Telomeres as dynamic structures of human genome: the effect of endogenous and exogenous factors
- Authors: Krapivin M.I.1, Sagurova Y.M.1, Efimova O.A.1, Tikhonov A.V.1, Pendina A.A.1
-
Affiliations:
- D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
- Issue: Vol 20, No 2 (2022)
- Pages: 111-140
- Section: Human ecological genetics
- URL: https://journals.rcsi.science/ecolgenet/article/view/106539
- DOI: https://doi.org/10.17816/ecogen106539
- ID: 106539
Cite item
Abstract
In this review, we summarize data on the structural and functional characteristics of human telomeres and analyze how endo- and exogenous factors influence telomere length. We elucidate the history of telomere investigation, describe their structure and functions, methods of their study. We also characterize the mechanisms of telomere lengthening and shortening. We discuss in detail endo- and exogenous factors affecting telomere length during gametogenesis, embryogenesis and in the postnatal period of human development. We describe how oxidative stress influences telomere length through guanine oxidation, single-strand breaks in DNA, decrease of telomerase activity and suppression of recombination in telomeric sequences. We conclude that the multidirectional effect of various factors, both sporadic and determined by the developmental program, ensures the dynamic equilibrium of telomere length. A shift in this balance due to increased influence of one or several factors can lead to telomere lengthening or shortening. Understanding the mechanisms underlying the telomere length changes and the critical periods of exposure to both protective and negative factors is important to contribute to the knowledge about telomere functions and to develop approaches of telomere length correction.
Full Text
##article.viewOnOriginalSite##About the authors
Mikhail I. Krapivin
D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
Author for correspondence.
Email: krapivin-mihail@mail.ru
ORCID iD: 0000-0002-1693-5973
SPIN-code: 4989-1932
Scopus Author ID: 56507166200
Junior Researcher
Russian Federation, Saint PetersburgYanina M. Sagurova
D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
Email: yanina.sagurova96@mail.ru
ORCID iD: 0000-0003-4947-8171
SPIN-code: 8908-7033
Scopus Author ID: 57212446052
Junior Researcher
Russian Federation, Saint PetersburgOlga A. Efimova
D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
Email: efimova_o82@mail.ru
ORCID iD: 0000-0003-4495-0983
SPIN-code: 6959-5014
Scopus Author ID: 14013324600
Cand. Sci. (Biol.), Head of laboratory of cytogenetics and cytogenomics of reproduction
Russian Federation, Saint PetersburgAndrey V. Tikhonov
D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
Email: tixonov5790@gmail.com
ORCID iD: 0000-0002-2557-6642
SPIN-code: 3170-2629
Scopus Author ID: 57191821068
Cand. Sci. (Biol.), Researcher
Russian Federation, Saint PetersburgAnna A. Pendina
D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology
Email: pendina@mail.ru
ORCID iD: 0000-0001-9182-9188
SPIN-code: 3123-2133
Scopus Author ID: 6506976983
Cand. Sci. (Biol.), Researcher
Russian Federation, Saint PetersburgReferences
- Moyzis RK, Buckingham JM, Cram LS, et al. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. PNAS USA. 1988;85(18):6622–6626. doi: 10.1073/pnas.85.18.6622
- De Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes and Development. 2005;19(18):2100–2110. doi: 10.1101/gad.1346005
- Azzalin CM, Reichenbach P, Khoriauli L, et al. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science. 2007;318(5851):798–801. doi: 10.1126/science.1147182
- Watson JD. Origin of concatemeric T7DNA. Nature New Biol. 1972;239(94):197–201. doi: 10.1038/newbio239197a0
- Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345(6274):458–460. doi: 10.1038/345458a0
- Vicencio JM, Galluzzi L, Tajeddine N, et al. Senescence, apoptosis or autophagy? Gerontology. 2008;54(2):92–99. doi: 10.1159/000129697
- McClintock B. The behavior in successive nuclear divisions of a chromosome broken at meiosis. PNAS USA. 1939;25(8):405. doi: 10.1073/pnas.25.8.405
- Muller HJ. The remaking of chromosomes. Collecting Net. 1938;13:181–198.
- Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25(3):585–621. doi: 10.1016/0014-4827(61)90192-6
- Olovnikov AM. A theory of marginotomy: the incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol. 1973;41(1): 181–190. doi: 10.1016/0022-5193(73)90198-7
- Szostak JW, Blackburn EH. Cloning yeast telomeres on linear plasmid vectors. Cell. 1982;29(1):245–255. doi: 10.1016/0092-8674(82)90109-X
- Lundblad V. DNA ends: maintenance of chromosome termini versus repair of double strand breaks. Mutat Res / Fundam Mol Mech Mutagen. 2000;451(1–2):227–240. doi: 10.1016/S0027-5107(00)00052-X
- Rhodes D, Fairall L, Simonsson T, et al. Telomere architecture. EMBO Rep. 2002;3(12):1139–1145. doi: 10.1093/embo-reports/kvf246
- O’Sullivan RJ, Karlseder J. Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol. 2010;11(3): 171–181. doi: 10.1038/nrm2848
- Griffith JD, Comeau L, Rosenfield S, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999;97(4):503–514. doi: 10.1016/S0092-8674(00)80760-6
- Muñoz-Jordán JL, Cross GA, de Lange T, Griffith JD. T-loops at trypanosome telomeres. EMBO J. 2001;20(3):579–588. doi: 10.1093/emboj/20.3.579
- Timashev LA, De Lange T. Characterization of t-loop formation by TRF2. Nucleus. 2020;11(1):164–177. doi: 10.1080/19491034.2020.1783782
- Parkinson GN, Lee MPH, Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature. 2002;417(6891):876–880. doi: 10.1038/nature755
- Xu Y. Chemistry in human telomere biology: structure, function and targeting of telomere DNA/RNA. Chem Soc Rev. 2011;40(5): 2719–2740. doi: 10.1039/C0CS00134A
- Spiegel J, Adhikari S, Balasubramanian S. The structure and function of DNA G-quadruplexes. Trends Chem. 2020;2(2):123–136. doi: 10.1016/j.trechm.2019.07.002
- Xu Y, Sato H, Sannohe Y, et al. Stable lariat formation based on a G-quadruplex scaffold. J Am Chem Soc. 2008;130(49):16470–16471. doi: 10.1021/ja806535j
