Impaired telomere length and telomerase activity in peripheral blood leukocytes and granulosa cells in patients with biochemical primary ovarian insufficiency
Abstract
Study question Are telomere length and telomerase activity associated with biochemical primary ovarian insufficiency (POI)? Summary answer Shortened telomere length and diminished telomerase activity were associated with biochemical POI. What is known already POI is a result of pathological reproductive aging and encompasses occult, biochemical and overt stages. Studies have indicated telomere length as a biomarker for biological aging. Study design, size, duration A total of 120 patients with biochemical POI and 279 control women were recruited by the Center for Reproductive Medicine of Shandong University. Participants/materials, setting, methods Telomere length in peripheral blood leukocytes (LTL) and granulosa cells (GTL) was measured using a modified Quantitative Polymerase Chain Reaction technique. The relative telomerase activity (RTA) in granulosa cells was detected using a modified quantitative-telomeric repeat amplification protocol assay. Main results and the role of chance After adjusting for age, patients with biochemical POI (n = 120) exhibited significantly shorter LTLs (0.75 ± 0.09 vs 1.79 ± 0.12, P Large scale data N/A. Limitations, reasons for caution The cross-sectional nature of this study might have its limit in telomere length as well as telomerase activity along with the progressing decline in ovarian function. Wider implications of the findings These findings suggest that telomere length and telomerase activity may be considered as indicators for progr…
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Patients with premature ovarian insufficiency have shorter telomeres and reduced telomerase activity in leukocytes and granulosa cells than healthy individuals.
“patients with premature ovarian insufficiency have shorter telomeres and reduced telomerase activity in leukocytes and granulosa cells than healthy individuals179”
From Telomere dysfunction in ageing and age-related diseases (2022) · cites this paper as [179]
Telomere shortening is associated with reduced fertility in several ways.
“Telomere shortening has been associated with reduced fertility in several ways177–180.”
From Telomere dysfunction in ageing and age-related diseases (2022) · cites this paper as [179]
Cites
Telomere measurement by quantitative PCR
Cawthon, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.10.e47 · Cited by 3,492 · see citing works
Accelerated telomere shortening in response to life stress
Epel, E. S., Blackburn, E. H., Lin, J., Dhabhar, F. S., Adler, N. E., Morrow, J. D., & Cawthon, R. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407162101 · Cited by 3,002 · see citing works
Aubert, G., & Lansdorp, P. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00026.2007 · Cited by 1,188 · see citing works
Nelson, L. M. (2009) · New England Journal of Medicine · doi:10.1056/nejmcp0808697 · Cited by 1,170 · see citing works
Brouilette, S., Moore, J. S., McMahon, A. D., Thompson, J. R., Ford, I., Shepherd, J., Packard, C. J., & Samani, N. J. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60071-3 · Cited by 744 · see citing works
Goswami, D., & Conway, G. S. (2005) · Human Reproduction Update · doi:10.1093/humupd/dmi012 · Cited by 713 · see citing works
White Cell Telomere Length and Risk of Premature Myocardial Infarction
Brouilette, S., Singh, R. K., Thompson, J. R., Goodall, A. H., & Samani, N. J. (2003) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000067426.96344.32 · Cited by 590 · see citing works
Primary ovarian insufficiency: a more accurate term for premature ovarian failure
Welt, C. K. (2007) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2007.03073.x · Cited by 538 · see citing works
Telomere length and risk of incident cancer and cancer mortality
Willeit, P., Willeit, J., Mayr, A., Weger, S., Oberhollenzer, F., Brandstätter, A., Kronenberg, F., & Kiechl, S. (2010) · JAMA · doi:10.1001/jama.2010.897 · Cited by 484 · see citing works
Nonradioactive detection of telomerase activity using the telomeric repeat amplification protocol
Herbert, B., Hochreiter, A. E., Wright, W. E., & Shay, J. W. (2006) · Nature Protocols · doi:10.1038/nprot.2006.239 · Cited by 267 · see citing works
Reproductive outcome in patients with diminished ovarian reserve
Levi, A. J., Raynault, M. F., Bergh, P. A., Drews, M. R., Miller, B. T., & Scott, R. T. W. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02017-9 · Cited by 261 · see citing works
Liu, L., Blasco, M. A., Trimarchi, J. R., & Keefe, D. L. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0735 · Cited by 157 · see citing works
Role of Telomeres and Telomerase in the Pathogenesis of Human Cancer
