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The investigation of the role of sirtuin-1 on embryo implantation in oxidative stress–induced mice

  • Embryo Biology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

Implantation is essential for a successful pregnancy. Despite the increasing number of studies, implantation is still an unknown process. This study aimed to determine whether sirtuin-1 has a role in embryo implantation in oxidative stress–induced mice.

Methods

Pregnant mice were separated into 5 groups: control, vehicle, paraquat, SRT1720, and SRT1720+Paraquat. Paraquat is a herbicide and is used to induce oxidative stress. SRT1720 is a specific sirtuin-1 activator. Implantation and inter-implantation sites were removed in the morning of the 5th day of pregnancy after Chicago blue injection was performed. Sirtuin-1 and Forkhead box O1 (FoxO1) were detected by immunohistochemistry and Western blot while acetylated lysine was evaluated by Western blot analysis. Reactive oxygen and nitrogen species (ROS/RNS) and superoxide dismutase (SOD) activity were determined by fluorometric and spectrometric methods, respectively.

Results

Although there was no embryo implantation in paraquat-treated mice, 5 out of 9 SRT1720+Paraquat-treated mice had implantation sites which were significantly higher compared to the paraquat-treated group. Sirtuin-1 and FoxO1 expressions were increased at implantation sites of SRT1720-treated mice. ROS/RNS levels were decreased, while deacetylated FoxO1 levels and SOD activity were increased in SRT1720-treated mice.

Conclusion

Our findings suggest that sirtuin-1 may play a role in embryo implantation against oxidative stress through FoxO1-SOD signaling.

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Data availability

Available upon request.

References

  1. Vasquez YM, Wang X, Wetendorf M, Franco HL, Mo Q, Wang T, et al. FOXO1 regulates uterine epithelial integrity and progesterone receptor expression critical for embryo implantation. PLoS Genet. 2018;14(11):e1007787. https://doi.org/10.1371/journal.pgen.1007787.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Liang J, Wang S, Wang Z. Role of microRNAs in embryo implantation. Reprod Biol Endocrinol. 2017;15(1):90. https://doi.org/10.1186/s12958-017-0309-7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Tu Z, Wang Q, Cui T, Wang J, Ran H, Bao H, et al. Uterine RAC1 via Pak1-ERM signaling directs normal luminal epithelial integrity conducive to on-time embryo implantation in mice. Cell Death Differ. 2016;23(1):169–81. https://doi.org/10.1038/cdd.2015.98.

    Article  PubMed  CAS  Google Scholar 

  4. Paria BC, Song H, Dey SK. Implantation: molecular basis of embryo-uterine dialogue. Int J Dev Biol. 2001;45(3):597–605.

    PubMed  CAS  Google Scholar 

  5. Tu Z, Ran H, Zhang S, Xia G, Wang B, Wang H. Molecular determinants of uterine receptivity. Int J Dev Biol. 2014;58(2-4):147–54. https://doi.org/10.1387/ijdb.130345wh.

    Article  PubMed  CAS  Google Scholar 

  6. Matsumoto H. Molecular and cellular events during blastocyst implantation in the receptive uterus: clues from mouse models. J Reprod Dev. 2017;63:445–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol. 2005;3:28. https://doi.org/10.1186/1477-7827-3-28.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Gupta S, Ghulmiyyah J, Sharma R, Halabi J, Agarwal A. Power of proteomics in linking oxidative stress and female infertility. Biomed Res Int. 2014;2014:916212–26. https://doi.org/10.1155/2014/916212.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chandra A, Surti N, Kesavan S, Agarwal A. Significance of oxidative stress in human reproduction. Arch Med. 2009;5(1A):528–42.

    Google Scholar 

  10. Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, et al. Oxidative stress, aging, and diseases. Clin Interv Aging. 2018;13:757–72. https://doi.org/10.2147/CIA.S158513.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Gawarammana IB, Buckley NA. Medical management of paraquat ingestion. Br J Clin Pharmacol. 2011;72(5):745–57. https://doi.org/10.1111/j.1365-2125.2011.04026.x.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Blanco-Ayala T, Anderica-Romero AC, Pedraza-Chaverri J. New insights into antioxidant strategies against paraquat toxicity. Free Radic Res. 2014;48(6):623–40. https://doi.org/10.3109/10715762.2014.899694.

    Article  PubMed  CAS  Google Scholar 

  13. Xing YQ, Li A, Yang Y, Li XX, Zhang LN, Guo HC. The regulation of FOXO1 and its role in disease progression. Life Sci. 2018;193:124–31. https://doi.org/10.1016/j.lfs.2017.11.030.

    Article  PubMed  CAS  Google Scholar 

  14. Tia N, Singh AK, Pandey P, Azad CS, Chaudhary P, Gambhir IS. Role of Forkhead Box O (FOXO) transcription factor in aging and diseases. Gene. 2018;648:97–105. https://doi.org/10.1016/j.gene.2018.01.051.