- Dejardin J, Kingston RE. Purification of proteins associated with specific genomic Loci. Cell. 2009;136(1):175–186. doi: 10.1016/j.cell.2008.11.045
- Bailey SM, Meyne J, Chen DJ, et al. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. PNAS. 1999;96(26):14899–14904. doi: 10.1073/pnas.96.26.14899
- Doksani Y. The response to DNA damage at telomeric repeats and its consequences for telomere function. Genes. 2019;10(4):318. doi: 10.3390/genes10040318
- Dechat T, Gajewski A, Korbei B, et al. LAP2alpha and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J Cell Sci. 2004;117(25):6117–6128. doi: 10.1242/jcs.01529
- Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet. 2007;8(4):299–309. doi: 10.1038/nrg2047
- Zhong Z, Shiue L, Kaplan S, de Lange T. A mammalian factor that binds telomeric TTAGGG repeats in vitro. Mol Cell Biol. 1992;12(11):4834–4843. doi: 10.1128/mcb.12.11.4834-4843.1992
- Bianchi A, Smith S, Chong L, et al. TRF1 is a dimer and bends telomeric DNA. EMBO J. 1997;16(7):1785–1794. doi: 10.1093/emboj/16.7.1785
- Bilaud T, Brun C, Ancelin K, et al. Telomeric localization of TRF2, a novel human telobox protein. Nat Genet. 1997;17(2):236–239. doi: 10.1038/ng1097-236
- Broccoli D, Smogorzewska A, Chong L, de Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet. 1997;17(2):231–235. doi: 10.1038/ng1097-231
- Fairall L, Chapman L, Moss H, et al. Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol Cell. 2001;8(2):351–361. doi: 10.1016/S1097-2765(01)00321-5
- Court R, Chapman L, Fairall L, Rhobes D. How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep. 2005;6(1):39–45. doi: 10.1038/sj.embor.7400314
- Baumann P, Cech TR. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science. 2001;292(5519): 1171–1175. doi: 10.1126/science.1060036
- Lei M, Podell ER, Cech TR. Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat Struct Mol Biol. 2004;11(12):1223–1229. doi: 10.1038/nsmb867
- O’Connor MS, Safari A, Xin H, et al. A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly. PNAS. 2006;103(32):11874–11879. doi: 10.1073/pnas.0605303103
- Zhao Y, Hoshiyama H, Shay JW, Wright WE. Quantitative telomeric overhang determination using a double-strand specific nuclease. Nucleic Acids Res. 2008;36(3): e14. doi: 10.1093/nar/gkm1063
- Zhdanova NS, Minina JM, Rubtsov NB. Mammalian telomere biology. Mol Biol. 2012;46(4):481–495. doi: 10.1134/S0026893312040152
- Longhese MP. DNA damage response at functional and dysfunctional telomeres. Genes and Development. 2008;22(2):125–140. doi: 10.1101/gad.1626908
- Muñoz-Espín D, Serrano M. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol. 2014;15(7):482–496. doi: 10.1038/nrm3823
- Kimura M, Stone RC, Hunt SC, et al. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat Protoc. 2010;5(9):1596–1607. doi: 10.1038/nprot.2010.124
- Aubert G, Hills M, Lansdorp P. Telomere Length Measuremen-caveats and a critical assessment of the available technologies and tools. Mutat Res / Fundam Mol Mech Mutagen. 2012;730(1–2):69–67. doi: 10.1016/j.mrfmmm.2011.04.003
- Coleman J, Baird DM, Royle NJ. The plasticity of human telomeres demonstrated by a hypervariable telomere repeat array that is located on some copies of 16p and 16q. Hum Mol Genet. 1999;8(9):1637–1646. doi: 10.1093/hmg/8.9.1637
- Bryant JE, Hutchings KG, Moyzis RK, Griffith JK. Measurement of telomeric DNA content in human tissues. Biotechniques. 1997;23(3):476–478. doi: 10.2144/97233st05
- Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009;37(3): e21. doi: 10.1093/nar/gkn1027
- Vasilishina AA, Kropotov A, Spivak I, et al. Relative human telomere length quantification by real-time PCR. In: Demaria M, editor. Cellular Senescence. Methods in Molecular Biology. New York: Humana Press, 2019. Vol. 1986. P. 39–44. doi: 10.1007/978-1-4939-8931-7_5
- Ozturk S, Sozen B, Demir N. Telomere length and telomerase activity during oocyte maturation and early embryo development in mammalian species. Mol Hum Reprod. 2013;20(1):15–30. doi: 10.1093/molehr/gat055
- Baird DM, Rowson J, Wynford-Thomas D, Kipling D. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet. 2003;33(2):203–207. doi: 10.1038/ng1084
- Montpetit AJ, Alhareeri AA, Montpetit M, et al. Telomere length: a review of methods for measurement. Nurs Res. 2014;63(4):289–299. doi: 10.1097/NNR.0000000000000037
- Zijlmans JMJM, Martens UM, Poon SSS, et al. Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. PNAS. 1997;94(14):7423–7428. doi: 10.1073/pnas.94.14.7423
- Poon SSS, Martens UM, Ward RK, Lansdorp PM. Telomere length measurements using digital fluorescence microscopy. Cytometry. 1999;36(4):267–278. doi: 10.1002/(SICI)1097-0320(19990801)36:4<267::AID-CYTO1>3.0.CO;2-O
- Turner S, Wong HP, Rai J, Hartshorne GM. Telomere lengths in human oocytes, cleavage stage embryos and blastocysts. Mol Hum Reprod. 2010;16(9):685–694. doi: 10.1093/molehr/gaq048
- Turner S, Hartshorne GM. Telomere lengths in human pronuclei, oocytes and spermatozoa. Mol Hum Reprod. 2013;19(8):510–518. doi: 10.1093/molehr/gat021
- Mania A, Mantzouratou A, Delhanty JD, et al. Telomere length in human blastocysts. Reprod Biomed Online. 2014;28(5):624–637. doi: 10.1016/j.rbmo.2013.12.010
- Perner S, Brüderlein S, Hasel C, et al. Quantifying telomere lengths of human individual chromosome arms by centromere-calibrated fluorescence in situ hybridization and digital imaging. Am J Pathol. 2003;163(5):1751–1756. doi: 10.1016/S0002-9440(10)63534-1
- Aida J, Izumiyama-Shimomura N, Nakamura KI, et al. Basal cells have longest telomeres measured by tissue Q-FISH method in lingual epithelium. Exp Gerontol. 2008;43(9):833–839. doi: 10.1016/j.exger.2008.06.001
- Pendina AA, Krapivin MI, Efimova OA, et al. Telomere length in metaphase chromosomes of human triploid zygotes. Int J Mol Sci. 2021;22(11):5579. doi: 10.3390/ijms22115579
- Krapivin MI, Tikhonov AV, Efimova OA, et al. Telomere length in chromosomally normal and abnormal miscarriages and ongoing pregnancies and its association with 5-hydroxymethylcytosine patterns. Int J Mol Sci. 2021;22(12):6622. doi: 10.3390/ijms22126622