Hahn, W. C. (2003) · Journal of Clinical Oncology · doi:10.1200/jco.2003.06.018 · Cited by 141 · see citing works
Correlation of Telomere Length and Telomerase Activity with Occult Ovarian Insufficiency
Butts, S. F., Riethman, H. C., Ratcliffe, S. J., Shaunik, A., Coutifaris, C., & Barnhart, K. T. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-2269 · Cited by 126 · see citing works
Telomere length and reproductive aging
Hanna, C. W., Bretherick, K. L., Gair, J., Fluker, M. R., Stephenson, M. D., & Robinson, W. P. (2009) · Human Reproduction · doi:10.1093/humrep/dep007 · Cited by 121 · see citing works
Effect of Long-Term Hormone Therapy on Telomere Length in Postmenopausal Women
Lee, D., Im, J., Kim, J., Lee, H.-R., & Shim, J. (2005) · Yonsei Medical Journal · doi:10.3349/ymj.2005.46.4.471 · Cited by 114 · see citing works
Telomere Length Shortening and Alzheimer Disease—A Mendelian Randomization Study
Zhan, Y., Song, C., Karlsson, R., Tillander, A., Reynolds, C. A., Pedersen, N. L., & Hägg, S. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2015.1513 · Cited by 111 · see citing works
Bayne, S., Li, H., Jones, M. E. E., Pinto, A. R., Sinderen, M. L. V., Drummond, A. E., Simpson, E. R., & Liu, J. (2011) · Protein & Cell · doi:10.1007/s13238-011-1033-2 · Cited by 86 · see citing works
Fossel, M. (1998) · JAMA · doi:10.1001/jama.279.21.1732 · Cited by 85 · see citing works
Association of Leukocyte Telomere Length with Type 2 Diabetes in Mainland Chinese Populations
Shen, Q., Zhao, X., Yu, L., Zhang, Z., Zhou, D., Kan, M., Zhang, D., Cao, L., Xing, Q., Yang, Y., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1562 · Cited by 75 · see citing works
Self-citationFertilization failure in IVF: why and what next?
Barlow, P., Englert, Y., Puissant, F., Lejeune, B., Delvigne, A., Rysselberge, M. V., & Leroy, F. O. G. (1990) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137122 · Cited by 71 · see citing works
Liu, J., & Li, H. (2010) · Reproduction · doi:10.1530/rep-10-0008 · Cited by 69 · see citing works
Role of arterial telomere dysfunction in hypertension
Morgan, R. G., Ives, S. J., Walker, A. E., Cawthon, R., Andtbacka, R. H. I., Noyes, D. R., Lesniewski, L. A., Richardson, R. S., & Donato, A. J. (2014) · Journal of Hypertension · doi:10.1097/hjh.0000000000000157 · Cited by 67 · see citing works
Li, Q., Du, J., Feng, R., Xu, Y., Wang, H., Sang, Q., Xing, Q., Zhao, X., Li, J., He, L., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-3685 · Cited by 66 · see citing works
Telomerase Activity in Normal Ovaries and Premature Ovarian Failure
Kinugawa, C., Murakami, T., Okamura, K., & Yajima, A. (2000) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.190.231 · Cited by 66 · see citing works
Is telomere length one of the determinants of reproductive life span?
Aydos, S., Elhan, A. H., & Tükün, A. (2005) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-004-0690-2 · Cited by 64 · see citing works
The Extent and Significance of Telomere Loss with Age
Baird, D. M., & Kipling, D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1297.044 · Cited by 56 · see citing works
Genetics of Early and Normal Menopause
Laven, J. S. E. (2015) · Seminars in Reproductive Medicine · doi:10.1055/s-0035-1567825 · Cited by 52 · see citing works
Jeon, B.-G., Kang, E., Kumar, B. M., Maeng, G., Ock, S., Kwack, D.-O., Park, B.-W., & Rho, G. (2011) · Cell Transplantation · doi:10.3727/096368911x565001 · Cited by 49 · see citing works
Leukocyte Telomere Length in Alzheimer’s Disease Patients with a Different Rate of Progression
Tedone, E., Arosio, B., Colombo, F., Ferri, E., Asselineau, D., Piette, F., Gussago, C., Belmin, J., Pariel, S., Benlhassan, K., et al. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-142808 · Cited by 36 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Telomere dysfunction in ageing and age-related diseases
Rossiello, F., Jurk, D., Passos, J. F., & d’Adda di Fagagna, F. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00842-x · Cited by 754 · see citing works
Bao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 389 · see citing works
Self-citationThe role of oxidative stress in ovarian aging: a review
Yan, F., Zhao, Q., Li, Y., Zheng, Z., Kong, X., Shu, C., Liu, Y., & Shi, Y. (2022) · Journal of Ovarian Research · doi:10.1186/s13048-022-01032-x · Cited by 307 · see citing works
Self-citationThe Role of Oxidative Stress and Natural Antioxidants in Ovarian Aging
Yang, L., Chen, Y., Liu, Y., Xing, Y., Miao, C., Zhao, Y., Chang, X., & Zhang, Q. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.617843 · Cited by 231 · see citing works
Self-citationShi, Y., Zhu, X.-T., Su-na, Z., Ma, Y., Han, Y., Yue, J., & Zhang, Y. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1172481 · Cited by 179 · see citing works
Can ovarian aging be delayed by pharmacological strategies?
