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Understanding the Role of Telomere Dynamics in Normal and Dysfunctional Human Reproduction

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Abstract

In modern society, fertility problems and demand of treatment seem to be on the rise, which led to an increased interest in research regarding human reproduction. Among these efforts, the study of the molecular senescence process has gain notorious popularity as aging is one of the most important variables involved in reproductive capacity and since the comprehension of telomere dynamics has become an important and influential theme. This new knowledge regarding the reproductive aging process is expected to offer new tools to understand the acquisition, maintenance, and loss of fertility potential. Therefore, this review seeks to clarify the relevance of molecular aging (evaluated by telomere shortening) in human reproduction, showing that it is a dynamic and variable process modulated according to the specific tissue and stage of development. As well, it is discussed how telomere status influence the development and progression of some fertility pathologies, the outcome of assisted reproductive treatments, and programming of aging in the offspring.

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References

  1. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet. 2005;6(8):611–622. doi:10.1038/nrg1656

    CAS  PubMed  Google Scholar 

  2. Kong CM, Lee XW, Wang X. Telomere shortening in human diseases. FEBS J. 2013;280(14):3180–3193. doi:10.1111/febs. 12326

    CAS  PubMed  Google Scholar 

  3. Lai TP, Wright WE, Shay JW. Comparison of telomere length measurement methods. Philos Trans R Soc B Biol Sci. 2018; 373(1741):20160451. doi:10.1098/rstb.2016.0451

    Google Scholar 

  4. 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

    PubMed  PubMed Central  Google Scholar 

  5. Chan SRWL, Blackburn EH. Telomeres and telomerase. Philos Trans R Soc Lond B Biol Sci. 2004;359(1441):109–121. doi:10. 1098/rstb.2003.1370

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Sukenik-Halevy R, Fejgin M, Kidron D, et al. Telomere aggregate formation in placenta specimens of pregnancies complicated with pre-eclampsia. Cancer Genet Cytogenet. 2009;195(1):27–30. doi: 10.1016/j.cancergencyto.2009.03.015

    CAS  PubMed  Google Scholar 

  7. Bernadotte A, Mikhelson VM, Spivak IM. Markers of cellular senescence. Telomere shortening as a marker of cellular senescence. Aging (Albany NY). 2016;8(1):3–11. doi:10.18632/aging.100871

    CAS  Google Scholar 

  8. Victorelli S, Passos JF. Telomeres and cell senescence—size matters not. EBioMedicine. 2017;21:14–20. doi:10.1016/j.ebiom.

    PubMed  PubMed Central  Google Scholar 

  9. George K, Kamath MS. Fertility and age. J Hum Reprod Sci. 2010;3(3):121–123. doi:10.4103/0974-1208.74152

    PubMed  PubMed Central  Google Scholar 

  10. Harris ID, Fronczak C, Roth L, Meacham RB. Fertility and the aging male. Rev Urol. 2011;13(4):e184–e190. http://www.ncbi.nlm.nih.gov/pubmed/22232567.

    PubMed  PubMed Central  Google Scholar 

  11. Kocourkova J, Burcin B, Kucera T. Demographic relevancy of increased use of assisted reproduction in European countries. Reprod Health. 2014;11:37. doi:10.1186/1742-4755-11-37

    PubMed  PubMed Central  Google Scholar 

  12. Stephen EH, Chandra A, King RB. Supply of and demand for assisted reproductive technologies in the United States: clinic-and population-based data, 1995-2010. Fertil Steril. 2016; 105(2):451–458. doi:10.1016/j.fertnstert.2015.10.007

    PubMed  Google Scholar 

  13. Aydos SE, Elhan AH, Tükün A. Is telomere length one of the determinants of reproductive life span? Arch Gynecol Obstet. 2005;272(2):113–116. doi:10.1007/s00404-004-0690-2

    PubMed  Google Scholar 

  14. Monaghan P, Eisenberg DTA, Harrington L, Nussey D. Under-standing diversity in telomere dynamics. Philos Trans R Soc Lond B Biol Sci. 2018;373(1741):20160435. doi:10.1098/rstb.2016.0435

    PubMed  PubMed Central  Google Scholar 

  15. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW. 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

    CAS  PubMed  Google Scholar 

  16. Jørgensen PB, Fedder J, Koelvraa S, Graakjaer J. Age-dependence of relative telomere length profiles during spermato-genesis in man. Maturitas. 2013;75(4):380–385. doi:10.1016/j.maturitas.2013.05.001