- Khavinson VKh, Pendina AA, Efimova OA, et al. Effect of peptide aedg on telomere length and mitotic index of PHA-stimulated human blood lymphocytes. Bull Exp Biol Med. 2019;168(1):141–144. doi: 10.1007/s10517-019-04664-0
- Blasco MA, Lee H-W, Hande MP, et al. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell. 1997;91(1):25–34. doi: 10.1016/S0092-8674(01)80006-4
- Gomes NMV, Ryder OA, Houck ML, et al. Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determinationnation. Aging Cell. 2011;10(5):761–768. doi: 10.1111/j.1474-9726.2011.00718.x
- Daniali L, Benetos A, Susser E, et al. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun. 2013;4(1):1597. doi: 10.1038/ncomms2602
- Ohki R, Tsurimoto T, Ishikawa F. In vitro reconstitution of the end replication problem. Mol Cell Biol. 2001;21(17):5753–5766. doi: 10.1128/MCB.21.17.5753-5766.2001
- Ohki R, Ishikawa F. Telomere-bound TRF1 and TRF2 stall the replication fork at telomeric repeats. Nucleic Acids Res. 2004;32(5):1627–1637. doi: 10.1093/nar/gkh309
- Webb CJ, Wu Y, Zakian VA. DNA repair at telomeres: keeping the ends intact. Cold Spring Harb Perspect Biol. 2013;5(6):a012666. doi: 10.1101/cshperspect.a012666
- Turner KJ, Vasu V, Griffin DK. Telomere biology and human phenotype. Cells. 2019;8(1):73. doi: 10.3390/cells8010073
- Maciejowski J, De Lange T. Telomeres in cancer: tumour suppression and genome instability. Nat Rev Mol Cell Biol. 2017;18(3): 175–186. doi: 10.1038/nrm.2016.171
- Wright WE, Piatyszek MA, Rainey WE, et al. Telomerase activity in human germline and embryonic tissues and cells. Dev Genet. 1996;18(2): 173–179. doi: 10.1002/(SICI)1520-6408(1996)18:2<173::AID-DVG10>3.0.CO;2-3
- Greider CW, Blackburn EH. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985;43(2):405–413. doi: 10.1016/0092-8674(85)90170-9
- Greider CW, Blackburn EH. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell. 1987;51(6):887–898. doi: 10.1016/0092-8674(87)90576-9
- Greider CW, Blackburn EH. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337(6205):331–337. doi: 10.1038/337331a0
- Cohen SB, Graham ME, Lovrecz GO, et al. Protein composition of catalytically active human telomerase from immortal cells. Science. 2007;315(5820):1850–1853. doi: 10.1126/science.1138596
- Dahse R, Fiedler W, Ernst G. Telomeres and telomerase: biological and clinical importance. Clin Chem. 1997;43(5):708–714. doi: 10.1093/clinchem/43.5.708
- Cristofari G, Adolf E, Reichenbach P, et al. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol Cell. 2007;27(6):882–889. doi: 10.1016/j.molcel.2007.07.020
- Mitchell JR, Cheng J, Collins K. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3' end. Mol Cell Biol. 1999;19(1):567–576. doi: 10.1128/MCB.19.1.567
- Chen J-L, Blasco MA, Greider CW. Secondary structure of vertebrate telomerase RNA. Cell. 2000;100(5):503–514. doi: 10.1016/S0092-8674(00)80687-X
- Armanios M, Blackburn EH. The telomere syndromes. Nat Rev Genet. 2012;13(10):693–704. doi: 10.1038/nrg3246
- Bilgili H, Białas AJ, Górski P, Piotrowski WJ. Telomere abnormalities in the pathobiology of idiopathic pulmonary fibrosis. J Clin Med. 2019;8(8):1232. doi: 10.3390/jcm8081232
- Calado RT, Regal JA, Kleiner DE, et al. A spectrum of severe familial liver disorders associate with telomerase mutations. PLoS ONE. 2009;4(11):e7926. doi: 10.1371/journal.pone.0007926
- Fogarty PF, Yamaguchi H, Wiestner A, et al. Late presentation of dyskeratosis congenita as apparently acquired aplastic anaemia due to mutations in telomerase RNA. Lancet. 2003;362(9396):1628–1630. doi: 10.1016/S0140-6736(03)14797-6
- Schratz KE, Gaysinskaya V, Cosner ZL, et al. Somatic reversion impacts myelodysplastic syndromes and acute myeloid leukemia evolution in the short telomere disorders. J Clin Investig. 2021;131(18): e147598. doi: 10.1172/JCI147598
- Diede SJ, Gottschling DE. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases α and δ. Cell. 1999;99(7):723–733. doi: 10.1016/S0092-8674(00)81670-0
- Marcand S, Brevet V, Mann C, Gilson E. Cell cycle restriction of telomere elongation. Curr Biol. 2000;10(8):487–490. doi: 10.1016/S0960-9822(00)00450-4
- Crees Z, Girard J, Rios Z, et al. Oligonucleotides and G-quadruplex stabilizers: targeting telomeres and telomerase in cancer therapy. Curr Pharm Des. 2014;20(41):6422–6437. doi: 10.2174/1381612820666140630100702
- Vannier JB, Pavicic-Kaltenbrunner V, Petalcorin MI, et al. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell. 2012;149(4):795–806. doi: 10.1016/j.cell.2012.03.030
- Vannier JB, Sarek G, Boulton SJ. RTEL1: functions of a disease-associated helicase. Trends Cell Biol. 2014;24(7):416–425. doi: 10.1016/j.tcb.2014.01.004
- Walne AJ, Vulliamy T, Kirwan M, et al. Constitutional mutations in RTEL1 cause severe dyskeratosis congenital. Am J Hum Genet. 2013;92(3):448–453. doi: 10.1016/j.ajhg.2013.02.001
- Teixeira MT, Arneric M, Sperisen P, et al. Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell. 2004;117(3):323–335. doi: 10.1016/s0092-8674(04)00334-4
- Van Steensel B, De Lange T. Control of telomere length by the human telomeric protein TRF1. Nature. 1997;385(6618):740–743. doi: 10.1038/385740a0
- Smogorzewska A, van Steensel B, Bianchi A, et al. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol. 2000;20(5):1659–1668. doi: 10.1128/MCB.20.5.1659-1668.2000
- Maeda T, Kurita R, Yokoo T, et al. Telomerase inhibition promotes an initial step of cell differentiation of primate embryonic stem cell. Biochem Biophys Res Commun. 2011;407(3):491–494. doi: 10.1016/j.bbrc.2011.03.044
- Saeed H, Iqtedar M. Stem cell function and maintenance — ends that matter: Role of telomeres and telomerase. J Biosci. 2013;38(3):641–649. doi: 10.1007/s12038-013-9346-3
- Collins K, Mitchell JR. Telomerase in the human organism. Oncogene. 2002;21(4):564–579. doi: 10.1038/sj.onc.1205083
- Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1992;266(5193):2011–2015. doi: 10.1126/science.7605428
- Yashima K, Maitra A, Rogers BB, et al. Expression of the RNA component of telomerase during human development and differentiation. Cell Growth Differ. 1998;9(9):805–813.