Zhang, J., Chen, Q., Du, D., Wu, T., Wen, J., Wu, M., Zhang, Y., Yan, W., Zhou, S., Li, Y., et al. (2019) · Aging · doi:10.18632/aging.101784 · Cited by 103 · see citing works
Mechanisms of mitochondrial dysfunction in ovarian aging and potential interventions
Ju, W., Zhao, Y., Yu, Y., Zhao, S., Xiang, S., & Lian, F. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1361289 · Cited by 96 · see citing works
Jiao, J., Shi, B., Wang, T., Fang, Y., Cao, T., Zhou, Y., Wang, X., & Li, D. (2018) · Human Reproduction · doi:10.1093/humrep/dey255 · Cited by 91 · see citing works
Telomere length: lights and shadows on their role in human reproduction
Rocca, M. S., Foresta, C., & Ferlin, A. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy208 · Cited by 89 · see citing works
Ovarian aging: mechanisms and intervention strategies
Zhu, Z., Xu, W., & Liu, L. (2022) · Medical Review · doi:10.1515/mr-2022-0031 · Cited by 87 · see citing works
The association of female and male infertility with telomere length (Review)
Vasilopoulos, E., Fragkiadaki, P., Kalliora, C., Fragou, D., Docea, A. O., Vakonaki, E., Tsoukalas, D., Călina, D. C., Bugă, A. M., Georgiadis, G., et al. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4225 · Cited by 84 · see citing works
Wu, C., Chen, D., Stout, M. B., Wu, M., & Wang, S. (2025) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2025.01.005 · Cited by 74 · see citing works
The Molecular Regulation in the Pathophysiology in Ovarian Aging
Li, C., Lin, L., Tsai, H., Chern, C.-U., Wen, Z., Wang, P., & Tsui, K. (2021) · Aging and Disease · doi:10.14336/ad.2020.1113 · Cited by 68 · see citing works
Self-citationDang, Y., Wang, X., Hao, Y., Zhang, X., Zhao, S., Ma, J., Qin, Y., & Chen, Z. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0163-8 · Cited by 66 · see citing works
Self-citationA kaleidoscopic view of ovarian genes associated with premature ovarian insufficiency and senescence
Yang, Q., Mümüşoğlu, S., Qin, Y., Sun, Y., & Hsueh, A. J. W. (2021) · The FASEB Journal · doi:10.1096/fj.202100756r · Cited by 63 · see citing works
Self-citationLi, Y., Li, R., Ouyang, N., Dai, K., Yuan, P., Zheng, L., & Wang, W. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.07.007 · Cited by 58 · see citing works
Aging-Related Ovarian Failure and Infertility: Melatonin to the Rescue
Reiter, R., Sharma, R., Romero, A., Manucha, W., Tan, D., Zuccari, D. A. P. D. C., & Chuffa, L. G. D. A. (2023) · Antioxidants · doi:10.3390/antiox12030695 · Cited by 64 · see citing works
Impact of NAD+ metabolism on ovarian aging
Liang, J., Huang, F., Song, Z., Tang, R., Zhang, P., & Chen, R. (2023) · Immunity & Ageing · doi:10.1186/s12979-023-00398-w · Cited by 56 · see citing works
Morin, S. J., Tao, X., Marín, D., Zhan, Y., Landis, J. N., Bedard, J., Scott, R. T. W., & Seli, E. U. (2018) · Aging · doi:10.18632/aging.101670 · Cited by 54 · see citing works
Ali, I., Padhiar, A. A., Wang, T., He, L., Chen, M., Wu, S., Zhou, Y., & Zhou, G. (2022) · Cells · doi:10.3390/cells11233713 · Cited by 52 · see citing works
Identification of a unique epigenetic profile in women with diminished ovarian reserve
Olsen, K. W., Fernandez, J. C., Chan, A. C., Freiesleben, N. L. C., Zedeler, A., Bungum, M., Cardona, A., Perry, J. R. B., Skouby, S. O., Hoffmann, E. R., et al. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.09.009 · Cited by 52 · see citing works
Dysregulated cytokine profile associated with biochemical premature ovarian insufficiency
