interspecies gynogenesis. J Appl Genetics 59:91–97
doi: 10.1007/s13353-017-0425-2
Quillet E, Garcia P, Guyomard R (1991) Analysis of the production of all homozygous lines of rainbow trout by gynogenesis. J Exp Biol 257:367–374
Rożyński R, Kuciński M, Dobosz S, Ocalewicz K (2023) Successful application of UV-irradiated rainbow trout (Oncorhynchus mykiss) spermatozoa to induce gynogenetic development of the European grayling (Thymallus thymallus). Aquaculture 574:739720
doi: 10.1016/j.aquaculture.2023.739720
Udroiu I, Marinaccio J, Sgura A (2022) Many functions of telomerase components: certainties, doubts, and inconsistencies. Int J Mol Sci 23:15189
pubmed: 36499514
pmcid: 9736166
doi: 10.3390/ijms232315189
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:7
doi: 10.1186/gb-2002-3-7-research0034
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
pubmed: 8934879
doi: 10.1002/(SICI)1520-6408(1996)18:2<173::AID-DVG10>3.0.CO;2-3
Xu J, Yang X (2001) Telomerase activity in early bovine embryos derived from parthenogenetic activation and nuclear transfer. Biol Rep 64:770–774
doi: 10.1095/biolreprod64.3.770
Yamada-Fukunaga T, Yamada M, Hamatani T, Chikazawa N, Ogawa S, Akutsu H, Miura T, Miyado K, Tarín JJ, Kuji N, Umezawa A, Yoshimura Y (2013) Age-associated telomere shortening in mouse oocytes. Rep Biol Endocrinol 11:108
doi: 10.1186/1477-7827-11-108
Yamaha E, Otani S, Minami A, Arai K (2002) Dorso-ventral axis perturbation in goldfish embryos caused by heat- and pressure-shock treatments for chromosomes set manipulation. Fish Sci 68:313–319
doi: 10.1046/j.1444-2906.2002.00427.x