- Wright DL, Jones EL, Mayer JF, et al. Characterization of telomerase activity in the human oocyte and preimplantation embryo. Mol Hum Reprod. 2001;7(10):947–955. doi: 10.1093/molehr/7.10.947
- Izadyar F, Wong J, Maki C, et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod. 2011;26(6):1296–1306. doi: 10.1093/humrep/der026
- Reig-Viader R, Capilla L, Vila-Cejudo M, et al. Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. J Urol. 2014;194(1):171. doi: 10.1016/j.fertnstert.2014.06.005
- Liu L, Bailey SM, Okuka M, et al. Telomere lengthening early in development. Nat Cell Biol. 2007;9(12):1436–1441. doi: 10.1038/ncb1664
- Dunham MA, Neumann AA, Fasching CL, Reddel RR. Telomere maintenance by recombination in human cells. Nat Genet. 2000;26(4):447–450. doi: 10.1038/82586
- Bryan TM, Englezou A, Dalla-Pozza L, et al. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nature Med. 1997;3:1271–1274. doi: 10.1038/nm1197-1271
- Wang RC, Smogorzewska A, De Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell. 2004;119(3):355–368. doi: 10.1016/j.cell.2004.10.011
- Nabetani A, Ishikawa F. Unusual telomeric DNAs in human telomerase-negative immortalized cells. Mol Cell Biol. 2009;29(3):703–713. doi: 10.1128/MCB.00603-08
- Ogino H, Nakabayashi K, Suzuki M, et al. Release of telomeric DNA from chromosomes in immortal human cells lacking telomerase activity. Biochem Biophys Res Commun. 1998;248(2):223–227. doi: 10.1006/bbrc.1998.8875
- Perrem K, Colgin LM, Neumann AA, et al. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol Cell Biol. 2001;21(12):3862–3875. doi: 10.1128/MCB.21.12.3862-3875.2001
- Londono-Vallejo JA, Der-Sarkissian H, Cazes L, et al. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 2004;64(7):2324–2327. doi: 10.1158/0008-5472.CAN-03-4035
- Cesare AJ, Reddel RR. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet. 2010;11(5):319–430. doi: 10.1038/nrg2763
- Blagoev KB, Goodwin EH. Telomere exchange and asymmetric segregation of chromosomes can account for the unlimited proliferative potential of ALT cell populations. DNA Repair. 2008;7(2):199–204. doi: 10.1016/j.dnarep.2007.09.012
- Henson JD, Cao Y, Huschtscha LI, et al. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat Biotechnol. 2009;27(12):1181–1185. doi: 10.1038/nbt.1587
- Muntoni A, Neumann AA, Hills M, Reddel RR. Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum Mol Genet. 2009;18(6): 1017–1027. doi: 10.1093/hmg/ddn436
- De Silanes IL, Grana O, De Bonis ML, et al. Identification of TERRA locus unveils a telomere protection role through association to nearly all chromosomes. Nat Commun. 2014;5(1):1–13. doi: 10.1038/ncomms5723
- Nergadze SG, Farnung BO, Wischnewski H, et al. CpG-island promoters drive transcription of human telomeres. RNA. 2009;15(12):2186–2194. doi: 10.1261/rna.1748309
- Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol. 2008;10(2):228–236. doi: 10.1038/ncb1685
- Porro A, Feuerhahn S, Reichenbach P, Lingner J. Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol Cell Biol. 2010;30(20):4808–4817. doi: 10.1128/MCB.00460-10
- Arnoult N, Van Beneden A, Decottignies A. Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1α. Nat Struct Mol Biol. 2012;19(9):948–956. doi: 10.1038/nsmb.2364
- Sandell LL, Gottschling DE, Zakian VA. Transcription of a yeast telomere alleviates telomere position effect without affecting chromosome stability. PNAS. 1994;91(25):12061–12065. doi: 10.1073/pnas.91.25.12061
- Pfeiffer V, Lingner J. TERRA promotes telomere shortening through exonuclease 1-mediated resection of chromosome ends. PLoS Genetics. 2012;8(6):1002747. doi: 10.1371/journal.pgen.1002747
- Redon S, Reichenbach P, Lingner J. The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 2010;38(17):5797–5806. doi: 10.1093/nar/gkq296
- Redon S, Zemp I, Lingner J. A three-state model for the regulation of telomerase by TERRA and hnRNPA1. Nucleic Acids Res. 2013;41(19):9117–9128. doi: 10.1093/nar/gkt695
- Cusanelli E, Romero CAP, Chartrand P. Telomeric noncoding RNA TERRA is induced by telomere shortening to nucleate telomerase molecules at short telomeres. Mol Cell. 2013;51(6):780–791. doi: 10.1016/j.molcel.2013.08.029
- Balk B, Maicher A, Dees M, et al. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol. 2013;20(10):1199–1205. doi: 10.1038/nsmb.2662
- Pfeiffer V, Crittin J, Grolimund L, et al. The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening. EMBO J. 2013;32(21):2861–2871. doi: 10.1038/emboj.2013.217
- Aguilera A, Garcia-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol Cell. 2012;46(2):115–124. doi: 10.1016/j.molcel.2012.04.009
- Hamperl S, Cimprich KA. Conflict resolution in the genome: how transcription and replication make it work. Cell. 2016;167(6): 1455–1467. doi: 10.1016/j.cell.2016.09.053
- Gonzalo S, Garcia-Cao M, Fraga MF, et al. Role of the RB1 family in stabilizing histone methylation at constitutive heterochromatin. Nature Cell Biol. 2005;7:420–428. doi: 10.1038/ncb1235
- Garcia-Cao M, O’Sullivan R, Peters AH, et al. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet. 2004;36(1):94–99. doi: 10.1038/ng1278
- Benetti R, Garcia-Cao M, Blasco MA. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat Genet. 2007;39(2):243–250. doi: 10.1038/ng1952
- Ancelin K, Brunori M, Bauwens S, et al. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol Cell Biol. 2002;22(10):3474–3487. doi: 10.1128/MCB.22.10.3474-3487.2002
- Loayza D, De Lange T. POT1 as a terminal transducer of TRF1 telomere length control. Nature. 2003;423(6943):1013–1018. doi: 10.1038/nature01688
- Blanco R, Munoz P, Flores JM, et al. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes and Development. 2007;21(2):206–220. doi: 10.1101/gad.406207
- Netzer C, Rieger L, Brero A, et al. SALL1, the gene mutated in Townes–Brocks syndrome, encodes a transcriptional repressor which interacts with TRF1/PIN2 and localizes to pericentromeric heterochromatin. Hum Mol Genet. 2001;10(26):3017–3024. doi: 10.1093/hmg/10.26.3017
- Kaminker P, Plachot C, Kim S-H, et al. Higher-order nuclear organization in growth arrest of human mammary epithelial cells: a novel role for telomere-associated protein TIN2. J Cell Sci. 2005;118(6):1321–1330. doi: 10.1242/jcs.01709