Liu, P., Zhang, X., Hu, J., Cui, L., Zhao, S., Jiao, X., & Qin, Y. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13292 · Cited by 48 · see citing works
Self-citationWu, Y., Zhou, S., Zhao, A., Mi, Y., & Zhang, C. (2022) · Cell Biology International · doi:10.1002/cbin.11960 · Cited by 43 · see citing works
Decreased expression of m6A demethylase FTO in ovarian aging
Sun, X., Zhang, Y., Hu, Y., An, J., Li, L., Wang, Y., & Zhang, X. (2020) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05895-7 · Cited by 43 · see citing works
Self-citationZhang, X., Dang, Y., Liu, R., Zhao, S., Ma, J., & Qin, Y. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29725 · Cited by 42 · see citing works
Self-citationLncRNA ZNF674-AS1 regulates granulosa cell glycolysis and proliferation by interacting with ALDOA
Li, D., Wang, X., Li, G., Dang, Y., Zhao, S., & Qin, Y. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00493-1 · Cited by 43 · see citing works
Self-citationOvarian rescue in women with premature ovarian insufficiency: facts and fiction
Pellicer, N., Cozzolino, M., Díaz‐García, C., Galliano, D., Cobo, A. C., Pellicer, A., & Herraiz, S. (2022) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2022.12.011 · Cited by 39 · see citing works
OXIDATIVE STRESS AND REPRODUCTIVE FUNCTION: Sperm telomeres, oxidative stress, and infertility
Moazamian, A., Gharagozloo, P., Aitken, R. J., & Drevet, J. R. (2022) · Reproduction · doi:10.1530/rep-22-0189 · Cited by 38 · see citing works
Multiomics insights into the female reproductive aging
Wei, S., Tang, W., Chen, D., Xiong, J., Xue, L., Dai, Y., Guo, Y., Wu, C., Dai, J., Wu, M., et al. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102245 · Cited by 37 · see citing works
Furtado, C. L. M., Luchiari, H. R., Pedroso, D. C. C., Kogure, G. S., Caetano, L. C., Santana, B. A., Santana, V. P., Benetti‐Pinto, C. L., dos Reis, F. M., Maciel, M. A., et al. (2018) · Fertility and Sterility · doi:10.1016/j.fertnstert.2018.04.017 · Cited by 39 · see citing works
Ovarian Telomerase and Female Fertility
Toupance, S., Fattet, A.-J., Thornton, S. N., Bénétos, A., Guéant, J., & Koscinski, I. (2021) · Biomedicines · doi:10.3390/biomedicines9070842 · Cited by 35 · see citing works
The Role of Noncoding RNA in the Pathophysiology and Treatment of Premature Ovarian Insufficiency
Pankiewicz, K., Laudański, P., & Issat, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179336 · Cited by 35 · see citing works
Aging and oocyte competence: A molecular cell perspective
Ferreira, A. F., Soares, M., Almeida‐Santos, T., Ramalho‐Santos, J., & Sousa, A. P. (2023) · WIREs Mechanisms of Disease · doi:10.1002/wsbm.1613 · Cited by 34 · see citing works
Fattet, A.-J., Toupance, S., Thornton, S. N., Monnin, N., Guéant, J., Bénétos, A., & Koscinski, I. (2020) · Journal of Ovarian Research · doi:10.1186/s13048-020-00702-y · Cited by 35 · see citing works
Relationship between the characteristic traits of polycystic ovary syndrome and susceptibility genes
Hong, S.-H., Hong, Y. S., Jeong, K., Chung, H., Lee, H., & Sung, Y.-A. (2020) · Scientific Reports · doi:10.1038/s41598-020-66633-2 · Cited by 32 · see citing works
Li, D., Wang, X., Dang, Y., Zhang, X., Zhao, S., Lü, G., Chan, W., Leung, P. C. K., & Qin, Y. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2020.10.041 · Cited by 33 · see citing works