    PubMed  Google Scholar 

  17. Reig-Viader R, Vila-Cejudo M, Vitelli V, et al. Telomeric repeat-containing RNA (TERRA) and telomerase are components of telomeres during mammalian gametogenesis J. Biol Reprod. 2014;90(5):780–791. doi:10.1095/biolreprod.113.116954

    Google Scholar 

  18. Schrader M, Müller M, Schulze W, et al. Quantification of the expression level of the gene encoding the catalytic subunit of telomerase in testicular tissue specimens predicts successful sperm recovery. Hum Reprod. 2002;17(1):150–156. http://www.ncbi.nlm.nih.gov/pubmed/11756380.

    CAS  PubMed  Google Scholar 

  19. Schrader M, Müller M, Heicappell R, Straub B, Miller K. Quantification of human telomerase RNA (hTR) and human telomerase reverse transcriptase (hTERT) mRNA in testicular tissue of infertile patients. Asian J Androl. 2001;3(4):263–270. http://www.ncbi.nlm.nih.gov/pubmed/11753470.

    CAS  PubMed  Google Scholar 

  20. Schrader M, Müller M, Heicappell R, Krause H, Schulze W, Miller K. Telomerase activity and expression of telomerase sub-units in the testicular tissue of infertile patients. Fertil Steril. 2000;73(4):706–711. http://www.ncbi.nlm.nih.gov/pubmed/10731529.

    CAS  PubMed  Google Scholar 

  21. Weikert S, Christoph F, Schulze W, et al. Testicular expression of survivin and human telomerase reverse transcriptase (hTERT) associated with spermatogenic function in infertile patients. Asian J Androl. 2006;8(1):95–100. doi:10.1111/j.1745-7262.2006. 00102.x

    CAS  PubMed  Google Scholar 

  22. Reig-Viader R, Brieno-Enriquez MA, Khouriauli L, et al. Telo-meric repeat-containing RNA and telomerase in human fetal oocytes. Hum Reprod. 2013;28(2):414–422. doi:10.1093/hum-rep/des363

    CAS  PubMed  Google Scholar 

  23. Wright DL, Jones EL, Mayer JF, Oehninger S, Gibbons WE, Lanzendorf SE. Characterization of telomerase activity in the human oocyte and preimplantation embryo. Mol Hum Reprod. 2001;7(10):947–955. http://www.ncbi.nlm.nih.gov/pubmed/11574663.

    CAS  PubMed  Google Scholar 

  24. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Treff NR, Su J, Taylor D, Scott RT Jr. Telomere DNA deficiency is associated with development of human embryonic aneuploidy. PLoS Genet. 2011;7(6):e1002161. doi:10.1371/journal.pgen.1002161

    Google Scholar 

  26. Menon R, Behnia F, Polettini J, Saade GR, Campisi J, Velarde M. Placental membrane aging and HMGB1 signaling associated with human parturition. Aging (Albany NY). 2016;8(2):216–230. doi: 10.18632/aging.100891

    CAS  Google Scholar 

  27. Gielen M, Hageman G, Pachen D, Derom C, Vlietinck R, Zeegers MP. Placental telomere length decreases with gestational age and is influenced by parity: a study of third trimester live-born twins. Placenta. 2014;35(10):791–796. doi:10.1016/j.placenta.2014.05. 010

    CAS  PubMed  Google Scholar 

  28. Menon R, Yu J, Basanta-Henry P, et al. Short fetal leukocyte telomere length and preterm prelabor rupture of the membranes. PLoS One. 2012;7(2):e31136. doi:10.1371/journal.pone.0031136

    Google Scholar 

  29. Polettini J, Behnia F, Taylor BD, Saade GR, Taylor RN, Menon R. Telomere fragment induced amnion cell senescence: a contributor to parturition? Sun K, ed. PLoS One. 2015;10(9):e0137188. doi:10.1371/journal.pone.0137188

    Google Scholar 

  30. Storer M, Mas A, Robert-Moreno A, et al. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell. 2013;155(5):1119–1130. doi:10.1016/j.cell.2013. 10.041

    CAS  PubMed  Google Scholar 

  31. Mun˜oz-Espín D, Can˜amero M, Maraver A, et al. Programmed cell senescence during mammalian embryonic development. Cell. 2013;155(5):1104–1118. doi:10.1016/j.cell.2013.10.019