- Brock GJR, Charlton J, Bird A. Densely methylated sequences that are preferentially localized at telomere-proximal regions of human chromosomes. Gene. 1999;240(2):269–277. doi: 10.1016/S0378-1119(99)00442-4
- Steinert S, Shay JW, Wright WE. Modification of subtelomeric DNA. Mol Cell Biol. 2004;24(10):4571–4580. doi: 10.1128/MCB.24.10.4571-4580.2004
- Yehezkel S, Segev Y, Viegas-Pequignot E, et al. Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum Mol Genet. 2008;17(18):2776–2789. doi: 10.1093/hmg/ddn177
- Ng LJ, Cropley JE, Pickett HA, Reddel RR. Telomerase activity is associated with an increase in DNA methylation at the proximal subtelomere and a reduction in telomeric transcription. Nucleic Acids Res. 2009;37(4):1152–1159. doi: 10.1093/nar/gkn1030
- Farnung BO, Brun CM, Arora R, et al. Telomerase efficiently elongates highly transcribing telomeres in human cancer cells. PLoS One. 2012;7(4): e35714. doi: 10.1371/journal.pone.0035714
- Gonzalo S, Jaco I, Fraga MF, et al. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat Cell Biol. 2006;8:416–424. doi: 10.1038/ncb1386
- Hastie ND, Dempster M, Dunlop MG., et al. Telomere reduction in human colorectal carcinoma and with ageing. Nature. 1990;346:866–868. doi: 10.1038/346866a0
- Dlouha D, Maluskova J, Kralova Lesna I, et al. Comparison of the relative telomere length measured in leukocytes and eleven different human tissues. Physiol Res. 2014;63(3):343–350. doi: 10.33549/physiolres.932856
- Lin J, Cheon J, Brown R, et al. Systematic and cell type-specific telomere length changes in subsets of lymphocytes. J Immunol Res. 2016;2016:5371050. doi: 10.1155/2016/5371050
- Keefe DL, Franco S, Liu L, et al. Telomere length predicts embryo fragmentation after in vitro fertilization in women — Toward a telomere theory of reproductive aging in women. Am J Obstet Gynecol. 2005;192(4):1256–1260. doi: 10.1016/j.ajog.2005.01.036
- Keefe DL, Liu L, Marquard K. Telomeres and aging-related meiotic dysfunction in women. Cell Mol Life Sci. 2007;64:139–143. doi: 10.1007/s00018-006-6466-z
- Treff NR, Su J, Taylor D, Scott RT Jr. Telomere DNA deficiency is associated with development of human embryonic aneuploidy. PLoS Genet. 2011;7: e1002161. doi: 10.1371/journal.pgen.1002161
- Keefe DL. Telomeres and genomic instability during early development. Eur J Med Genet. 2020;63(2):103638. doi: 10.1016/j.ejmg.2019.03.002
- Wang F, Pan X, Kalmbach K, et al. Robust measurement of telomere length in single cells. PNAS USA. 2013;110(21):1906–1912. doi: 10.1073/pnas.1306639110
- Polani PE, Crolla JA. A test of the production line hypothesis of mammalian oogenesis. Hum Genet. 1991;88(1):64–70. doi: 10.1007/BF00204931
- Liu J, Liu M, Ye X, et al. Delay in oocyte aging in mice by the antioxidant N-acetyl-Lcysteine (NAC). Hum Reprod. 2012;27(5): 1411–1420. doi: 10.1093/humrep/des019
- Cherif H, Tarry JL, Ozanne SE, Hales CN. Ageing and telomeres: A study into organ- and gender-specific telomere shortening. Nucleic Acids Res. 2003;31(5):1576–1583. doi: 10.1093/nar/gkg208
- Fitzpatrick AL, Kronmal RA, Gardner JP, et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am J Epidemiol. 2007;165(1):14–21. doi: 10.1093/aje/kwj346
- Nawrot TS, Staessen JA, Gardner JP, Aviv A. Telomere length and possible link to X chromosome. Lancet. 2004. Vol. 363, No. 9408. P. 507–510. doi: 10.1016/S0140-6736(04)15535-9
- Bischoff C, Petersen HC, Graakjaer J, et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology. 2006;17(2):190–194. doi: 10.1097/01.ede.0000199436.55248.10
- de Frutos C, Lopez-Cardona AP, Balvis NF, et al. Spermatozoa telomeres determine telomere length in early embryos and offspring. Reproduction. 2016;151(1):1–7. doi: 10.1530/REP-15-0375
- Keefe DL. Telomeres, reproductive aging, and genomic instability during early development. Reprod Sci. 2016;23(12):1612–1615. doi: 10.1177/1933719116676397
- Allsopp RC, Vaziri H, Patterson C, et al. Telomere length predicts replicative capacity of human fibroblasts. PNAS USA. 1992;89(21):10114–10118. doi: 10.1073/pnas.89.21.10114
- Baird DM, Britt-Compton B, Rowson J, et al. Telomere instability in the male germline. Hum Mol Genet. 2006;15(1):45–51. doi: 10.1093/hmg/ddi424
- Kimura M, Cherkas LF, Kato BS, et al. Offspring’s leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genetics. 2008;4(2): e37. doi: 10.1371/journal.pgen.0040037
- Aston KI, Hunt SC, Susser E, et al. Divergence of sperm and leukocyte age-dependent telomere dynamics: Implications for male-driven evolution of telomere length in humans. Mol Hum Reprod. 2012;18(11):517–522. doi: 10.1093/molehr/gas028
- Antunes DMF, Kalmbach KH, Wang F, et al. A single-cell assay for telomere DNA content shows increasing telomere length heterogeneity, as well as increasing mean telomere length in human spermatozoa with advancing age. J Assist Reprod Genet. 2015;32(11):1685–1690. doi: 10.1007/s10815-015-0574-3
- Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53. doi: 10.1530/rep.0.1210647
- Wang W, Chen H, Li R, et al. Telomerase activity is more significant for predicting the outcome of IVF treatment than telomere length in granulosa cells. Reproduction. 2014;147(5):649–657. doi: 10.1530/REP-13-0223
- Cheng E-H, Chen S-U, Lee T-H, et al. Evaluation of telomere length in cumulus cells as a potential biomarker of oocyte and embryo quality. Hum Reprod. 2013;28(4):929–936. doi: 10.1093/humrep/det004
- Bakaysa SL, Mucci LA, Slagboom PE, et al. Telomere length predicts survival independent of genetic influences. Aging Cell. 2007;6(6):769–774. doi: 10.1111/j.1474-9726.2007.00340.x
- Njajou OT, Cawthon RM, Damcott CM, et al. Telomere length is paternally inherited and is associated with parental lifespan. PNAS USA. 2007;104(29):12135–12139. doi: 10.1073/pnas.0702703104
- Graakjaer J, Bischoff C, Korsholm L, et al. The pattern of chromosome-specific variations in telomere length in humans is determined by inherited, telomere-near factors and is maintained throughout life. Mech Ageing Dev. 2003;124(5):629–640. doi: 10.1016/s0047-6374(03)00081-2
- Slagboom PE, Droog S, Boomsma DI. Genetic determination of telomere size in humans: A twin study of three age groups. Am J Hum Genet. 1994;55(5):876–882.