Self-citationExploration of the mechanism and therapy of ovarian aging by targeting cellular senescence
Tang, W., Wang, K., Feng, Y., Tsui, K., Singh, K. K., Stout, M. B., Wang, S., & Wu, M. (2025) · Life Medicine · doi:10.1093/lifemedi/lnaf004 · Cited by 32 · see citing works
Sperm telomere length in donor samples is not related to ICSI outcome
Torra‐Massana, M., Barragán, M., Bellu, E., Oliva, R., Rodríguez, A., & Vassena, R. (2018) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-017-1104-2 · Cited by 31 · see citing works
Hanson, B. M., Tao, X., Zhan, Y., Kim, J. G., Klimczak, A. M., Herlihy, N. S., Scott, R. T., & Seli, E. U. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.09.164 · Cited by 31 · see citing works
Protsenko, E., Rehkopf, D. H., Prather, A. A., Epel, E. S., & Lin, J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0240185 · Cited by 29 · see citing works
Stem Cell Paracrine Signaling for Treatment of Premature Ovarian Insufficiency
Polonio, A. M., García-Velasco, J. A., & Herraiz, S. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.626322 · Cited by 31 · see citing works
Sun, D., Wang, Y., Sun, N., Jiang, Z., Li, Z., Wang, L., Yang, F., & Li, W. (2023) · Journal of Ovarian Research · doi:10.1186/s13048-023-01115-3 · Cited by 28 · see citing works
Impact of Ovarian Aging in Reproduction: From Telomeres and Mice Models to Ovarian Rejuvenation.
Polonio, A. M., Chico-Sordo, L., Córdova-Oriz, I., Medrano, M., García-Velasco, J. A., & Varela, E. (2020) · PubMed Central · Cited by 28 · see citing works
Reproductive aging and telomeres: Are women and men equally affected?
Chico-Sordo, L., Córdova-Oriz, I., Polonio, A. M., S-Mellado, L. S., Medrano, M., García-Velasco, J. A., & Varela, E. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111541 · Cited by 27 · see citing works
Lnc-GULP1–2:1 affects granulosa cell proliferation by regulating COL3A1 expression and localization
Yao, G., Kong, Y., Yang, G., Kong, D., Xu, Y., He, J. H., Xu, Z., Bai, Y., Fan, H., He, Q., et al. (2021) · Journal of Ovarian Research · doi:10.1186/s13048-021-00769-1 · Cited by 27 · see citing works
Vitamin D in human reproduction
Franasiak, J. M., Lara-Molina, E. E., & Pellicer, A. (2017) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000375 · Cited by 25 · see citing works
Zhou, X., Li, Y., Zhang, J., Liu, Y., Zhe, J., Zhang, Q., Chen, Y.-X., Chen, X., & Chen, S. (2020) · Epigenomics · doi:10.2217/epi-2019-0147 · Cited by 24 · see citing works
Self-citationCumulus cells have longer telomeres than leukocytes in reproductive-age women
Lara-Molina, E. E., Franasiak, J. M., Marín, D., Tao, X., Díaz-Gimeno, P., Florensa, M., Martin, M., Seli, E. U., & Pellicer, A. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.08.089 · Cited by 24 · see citing works
The Final Phases of Ovarian Aging: A Tale of Diverging Functional Trajectories
Bochynska, S., García‐Pérez, M. Á., Tarín, J. J., Szeliga, A., Męczekalski, B., & Cano, A. (2025) · Journal of Clinical Medicine · doi:10.3390/jcm14165834 · Cited by 26 · see citing works
M’kacher, R., Colicchio, B., Marquet, V., Borie, C., Najar, W., Hempel, W. M., Heidingsfelder, L., Oudrhiri, N., Jawhari, M. A., Wilhelm-Murer, N., et al. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.07.005 · Cited by 23 · see citing works
Telomere shortening in blood leukocytes of patients with posttraumatic stress disorder
Avetyan, D., Zakharyan, R., Petřek, M., & Arakelyan, A. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.01.018 · Cited by 23 · see citing works