    Google Scholar 

  32. Chuprin A, Gal H, Biron-Shental T, et al. Cell fusion induced by ERVWE1 or measles virus causes cellular senescence. Genes Dev. 2013;27(21):2356–2366. doi:10.1101/gad.227512.113

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Ferrari F, Facchinetti F, Saade G, Menon R. Placental telomere shortening in stillbirth: a sign of premature senescence? J Matern Neonatal Med. 2016;29(8):1283–1288. doi:10.3109/14767058. 2015.1046045

    CAS  Google Scholar 

  34. Biron-Shental T, Sukenik Halevy R, Goldberg-Bittman L, Kidron D, Fejgin MD, Amiel A. Telomeres are shorter in placental tro-phoblasts of pregnancies complicated with intrauterine growth restriction (IUGR). Early Hum Dev. 2010;86(7):451–456. doi: 10.1016/j.earlhumdev.2010.06.002

    CAS  PubMed  Google Scholar 

  35. Davy P, Nagata M, Bullard P, Fogelson NS, Allsopp R. Fetal growth restriction is associated with accelerated telomere shortening and increased expression of cell senescence markers in the placenta. Placenta. 2009;30(6):539–542. doi:10.1016/j.placenta.2009.03.005

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Biron-Shental T, Sukenik-Halevy R, Sharon Y, et al. Short telo-meres may play a role in placental dysfunction in preeclampsia and intrauterine growth restriction. Am J Obstet Gynecol. 2010; 202(4):381.e1–381.e7. doi:10.1016/j.ajog.2010.01.036

    Google Scholar 

  37. Toutain J, Prochazkova-Carlotti M, Cappellen D, et al. Reduced placental telomere length during pregnancies complicated by intrauterine growth restriction. Tian X (Cindy), ed. PLoS One. 2013;8(1):e54013. doi:10.1371/journal.pone.0054013

    Google Scholar 

  38. Biron-Shental T, Sukenik-Halevy R, Sharon Y, Laish I, Fejgin MD, Amiel A. Telomere shortening in intra uterine growth restriction placentas. Early Hum Dev. 2014;90(9):465–469. doi: 10.1016/j.earlhumdev.2014.06.003

    CAS  PubMed  Google Scholar 

  39. Sukenik-Halevy R, Amiel A, Kidron D, Liberman M, Ganor-Paz Y, Biron-Shental T. Telomere homeostasis in trophoblasts and in cord blood cells from pregnancies complicated with preeclampsia. Am J Obstet Gynecol. 2016;214(2):283.e1-283.e7. doi:10. 1016/j.ajog.2015.08.050

    PubMed  Google Scholar 

  40. Biron-Shental T, Liberman M, Elbaz M, Laish I, Sharony R, Amiel A. Telomere homeostasis in placentas from pregnancies with uncontrolled diabetes. Placenta. 2016;44:13–18. doi:10. 1016/j.placenta.2016.05.009

    CAS  PubMed  Google Scholar 

  41. Biron-Shental T, Sukenik-Halevy R, Naboani H, Liberman M, Kats R, Amiel A. Telomeres are shorter in placentas from pregnancies with uncontrolled diabetes. Placenta. 2015;36(2): 199–203. doi:10.1016/j.placenta.2014.11.011

    CAS  PubMed  Google Scholar 

  42. Zinkovaá A, Marovaá D, Koperdaákovaá J, Mirchi TP, Korabecnaá M, Jirkovskaá M. Relative amount of telomeric sequences in terminal villi does not differ between normal term placentas and placentas from patients with well-controlled type 1 diabetes mellitus. Placenta. 2017;55:1–4. doi:10.1016/j.placenta.2017.04.016

    Google Scholar 

  43. Thilagavathi J, Kumar M, Mishra SS, Venkatesh S, Kumar R, Dada R. Analysis of sperm telomere length in men with idiopathic infertility. Arch Gynecol Obstet. 2013;287(4):803–807. doi:10. 1007/s00404-012-2632-8

    CAS  PubMed  Google Scholar 

  44. Shuyuan L, Changjun Z, Haiying P, et al. Association study of telomere length with idiopathic male infertility. Yi Chuan. 2015; 37(11):1137–1142. doi:10.16288/j.yczz.15-267

    Google Scholar 

  45. Reig-Viader R, Capilla L, Vila-Cejudo M, et al. Telomere home-ostasis is compromised in spermatocytes from patients with idio-pathic infertility. Fertil Steril. 2014;102(3):728.e1–738.e1. doi: 10.1016/j.fertnstert.2014.06.005