- Graakjaer J, Pascoe L, Der-Sarkissian H, et al. The relative lengths of individual telomeres are defined in the zygote and strictly maintained during life. Aging Cell. 2004;3(3):97–102. doi: 10.1111/j.1474-9728.2004.00093.x
- Graakjaer J, Londono-Vallejo JA, Christensen K, Kolvraa S. The pattern of chromosome-specific variations in telomere length in humans shows signs of heritability and is maintained through life. PNAS. 2006;1067(1):311–316. doi: 10.1196/annals.1354.042
- Factor-Litvak P, Susser E, Kezios K, et al. Leukocyte telomere length in newborns: implications for the role of telomeres in human disease. Pediatrics. 2016;137(4): e20153927. doi: 10.1542/peds.2015-3927
- Benetos A, Dalgard C, Labat C, et al. Sex difference in leukocyte telomere length is ablated in opposite-sex co-twins. Int J Epidemiol. 2014;43(6):1799–1805. doi: 10.1093/ije/dyu146
- Li H, Simpson ER, Liu J-P. Oestrogen, telomerase, ovarian ageing and cancer. Clin Exp Pharmacol Physiol. 2010;37(1):78–82. doi: 10.1111/j.1440-1681.2009.05238.x
- Entringer S, Epel ES, Lin J, et al. Maternal estriol concentrations in early gestation predict infant telomere length. J Clin Endocrinol Metab. 2015;100(1):267–273. doi: 10.1210/jc.2014-2744
- Martens DS, Plusquin M, Gyselaers W, et al. Maternal pre-pregnancy body mass index and newborn telomere length. BMC Med. 2016;14:148. doi: 10.1186/s12916-016-0689-0
- Entringer S, Epel ES, Lin J, et al. Maternal folate concentration in early pregnancy and newborn telomere length. Ann Nutr Metab. 2015;66:202–208. doi: 10.1159/000381925
- Kim J-H, Kim GJ, Lee D, et al. Higher maternal vitamin D concentrations are associated with longer leukocyte telomeres in newborns. Matern Child Nutr. 2018;14: e12475. doi: 10.1111/mcn.12475
- Daneels L, Martens DS, Arredouani S, et al. Maternal vitamin D and newborn telomere length. Nutrients. 2021;13(6):2012. doi: 10.3390/nu13062012
- Lau C, Anitole K, Hodes C, et al. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci. 2007;99(2): 366–394. doi: 10.1093/toxsci/kfm128
- Pan D, Shao Y, Song Y, et al. Association between maternal per- and polyfluoroalkyl substance exposure and newborn telomere length: Effect modification by birth seasons. Environ Int. 2022;161:107125. doi: 10.1016/j.envint.2022.107125
- Chen T, Zhang L, Yue J-Q, et al. Prenatal PFOS exposure induces oxidative stress and apoptosis in the lung of rat off-spring. Reprod Toxicol. 2012;33(4):538–545. doi: 10.1016/j.reprotox.2011.03.003
- Watad A, Azrielant S, Bragazzi NL, et al. Seasonality and autoimmune diseases: The contribution of the four seasons to the mosaic of autoimmunity. J Autoimmun. 2017;82:13–30. doi: 10.1016/j.jaut.2017.06.001
- Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24(4):385–396. doi: 10.2307/2136404
- Nast I, Bolten M, Meinlschmidt G, Hellhammer DH. How to measure prenatal stress? A systematic review of psychometric instruments to assess psychosocial stress during pregnancy. Paediatr Perinat Epidemiol. 2013;27(4):313–322. doi: 10.1111/ppe.12051
- Marchetto NM, Glynn RA, Ferry ML, et al. Prenatal stress and newborn telomere length. Am J Obstet Gynecol. 2016;215(1): 94-e1–94-e8. doi: 10.1016/j.ajog.2016.01.177
- Send TS, Gilles M, Codd V, et al. Telomere length in newborns is related to maternal stress during pregnancy. Neuropsychopharmacology. 2017;42:2407–2413. doi: 10.1038/npp.2017.73
- Carroll JE, Mahrer NE, Shalowitz M, et al. Prenatal maternal stress prospectively relates to shorter child buccal cell telomere length. Psychoneuroendocrinology. 2020;121:104841. doi: 10.1016/j.psyneuen.2020.104841
- Xu J, Ye J, Wu Y, et al. Reduced fetal telomere length in gestational diabetes. PloS one. 2014;9(1):e86161. doi: 10.1371/journal.pone.0086161
- Kinalski M, Śledziewski A, Telejko B, et al. Lipid peroxidation, antioxidant defence and acid-base status in cord blood at birth: the influence of diabetes. Horm Metab Res. 2001;33(4):227–231. doi: 10.1055/s-2001-14953
- Sobki SH, Al-Senaidy AM, Al-Shammari TA, et al. Impact of gestational diabetes on lipid profiling and indices of oxidative stress in maternal and cord plasma. Saudi Med J. 2004;25(7):876–880.
- Benetos A, Kark JD, Susser E, et al. Tracking and fixed ranking of leukocyte telomere length across the adult life course. Aging Cell. 2013;12(4):615–621. doi: 10.1111/acel.12086
- Barnes RP, Fouquerel E, Opresko PL. The impact of oxidative DNA damage and stress on telomere homeostasis. Mech Ageing Dev. 2019;177:37–45. doi: 10.1016/j.mad.2018.03.013
- Ghimire S, Hill CV, Sy FS, Rodriguez R. Decline in telomere length by age and effect modification by gender, allostatic load and comorbidities in National Health and Nutrition Examination Survey (1999–2002). PloS One. 2019;14(8): e0221690. doi: 10.1371/journal.pone.0221690
- Simon NM, Smoller JW, McNamara KL, et al. Telomere shortening and mood disorders: preliminary support for a chronic stress model of accelerated aging. Biol Psychiatry. 2006;60(5):432–435. doi: 10.1016/j.biopsych.2006.02.004
- Shalev I, Moffitt TE, Sugden K, et al. Exposure to violence during childhood is associated with telomere erosion from 5 to 10 years of age: a longitudinal study. Mol Psychiatry. 2013;18(5):576–581. doi: 10.1038/mp.2012.32
- Puterman E, Lin J, Blackburn E, et al. The power of exercise: buffering the effect of chronic stress on telomere length. PloS One. 2010;5(5): e10837. doi: 10.1371/journal.pone.0010837
- McGrath M, Wong JYY, Michaud D, et al. Telomere length, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiol Prevent Biomark. 2007;16(4):815–819. doi: 10.1158/1055-9965.EPI-06-0961
- Pavanello S, Hoxha M, Dioni L, et al. Shortened telomeres in individuals with abuse in alcohol consumption. Int J Cancer. 2011;129(4):983–992. doi: 10.1002/ijc.25999
- Carulli L, Anzivino C, Baldelli E, et al. Telomere length elongation after weight loss intervention in obese adults. Mol Genet Metabol. 2016;118(2):138–142. doi: 10.1016/j.ymgme.2016.04.003
- Ikeda H, Aida J, Hatamochi A, et al. Quantitative fluorescence in situ hybridization measurement of telomere length in skin with/without sun exposure or actinic keratosis. Hum Pathol. 2014;45(3): 473–480. doi: 10.1016/j.humpath.2013.10.009
- Kesäniemi J, Lavrinienko A, Tukalenko E, et al. Exposure to environmental radionuclides associates with tissue-specific impacts on telomerase expression and telomere length. Sci Rep. 2019;9(1):850. doi: 10.1038/s41598-018-37164-8
- Ilyenko I, Lyaskivska O, Bazyka D. Analysis of relative telomere length and apoptosis in humans exposed to ionising radiation. Exp Oncol. 2011;33(4):235–238.