Insights into the Role of Telomeres in Human Embryological Parameters. Opinions Regarding IVF
Anifandis, G., Σαμαρά, Μ., Simopoulou, M., Messini, C. I., Chatzimeletiou, K., Thodou, E., Daponte, A. I., & Georgiou, I. A. (2021) · Journal of Developmental Biology · doi:10.3390/jdb9040049 · Cited by 22 · see citing works
Telomere Shortening and Fusions: A Link to Aneuploidy in Early Human Embryo Development
Kohlrausch, F. B., Wang, F., Chamani, I. J., & Keefe, D. L. (2021) · Obstetrical & Gynecological Survey · doi:10.1097/ogx.0000000000000907 · Cited by 21 · see citing works
Telomeres, aging and reproduction
Córdova-Oriz, I., Chico-Sordo, L., & Varela, E. (2022) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000779 · Cited by 21 · see citing works
The Interplay between Telomeres, Mitochondria, and Chronic Stress Exposure in the Aging Egg
Derevyanko, A., Skowrońska, A., Skowroński, M. T., & Kordowitzki, P. (2022) · Cells · doi:10.3390/cells11162612 · Cited by 22 · see citing works
Valtetsiotis, K., Valsamakis, G., Charmandari, E., & Vlahos, N. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129828 · Cited by 19 · see citing works
Telomere Length, a New Biomarker of Male (in)Fertility? A Systematic Review of the Literature
Fattet, A.-J., Chaillot, M., & Koscinski, I. (2023) · Genes · doi:10.3390/genes14020425 · Cited by 19 · see citing works
Xu, X., Shen, H., Yu, M., Du, M., & Li, X. (2022) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2022.01.016 · Cited by 18 · see citing works
Self-citationPiani, L. L., Reschini, M., Somigliana, E., Ferrari, S., Busnelli, A., Viganò, P., Favero, C., Albetti, B., Hoxha, M., & Bollati, V. (2022) · PLoS ONE · doi:10.1371/journal.pone.0261591 · Cited by 17 · see citing works
Yu, T.-N., Cheng, E., Tsai, H.-N., Lin, P., Chen, C.-H., Huang, C., Lee, T., & Lee, M. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11071824 · Cited by 17 · see citing works
Tire, B., & Öztürk, S. (2023) · Journal of Ovarian Research · doi:10.1186/s13048-023-01211-4 · Cited by 18 · see citing works
Stem cell-based therapeutic potential in female ovarian aging and infertility
Cui, X., & Jing, X. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-024-01492-3 · Cited by 19 · see citing works
Zhang, Y., Wu, Q., Bai, F., Hu, Y., Xu, B., Tang, Y., & Wu, J. (2025) · Journal of Ovarian Research · doi:10.1186/s13048-025-01651-0 · Cited by 16 · see citing works
Garg, A., & Seli, E. U. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2023.11.011 · Cited by 13 · see citing works
Christensen, M. W., Keefe, D. L., Wang, F., Hansen, C. S., Chamani, I. J., Sommer, C., Nyegaard, M., Rohde, P. D., Nielsen, A. L., Bybjerg‐Grauholm, J., et al. (2021) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-021-02326-7 · Cited by 12 · see citing works
Kong, Y., Yang, G., Feng, X., Ji, Z., Wang, X., Shao, Y., Meng, J., Yao, G., Ren, C., & Yang, G. S. (2024) · Communications Biology · doi:10.1038/s42003-024-06857-4 · Cited by 11 · see citing works
Telomeres and oocyte maturation rate are not reduced by COVID-19 except in severe cases
Chico-Sordo, L., Polonio, A. M., Córdova-Oriz, I., Medrano, M., Herraiz, S., Bronet, F., García-Velasco, J. A., & Varela, E. (2022) · Reproduction · doi:10.1530/rep-22-0243 · Cited by 11 · see citing works
Intraovarian condensed platelet cytokines for infertility and menopause—Mirage or miracle?