    Google Scholar 

  46. Biron-Shental T, Wiser A, Hershko-Klement A, Markovitch O, Amiel A, Berkovitch A. Sub-fertile sperm cells exemplify telo-mere dysfunction. J Assist Reprod Genet. 2018;35(1):143–148. doi:10.1007/s10815-017-1029-9

    PubMed  Google Scholar 

  47. Antunes DMF, Kalmbach KH, Wang F, et al. A single-cell assay for telomere DNA content shows increasing telomere length het-erogeneity, 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

    PubMed  PubMed Central  Google Scholar 

  48. Ferlin A, Rampazzo E, Rocca MS, et al. In young men sperm telomere length is related to sperm number and parental age. Hum Reprod. 2013;28(12):3370–3376. doi:10.1093/humrep/det392

    CAS  PubMed  Google Scholar 

  49. Yang Q, Zhang N, Zhao F, et al. Processing of semen by density gradient centrifugation selects spermatozoa with longer telomeres for assisted reproduction techniques. Reprod Biomed Online. 2015;31(1):44–50. doi:10.1016/j.rbmo.2015.02.016

    PubMed  Google Scholar 

  50. Yang Q, Zhao F, Dai S, et al. Sperm telomere length is positively associated with the quality of early embryonic development. Hum Reprod. 2015;30(8):1876–1881. doi:10.1093/humrep/dev144

    CAS  PubMed  Google Scholar 

  51. Rocca MS, Speltra E, Menegazzo M, Garolla A, Foresta C, Ferlin A. Sperm telomere length as a parameter of sperm quality in normozoospermic men. Hum Reprod. 2016;31(6):1158–1163. doi:10.1093/humrep/dew061

    CAS  PubMed  Google Scholar 

  52. Thilagavathi J, Mishra SS, Kumar M, et al. Analysis of telomere length in couples experiencing idiopathic recurrent pregnancy loss. J Assist Reprod Genet. 2013;30(6):793–798. doi:10.1007/s10815-013-9993-1

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Mishra S, Kumar R, Malhotra N, Singh N, Dada R. Mild oxidative stress is beneficial for sperm telomere length maintenance. World J Methodol. 2016;6(2):163. doi:10.5662/wjm.v6.i2.163

    PubMed  PubMed Central  Google Scholar 

  54. Santiso R, Tamayo M, Gosaálvez J, Meseguer M, Garrido N, Fernaández JL. Swim-up procedure selects spermatozoa with longer telomere length. Mutat Res Mol Mech Mutagen. 2010; 688(1-2):88–90. doi:10.1016/j.mrfmmm.2010.03.003

    CAS  Google Scholar 

  55. Zhao F, Yang Q, Shi S, Luo X, Sun Y. Semen preparation methods and sperm telomere length: density gradient centrifugation versus the swim up procedure. Sci Rep. 2016;6:39051. doi:10. 1038/srep39051

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Arias-Sosa LA, Acosta ID, Lucena-Quevedo E, Moreno-Ortiz H, Esteban-Pérez C, Forero-Castro M. Genetic and epigenetic varia-tions associated with idiopathic recurrent pregnancy loss. J Assist Reprod Genet. 2018;35(3):355–366. doi:10.1007/s10815-017-1108-y

    PubMed  PubMed Central  Google Scholar 

  57. Hanna CW, Bretherick KL, Gair JL, Fluker MR, Stephenson MD, Robinson WP. Telomere length and reproductive aging. Hum Reprod. 2009;24(5):1206–1211. doi:10.1093/humrep/dep007

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Bhaumik P, Bhattacharya M, Ghosh P, Ghosh S, Kumar Dey S. Telomere length analysis in Down syndrome birth. Mech Ageing Dev. 2017;164:20–26. doi:10.1016/j.mad.2017.03.006

    CAS  PubMed  Google Scholar 

  59. Ghosh S, Feingold E, Chakraborty S, Dey SK. Telomere length is associated with types of chromosome 21 nondisjunction: a new insight into the maternal age effect on Down syndrome birth. Hum Genet. 2010;127(4):403–409. doi:10.1007/s00439-009-0785-8

    PubMed  Google Scholar 

  60. Albizua I, Rambo-Martin BL, Allen EG, He W, Amin AS, Sherman SL. Association between telomere length and chromosome 21 nondisjunction in the oocyte. Hum Genet. 2015;134(11-12): 1263–1270. doi:10.1007/s00439-015-1603-0