- Lustig A, Shterev I, Geyer S, et al. Long term effects of radiation exposure on telomere lengths of leukocytes and its associated biomarkers among atomic-bomb survivors. Oncotarget. 2016;7(26):38988–38998. doi: 10.18632/oncotarget.880
- McKenna MJ, Robinson E, Taylor L, et al. Chromosome translocations, inversions and telomere length for retrospective biodosimetry on exposed U.S. Atomic veterans. Radiat Res. 2019;191(4): 311–322. doi: 10.1667/RR15240.1
- Liu B, Sun Y, Xu G, et al. Association between body iron status and leukocyte telomere length, a biomarker of biological aging, in a nationally representative sample of US adults. J Acad Nutr Diet. 2019;119(4):617–625. doi: 10.1016/j.jand.2018.09.007
- Pottier G, Viau M, Ricoul M, et al. Lead exposure induces telomere instability in human cells. PloS one. 2013;8(6):e67501. doi: 10.1371/journal.pone.0067501
- Nomura SJ, Robien K, Zota AR. Serum folate, vitamin B-12, vitamin A, γ-tocopherol, α-tocopherol, and carotenoids do not modify associations between cadmium exposure and leukocyte telomere length in the general US adult population. J Nutr. 2017;147(4): 538–548. doi: 10.3945/jn.116.243162
- Wu Y, Liu Y, Ni N, et al. High lead exposure is associated with telomere length shortening in Chinese battery manufacturing plant workers. Occup Environ Med. 2012;69(8):557–563. doi: 10.1136/oemed-2011-100478
- Pawlas N, Płachetka A, Kozłowska A, et al. Telomere length, telomerase expression, and oxidative stress in lead smelters. Toxicol Ind Health. 2016;32(12):1961–1970. doi: 10.1177/0748233715601758
- de Souza MR, Kahl VFS, Rohr P, et al. Shorter telomere length and DNA hypermethylation in peripheral blood cells of coal workers. Mutat Res / Genet Toxicol Environ Mutagen. 2018;836(B):36–41. doi: 10.1016/j.mrgentox.2018.03.009
- Rohr P, da Silva J, da Silva FR, et al. Evaluation of genetic damage in open-cast coal mine workers using the buccal micronucleus cytome assay. Environ Mol Mutagen. 2013;54(1):65–71. doi: 10.1002/em.21744
- Nagpal R, Mainali R, Ahmadi S, et al. Gut microbiome and aging: Physiological and mechanistic insights. Nutr Healthy Aging. 2018;4(4):267–285. doi: 10.3233/NHA-170030
- DeJong EN, Surette MG, Bowdish DME. The gut microbiota and unhealthy aging: disentangling cause from consequence. Cell Host Microbe. 2020;28(2):180–189. doi: 10.1016/j.chom.2020.07.013
- Chen S-S, Liao X-M, Wei Q-Z, et al. Associations of the gut microbiota composition and fecal short-chain fatty acids with leukocyte telomere length in children aged 6–9 years old in Guangzhou, China: A cross-sectional study. J Nutr. 2022;152(6):1549–1559. doi: 10.1093/jn/nxac063
- Dowd JB, Bosch JA, Steptoe A, et al. Persistent herpesvirus infections and telomere attrition over 3 years in the Whitehall II cohort. J Infect Dis. 2017;216(5):565–572. doi: 10.1093/infdis/jix255
- Trevisan M, Matkovic U, Cusinato R, et al. Human cytomegalovirus productively infects adrenocortical cells and induces an early cortisol response. J Cell Physiol. 2009;221(3):629–641. doi: 10.1002/jcp.21896
- Choi J, Fauce SR, Effros RB. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain Behav Immun. 2008;22(4):600–605. doi: 10.1016/j.bbi.2007.12.004
- Shu Y, Wu M, Yang S, et al. Association of dietary selenium intake with telomere length in middle-aged and older adults. Clin Nutr. 2020;39(10):3086–3091. doi: 10.1016/j.clnu.2020.01.014
- Lin Z, Gao H, Wang B, et al. Dietary copper intake and its association with telomere length: a population based study. Front Endocrinol. 2018;9:404. doi: 10.3389/fendo.2018.00404
- Furumoto K, Inoue E, Nagao N, et al. Age-dependent telomere shortening is slowed down by enrichment of intracellular vitamin C via suppression of oxidative stress. Life Sci. 1998;63(11):935–948. doi: 10.1016/S0024-3205(98)00351-8
- Shin C, Baik I. Leukocyte telomere length is associated with serum vitamin B12 and homocysteine levels in older adults with the presence of systemic inflammation. Clin Nutrit Res. 2016;5(1):7–14. doi: 10.7762/cnr.2016.5.1.7
- Lee J-Y, Shin C, Baik I. Longitudinal associations between micronutrient consumption and leukocyte telomere length. J Hum Nutr Dietet. 2017;30(2):236–243. doi: 10.1111/jhn.12403
- Richards JB, Valdes AM, Gardner JP, et al. Higher serum vitamin D concentrations are associated with longer leukocyte telomere length in women. Am J Clin Nutr. 2007;86(5):1420–1425. doi: 10.1093/ajcn/86.5.1420
- Oyama J-I, Shiraki A, Nishikido T, et al. EGCG, a green tea catechin, attenuates the progression of heart failure induced by the heart/muscle-specific deletion of MnSOD in mice. J Cardiology. 2017;69(2):417–427. doi: 10.1016/j.jjcc.2016.05.019
- Coussons-Read ME, Lobel M, Carey JC, et al. The occurrence of preterm delivery is linked to pregnancy-specific distress and elevated inflammatory markers across gestation. Brain Behav Immun. 2012;26(4):650–659. DOI: 1016/j.bbi.2012.02.009
- Ross KM, Cole SW, Carroll JE, Schetter C.D. Elevated pro-inflammatory gene expression in the third trimester of pregnancy in mothers who experienced stressful life events. Brain Behav Immun. 2019;76:97–103. doi: 10.1016/j.bbi.2018.11.009
- Rakers F, Rupprecht S, Dreiling M, et al. Transfer of maternal psychosocial stress to the fetus. Neuroscie Biobehav Rev. 2020;117:185–197. doi: 10.1016/j.neubiorev.2017.02.019
- McCloskey K, Ponsonby A-L, Collier F, et al. The association between higher maternal pre-pregnancy body mass index and increased birth weight, adiposity and inflammation in the newborn. Pediatr Obes. 2018;13(1):46–53. doi: 10.1111/ijpo.12187
- Lieu PT, Heiskala M, Peterson PA, Yang Y. The roles of iron in health and disease. Mol Asp Med. 2001;22(1–2):1–87. doi: 10.1016/S0098-2997(00)00006-6