Sills, E. S., Wood, S. H., & Walsh, A. P. H. (2022) · Biochimie · doi:10.1016/j.biochi.2022.08.020 · Cited by 11 · see citing works
Lyu, W., Li, D., Li, S., Hu, H., Zhou, J., & Wang, L. (2024) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2024.2361306 · Cited by 10 · see citing works
Mechanistic study on the role of multi-pathway autophagy in ovarian aging: literature review
Zhu, X., Li, H., Xue, T., Wang, S., Zhu, R., Luo, J., Ju, R., Zhang, P., Cui, X., & Jing, X. (2025) · APOPTOSIS · doi:10.1007/s10495-025-02181-2 · Cited by 10 · see citing works
Hao, Y., Lv, M., Peng, J. P., Kuang, D., Zhang, Z., Zhang, Z., Wang, T., Yang, B., Wei, Z., Zhou, P., et al. (2023) · Molecular Medicine Reports · doi:10.3892/mmr.2023.13093 · Cited by 10 · see citing works
Telomeres and SIRT1 as Biomarkers of Gamete Oxidative Stress, Fertility, and Potential IVF Outcome
Pańczyszyn, A., Boniewska‐Bernacka, E., Wertel, I., Sadakierska−Chudy, A., & Goc, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25168652 · Cited by 8 · see citing works
The Aging Ovary and the Tales Learned Since Fetal Development
Lopez, J., Hohensee, G., Liang, J., Sela, M., Johnson, J., & Kallen, A. N. (2023) · Sexual Development · doi:10.1159/000532072 · Cited by 8 · see citing works
Chromosome ends and the theory of marginotomy: implications for reproduction
Córdova-Oriz, I., Polonio, A. M., Cuadrado-Torroglosa, I., Chico-Sordo, L., Medrano, M., García-Velasco, J. A., & Varela, E. (2023) · Biogerontology · doi:10.1007/s10522-023-10071-w · Cited by 8 · see citing works
Polonio, A. M., Medrano, M., Chico-Sordo, L., Córdova-Oriz, I., Cozzolino, M., Montáns, J., Herraiz, S., Seli, E. U., Pellicer, A., García-Velasco, J. A., et al. (2023) · Aging · doi:10.18632/aging.204731 · Cited by 9 · see citing works
Mathematical model to study the aging of the human follicle according to the telomerase activity
Portillo, A. M., Varela, E., & García-Velasco, J. A. (2018) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2018.11.036 · Cited by 8 · see citing works
Understanding the Role of Telomere Dynamics in Normal and Dysfunctional Human Reproduction
Arias-Sosa, L. A. (2018) · Reproductive Sciences · doi:10.1177/1933719118804409 · Cited by 7 · see citing works
Yaba, A., Ağuş, S., Yıldırım, E., Erdogan, C. S., & Yılmaz, B. (2020) · Journal of Receptors and Signal Transduction · doi:10.1080/10799893.2020.1735419 · Cited by 7 · see citing works
Konstantinidou, F., Budani, M. C., Marconi, G. D., Gonnella, F., Sarra, A., Trubiani, O., Stuppia, L., Tiboni, G. M., & Gatta, V. (2022) · Antioxidants · doi:10.3390/antiox11091841 · Cited by 7 · see citing works
Córdova-Oriz, I., Kohls, G., Iglesias, C., Polonio, A. M., Chico-Sordo, L., Toribio, M., Meseguer, M., Varela, E., Pellicer, A., & García-Velasco, J. A. (2023) · Women s Health Reports · doi:10.1089/whr.2023.0013 · Cited by 7 · see citing works
Portillo, A. M., & Peláez-Rodríguez, C. (2021) · Mathematical Medicine and Biology A Journal of the IMA · doi:10.1093/imammb/dqab004 · Cited by 7 · see citing works
Fragkiadaki, P., Kouvidi, E., Angelaki, A., Nikolopoulou, D. I., Vakonaki, E., & Tsatsakis, A. M. (2024) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-024-03117-6 · Cited by 6 · see citing works
Yang, Q., Zhang, J., & Fan, Z. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-024-01466-5 · Cited by 6 · see citing works
Sayban, S., Mirfakhraie, R., Omrani, M. D., Ghaedi, H., Heidary, H., Yaghoobi, H., Azizi, F., & Pouresmaeili, F. (2018) · Meta Gene · doi:10.1016/j.mgene.2018.07.005 · Cited by 6 · see citing works
Fertility, IVF and reproductive genetics
Varela, E., Sánchez-de-Puerta, I., & García-Velasco, J. A. (2018) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000456 · Cited by 6 · see citing works
Telomerase activity, telomere length, and the euploidy rate of human embryos
Longo, M., Greco, E., Listorti, I., Varricchio, M. T., Litwicka, K., Arrivi, C., Mencacci, C., & Greco, P. (2024) · Gynecological Endocrinology · doi:10.1080/09513590.2024.2373742 · Cited by 5 · see citing works