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Ray A, Hong CS, Feingold E, et al. Maternal telomere length and risk of down syndrome: epidemiological impact of smokeless chewing tobacco and oral contraceptive on segregation of chromosome 21. Public Health Genomics. 2015;19(1):11–18. doi:10.1159/000439245

    PubMed  Google Scholar 

  62. Butts S, Riethman H, Ratcliffe S, Shaunik A, Coutifaris C, Barnhart K. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab. 2009;94(12):4835–4843. doi:10.1210/jc.2008-2269

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Xu X, Chen X, Zhang X, et al. Impaired telomere length and telomerase activity in peripheral blood leukocytes and granulosa cells in patients with biochemical primary ovarian insufficiency. Hum Reprod. 2016;32(1):201–207. doi:10.1093/humrep/dew283

    PubMed  Google Scholar 

  64. Li Q, Du J, Feng R, et al. A possible new mechanism in the pathophysiology of polycystic ovary syndrome (PCOS): the discovery that leukocyte telomere length is strongly associated with PCOS. J Clin Endocrinol Metab. 2014;99(2):E234–E240. doi:10. 1210/jc.2013-3685

    CAS  PubMed  Google Scholar 

  65. Pedroso DCC, Miranda-Furtado CL, Kogure GS, et al. Inflammatory biomarkers and telomere length in women with polycystic ovary syndrome. Fertil Steril. 2015;103(2):542.e1–547.e2. doi:10. 1016/j.fertnstert.2014.10.035

    Google Scholar 

  66. Wei D, Xie J, Yin B, et al. Significantly lengthened telomere in granulosa cells from women with polycystic ovarian syndrome (PCOS). J Assist Reprod Genet. 2017;34(7):861–866. doi:10. 1007/s10815-017-0945-z

    PubMed  PubMed Central  Google Scholar 

  67. Li Y, Deng B, Ouyang N, Yuan P, Zheng L, Wang W. Telomere length is short in PCOS and oral contraceptive does not affect the telomerase activity in granulosa cells of patients with PCOS. J Assist Reprod Genet. 2017;34(7):849–859. doi:10.1007/ s10815-017-0929-z

    PubMed  PubMed Central  Google Scholar 

  68. Czamanski-Cohen J, Sarid O, Cwikel J, et al. Cell-free DNA and telomere length among women undergoing in vitro fertilization treatment. J Assist Reprod Genet. 2015;32(11):1697–1703. doi: 10.1007/s10815-015-0581-4

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Wang W, Chen H, Li R, et al. Telomerase activity is more significant for predicting the outcome of IVF treatment than telo-mere length in granulosa cells. Reproduction. 2014;147(5): 649–657. doi:10.1530/REP-13-0223

    CAS  PubMed  Google Scholar 

  70. Chen H, Wang W, Mo Y, et al. Women with high telomerase activity in luteinised granulosa cells have a higher pregnancy rate during in vitro fertilisation treatment. J Assist Reprod Genet. 2011;28(9):797–807. doi:10.1007/s10815-011-9600-2

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Cheng EH, Chen SU, Lee TH, 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

    CAS  PubMed  Google Scholar 

  72. Njajou OT, Cawthon RM, Damcott CM, et al. Telomere length is paternally inherited and is associated with parental lifespan. Proc Natl Acad Sci U S A. 2007;104(29):12135–12139. doi:10.1073/ pnas.0702703104

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Nordfjäll K, Svenson U, Norrback KF, Adolfsson R, Roos G. Large-scale parent-child comparison confirms a strong paternal influence on telomere length. Eur J Hum Genet. 2010;18(3): 385–389. doi:10.1038/ejhg.2009.178

    PubMed  Google Scholar 

  74. Nordfjäll K, Larefalk A, Lindgren P, Holmberg D, Roos G. Telomere length and heredity: indications of paternal inheritance. Proc Natl Acad Sci U S A. 2005;102(45):16374–16378. doi:10. 1073/pnas.0501724102

    PubMed  PubMed Central  Google Scholar 

  75. Kimura M, Cherkas LF, Kato BS, et al. Offspring’s leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet. 2008;4(2):e37. doi:10.1371/journal.pgen.0040037

    Google Scholar 

  76. Eisenberg DTA, Hayes MG, Kuzawa CW. Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants. Proc Natl Acad Sci U S A. 2012;109(26):10251–10256. doi:10.1073/pnas.1202092109