- Hartwig A. Mechanisms in cadmium-induced carcinogenicity: recent insights. Biometals. 2010;23(5):951–960. doi: 10.1007/s10534-010-9330-4
- Rochette PJ, Brash DE. Human telomeres are hypersensitive to UV-induced DNA Damage and refractory to repair. PLoS Genetics. 2010;6(4): e1000926. doi: 10.1371/journal.pgen.1000926
- Ma H-M, Liu W, Zhang P, et al. Human skin fibroblast telomeres are shortened after ultraviolet irradiation. J Int Med Res. 2012;40(5):1871–1877. doi: 10.1177/030006051204000526
- Huang Z, Rose AH, Hoffmann PR. The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxidants and Redox Signaling. 2012;16(7): 705–743. doi: 10.1089/ars.2011.4145
- Tainer JA, Getzoff ED, Richardson JS, Richardson D.C. Structure and mechanism of copper, zinc superoxide dismutase. Nature. 1983;306:284–287. doi: 10.1038/306284a0
- Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal. 2011;15:1583–606. doi: 10.1089/ars.2011.3999
- Werner C, Fürster T, Widmann T, et al. Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall. Circulation. 2009;120(24):2438–2447. doi: 10.1161/CIRCULATIONAHA.109.861005
- Hagman M, Werner C, Kamp K, et al. Reduced telomere shortening in lifelong trained male football players compared to age-matched inactive controls. Prog Cardiovasc Dis. 2020;63(6):738–749. doi: 10.1016/j.pcad.2020.05.009
- Denham J, Sellami M. Exercise training increases telomerase reverse transcriptase gene expression and telomerase activity: A systematic review and meta-analysis. Ageing Res Rev. 2021;70:101411. doi: 10.1016/j.arr.2021.101411
- Gidron Y, Russ K, Tissarchondou H, Warner J. The relation between psychological factors and DNA-damage: a critical review. Biol Psychology. 2006;72(3):291–304. doi: 10.1016/j.biopsycho.2005.11.011
- Li G, He H. Hormesis, allostatic buffering capacity and physiological mechanism of physical activity: a new theoretic framework. Med Hypotheses. 2009;72(5):527–532. doi: 10.1016/j.mehy.2008.12.037
- Wang Z, Rhee DB, Lu J, et al. Characterization of oxidative guanine damage and repair in mammalian telomeres. PLoS Genetics. 2010;6(5): e1000951. doi: 10.1371/journal.pgen.1000951
- Fouquerel E, Barnes RP, Uttam S, et al. Targeted and persistent 8-oxoguanine base damage at telomeres promotes telomere loss and crisis. Mol Cell. 2019;75(1):117–130. doi: 10.1016/j.molcel.2019.04.024
- Lazzerini-Denchi E, Sfeir A. Stop pulling my strings — what telomeres taught us about the DNA damage response. Nat Rev Mol Cell Biol. 2016;17(6):364–378. doi: 10.1038/nrm.2016.43
- Petersen S, Saretzki G, von Zglinicki T. Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res. 1998;239(1):152–160. doi: 10.1006/excr.1997.3893
- Richter T, Saretzki G, Nelson G, et al. TRF2 overexpression diminishes repair of telomeric single-strand breaks and accelerates telomere shortening in human fibroblasts. Mech Ageing Dev. 2007;128(4):340–345. doi: 10.1016/j.mad.2007.02.003
- Karlseder J, Hoke K, Mirzoeva OK, et al. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2004;2(8): e240. doi: 10.1371/journal.pbio.0020240
- Fotiadou P, Henegariu O, Sweasy JB, et al. DNA polymerase β interacts with TRF2 and induces telomere dysfunction in a murine mammary cell line. Cancer Res. 2004;64(11):3830–3837. doi: 10.1158/0008-5472.CAN-04-0136
- Tchirkov A, Lansdorp PM. Role of oxidative stress in telomere shortening in cultured fibroblasts from normal individuals and patients with ataxia–telangiectasia. Hum Mol Genet. 2003;12(3): 227–232. doi: 10.1093/hmg/ddg023
- Haendeler J, Hoffmann J, Brandes RP, et al. Hydrogen peroxide triggers nuclear export of telomerase reverse transcriptase via Src kinase family-dependent phosphorylation of tyrosine 707. Mol Cell Biol. 2003;23(13):4598–4610. doi: 10.1128/MCB.23.13.4598-4610.2003
- Haendeler J, Dröse S, Büchner N, et al. Mitochondrial telomerase reverse transcriptase binds to and protects mitochondrial DNA and function from damage. Arterioscler Thromb Vasc Biol. 2009;29(6):929–935. doi: 10.1161/ATVBAHA.109.185546
- Miwa S, Czapiewski R, Wan T, et al. Decreased mTOR signalling reduces mitochondrial ROS in brain via accumulation of the telomerase protein TERT within mitochondria. Aging (Albany NY). 2016;8(10):2551–2567. doi: 10.18632/aging.101089
- Maida Y, Yasukawa M, Furuuchi M, et al. An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature. 2009;461(7261):230–235. doi: 10.1038/nature08283
- Sharma NK, Reyes A, Green P, et al. Human telomerase acts as a hTR-independent reverse transcriptase in mitochondria. Nucleic Acids Res. 2012;40(2):712–725. doi: 10.1093/nar/gkr758
- Ahmed S, Passos JF, Birket MJ, et al. Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J Cell Sci. 2008;121(7):1046–1053. doi: 10.1242/jcs.019372
- Hofer T, Seo AY, Prudencio M, Leeuwenburgh C. A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol Chem. 2006;387(1):103–11. doi: 10.1515/BC.2006.014
- Huang H-Y, Wang S-R, Wu L-Y, et al. Biochemical insights into the role of guanosine oxidation on RNA G-quadruplex. CCS Chemistry. 2020;2(6):605–612. doi: 10.31635/ccschem.020.202000173
- Floyd RA, Hensley K, Jaffery F, et al. Increased oxidative stress brought on by pro-inflammatory cytokines in neurodegenerative processes and the protective role of nitrone-based free radical traps. Life Sci. 1999;65(18–19):1893–1899. doi: 10.1016/S0024-3205(99)00443-9
- Beyne-Rauzy O, Prade-Houdellier N, Demur C, et al. Tumor necrosis factor-α inhibits hTERT gene expression in human myeloid normal and leukemic cells. Blood. 2005;106(9):3200–3205. doi: 10.1182/blood-2005-04-1386
- Oikawa S, Kawanishi S. Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Letters. 1999;453(3):365–368. doi: 10.1016/S0014-5793(99)00748-6
- Kawanishi S, Oikawa S. Mechanism of telomere shortening by oxidative stress. Ann NY Acad Sci. 2004;1019(1):278–284. doi: 10.1196/annals.1297.047