LINE-1 Methylation sustains telomere length in pregnant women: effects on pregnancy failure
Gemmati, D., Scarpellini, F., Salvatori, F., D’Aversa, E., Marci, R., Capucci, R., Antonica, B., Grisafi, M., Turato, E., Vargas, J. V., et al. (2025) · Clinical Epigenetics · doi:10.1186/s13148-025-01937-6 · Cited by 5 · see citing works
Kim, C., Puterman, E. M., Hou, L., Slaughter, J. C., Terry, J. G., & Wellons, M. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.03.021 · Cited by 5 · see citing works
A decade of discovery: the stunning progress of premature ovarian insufficiency research in China
Wang, X., & Chen, Z. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac085 · Cited by 5 · see citing works
Self-citationProtective Effect of Tyrosol on Cisplatin–Induced Ovarian Inflammation and Oxidative Stress in Rats
Gökçek, İ., Gözer, A., Kutlu, T., Güvenç, M., Aydın, L., & Uyanık, G. (2024) · Revista Científica de la Facultad de Ciencias Veterinarias · doi:10.52973/rcfcv-e34444 · Cited by 4 · see citing works
Guo, H., Pan, S., Zhao, J., Kong, D.-X., Geng, C.-P., & Miao, S. (2025) · Gynecological Endocrinology · doi:10.1080/09513590.2025.2471549 · Cited by 4 · see citing works
Telomere length of granulosa cells is positively associated with oocyte maturation and fertilization
Jiang, S., Jiang, X., Li, D., Lyu, Q., & Li, W. (2025) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2025.104803 · Cited by 4 · see citing works
Portillo, A. M., Varela, E., & García-Velasco, J. A. (2023) · Mathematical Biosciences · doi:10.1016/j.mbs.2023.108985 · Cited by 3 · see citing works
Portillo, A. M., García-Velasco, J. A., & Varela, E. (2024) · Mathematical Biosciences · doi:10.1016/j.mbs.2024.109305 · Cited by 3 · see citing works
Sills, E. S., & Wood, S. H. (2023) · Medicines · doi:10.3390/medicines10070040 · Cited by 2 · see citing works
Ma, J., Xiong, Z.-Y., Cai, X.-C., Li, X., Ren, S.-Y., An, S.-Q., Zhang, Z., & Zhang, Y. (2024) · Aging · doi:10.18632/aging.205607 · Cited by 2 · see citing works
She, J., Liu, R., Mao, S. H., Zhou, B., Wu, X., Ding, M.-Z., Wang, L.-X., Cao, Y.-N., Wu, H., Long, Y., et al. (2024) · Reproductive and Developmental Medicine · doi:10.1097/rd9.0000000000000108 · Cited by 1 · see citing works
Cheng, Y., Huang, C.-R., Cheng, Y.-H., Chang, Y.-C., Weng, P.-L., & Lan, K. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26062513 · Cited by 1 · see citing works
Portillo, A. M., García-Velasco, J. A., & Varela, E. (2025) · Biosystems · doi:10.1016/j.biosystems.2025.105577 · Cited by 1 · see citing works
Genetics of premature ovarian insufficiency
Serna, J., Varela, E., & García-Velasco, J. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816561-4.00011-9 · Cited by 1 · see citing works
- Authors
- Xu, X., Chen, X., Zhang, X., Liu, Y., Wang, Z., Wang, P., Du, Y., Qin, Y., & Chen, Z.-J.
- Affiliations
- Shandong University (CN)
- Chinese Academy of Sciences (CN)
- Corresponding author
- Chen, Zi-Jiang
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-11-11
- Volume
- 32
- Issue
- 1
- Pages
- 201-207
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2556684732
- Cited by
- 109
- References
- 30
- Citations by year
- 2026: 3 · 2025: 10 · 2024: 14 · 2023: 18 · 2022: 17 · 2021: 16 · 2020: 14 · 2019: 6 · 2018: 10 · 2017: 1
- FWCI
- 4.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Basic Research Program of China (2012CB944700)
- Science research foundation (201402004)
- National Natural Science Foundation of China (31471352, 81270662, 81471509, 81300461, 81522018)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Keywords
- telomere length, telomerase activity, peripheral blood leukocytes, granulosa cells, biological aging, reproductive aging, premature ovarian failure, women of reproductive age, ovarian reserve, telomere repeat amplification protocol, quantitative polymerase chain reaction
- MeSH terms
- Adult, Cross-Sectional Studies, Female, Granulosa Cells, Humans, Leukocytes, Mononuclear, Telomere, Primary Ovarian Insufficiency, Telomerase
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