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 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

    CAS  PubMed  Google Scholar 

  79. Eisenberg DTA, Kuzawa CW. The paternal age at conception effect on offspring telomere length: mechanistic, comparative and adaptive perspectives. Philos Trans R Soc Lond B Biol Sci. 2018; 373(1741):20160442. doi:10.1098/rstb.2016.0442

    PubMed  PubMed Central  Google Scholar 

  80. Entringer S, de Punder K, Buss C, Wadhwa PD. The fetal programming of telomere biology hypothesis: an update. Philos Trans R Soc Lond B Biol Sci. 2018;373(1741):20170151. doi: 10.1098/rstb.2017.0151

    PubMed  PubMed Central  Google Scholar 

  81. Entringer S, Epel ES, Lin J, et al. Maternal psychosocial stress during pregnancy is associated with newborn leukocyte telomere length. Am J Obstet Gynecol. 2013;208(2):134.e1-134.e7. doi:10. 1016/j.ajog.2012.11.033

    PubMed  Google Scholar 

  82. Entringer S, Epel ES, Kumsta R, et al. Stress exposure in intrau-terine life is associated with shorter telomere length in young adulthood. Proc Natl Acad Sci U S A. 2011;108(33):E513–E518. doi:10.1073/pnas.1107759108

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Salihu HM, King LM, Nwoga C, et al. Association between maternal-perceived psychological stress and fetal telomere length. South Med J. 2016;109(12):767–772. doi:10.14423/SMJ. 0000000000000567

    PubMed  Google Scholar 

  84. 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

    PubMed  Google Scholar 

  85. Salihu HM, Pradhan A, King L, et al. Impact of intrauterine tobacco exposure on fetal telomere length. Am J Obstet Gynecol. 2015;212(2):205.e1-205.e8. doi:10.1016/j.ajog.2014.08.026

    PubMed  Google Scholar 

  86. Theall KP, McKasson S, Mabile E, Dunaway LF, Drury SS. Early hits and long-term consequences: tracking the lasting impact of prenatal smoke exposure on telomere length in children. Am J Public Health. 2013;103(S1):S133-S135. doi:10.2105/AJPH.2012.301208

    Google Scholar 

  87. Mirzakhani H, de Vivo I, Leeder JS, et al. Early pregnancy intrauterine fetal exposure to maternal smoking and impact on fetal telomere length. Eur J Obstet Gynecol Reprod Biol. 2017; 218:27–32. doi:10.1016/j.ejogrb.2017.09.013

    CAS  PubMed  Google Scholar 

  88. Martens DS, Plusquin M, Gyselaers W, de Vivo I, Nawrot TS. Maternal pre-pregnancy body mass index and newborn telomere length. BMC Med. 2016;14(1):148. doi:10.1186/s12916-016-0689-0

    PubMed  PubMed Central  Google Scholar 

  89. Entringer S, Epel ES, Lin J, et al. Maternal folate concentration in early pregnancy and newborn telomere length. Ann Nutr Metab. 2015;66(4):202–208. doi:10.1159/000381925

    CAS  PubMed  Google Scholar 

  90. Bijnens E, Zeegers MP, Gielen M, et al. Lower placental telomere length may be attributed to maternal residential traffic exposure; a twin study. Environ Int. 2015;79:1–7. doi:10.1016/j.envint.2015. 02.008

    PubMed  Google Scholar 

  91. Martens DS, Cox B, Janssen BG, et al. Prenatal air pollution and newborns’ predisposition to accelerated biological aging. JAMA Pediatr. 2017;171(12):1160. doi:10.1001/jamapediatrics.2017. 3024

    PubMed  PubMed Central  Google Scholar 

  92. Lin S, Huo X, Zhang Q, et al. Short placental telomere was associated with cadmium pollution in an electronic waste recycling town in china. Lustig AJ, ed. PLoS One. 2013;8(4):e60815. doi:10. 1371/journal.pone.0060815

    Google Scholar 

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  1. School of Biological Science, Universidad Pedagógica y Tecnológica de Colombia, Avenida Central del Norte 39-115, 150003, Tunja, Boyacaá, Colombia

    Luis Alejandro Arias-Sosa

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Arias-Sosa, L.A. Understanding the Role of Telomere Dynamics in Normal and Dysfunctional Human Reproduction. Reprod. Sci. 26, 6–17 (2019). https://doi.org/10.1177/1933719118804409

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