    Article  PubMed  CAS  Google Scholar 

  15. Murtaza G, Khan AK, Rashid R, Muneer S, Hasan SMF, Chen J. FOXO transcriptional factors and long-term living. Oxidative Med Cell Longev. 2017;2017:3494289–8. https://doi.org/10.1155/2017/3494289.

    Article  CAS  Google Scholar 

  16. Obsil T, Obsilova V. Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene. 2008;27(16):2263–75. https://doi.org/10.1038/onc.2008.20.

    Article  PubMed  CAS  Google Scholar 

  17. Merksamer PI, Liu Y, He W, Hirschey MD, Chen D, Verdin E. The sirtuins, oxidative stress and aging: an emerging link. Aging. 2013;5(3):144–50. https://doi.org/10.18632/aging.100544.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Kobayashi Y, Furukawa-Hibi Y, Chen C, Horio Y, Isobe K, Ikeda K, et al. SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int J Mol Med. 2005;16(2):237–43.

    PubMed  CAS  Google Scholar 

  19. Favero G, Franceschetti L, Rodella LF, Rezzani R. Sirtuins, aging, and cardiovascular risks. Age. 2015;37(4):9804. https://doi.org/10.1007/s11357-015-9804-y.

    Article  PubMed  CAS  Google Scholar 

  20. Yao H, Hwang JW, Sundar IK, Friedman AE, McBurney MW, Guarente L, et al. SIRT1 redresses the imbalance of tissue inhibitor of matrix metalloproteinase-1 and matrix metalloproteinase-9 in the development of mouse emphysema and human COPD. Am J Physiol Lung Cell Mol Physiol. 2013;305(9):L615–24. https://doi.org/10.1152/ajplung.00249.2012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Mitchell SJ, Martin-Montalvo A, Mercken EM, Palacios HH, Ward TM, Abulwerdi G, et al. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep. 2014;6(5):836–43. https://doi.org/10.1016/j.celrep.2014.01.031.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Zhou XL, Xu JJ, Ni YH, Chen XC, Zhang HX, Zhang XM, et al. SIRT1 activator (SRT1720) improves the follicle reserve and prolongs the ovarian lifespan of diet-induced obesity in female mice via activating SIRT1 and suppressing mTOR signaling. J Ovarian Res. 2014;7:97. https://doi.org/10.1186/s13048-014-0097-z.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Shirane A, Wada-Hiraike O, Tanikawa M, Seiki T, Hiraike H, Miyamoto Y, et al. Regulation of SIRT1 determines initial step of endometrial receptivity by controlling E-cadherin expression. Biochem Biophys Res Commun. 2012;424(3):604–10. https://doi.org/10.1016/j.bbrc.2012.06.160.

    Article  PubMed  CAS  Google Scholar 

  24. Paria BC, Huet-Hudson YM, Dey SK. Blastocyst’s state of activity determines the “window” of implantation in the receptive mouse uterus. Proc Natl Acad Sci U S A. 1993;90(21):10159–62. https://doi.org/10.1073/pnas.90.21.10159.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Song H, Lim H, Paria BC, Matsumoto H, Swift LL, Morrow J, et al. Cytosolic phospholipase A2α is crucial for ‘on-time’embryo implantation that directs subsequent development. Development. 2002;129(12):2879–89.

    Article  CAS  PubMed  Google Scholar 

  26. Acar N, Soylu H, Edizer I, Ozbey O, Er H, Akkoyunlu G, et al. Expression of nuclear factor erythroid 2-related factor 2 (Nrf2) and peroxiredoxin 6 (Prdx6) proteins in healthy and pathologic placentas of human and rat. Acta Histochem. 2014;116(8):1289–300. https://doi.org/10.1016/j.acthis.2014.07.012.

    Article  PubMed  CAS  Google Scholar 

  27. Acar N, Turkay Korgun E, Ustunel I. Cell cycle inhibitor p57 expression in normal and diabetic rat placentas during some stages of pregnancy. 2012;27(1):59–68. https://doi.org/10.14670/HH-27.59.

  28. Zhang Y, Xu Z, Wang H, Dong Y, Shi HN, Culley DJ, et al. Anesthetics isoflurane and desflurane differently affect mitochondrial function, learning, and memory. Ann Neurol. 2012;71(5):687–98. https://doi.org/10.1002/ana.23536.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Dhall S, Do DC, Garcia M, Kim J, Mirebrahim SH, Lyubovitsky J, et al. Generating and reversing chronic wounds in diabetic mice by manipulating wound redox parameters. J Diabetes Res. 2014;2014:562625–18. https://doi.org/10.1155/2014/562625.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Li Y, Sun X, Dey SK. Entosis allows timely elimination of the luminal epithelial barrier for embryo implantation. Cell Rep. 2015;11(3):358–65. https://doi.org/10.1016/j.celrep.2015.03.035.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Hausburg MA, Dekrey GK, Salmen JJ, Palic MR, Gardiner CS. Effects of paraquat on development of preimplantation embryos in vivo and in vitro. Reprod Toxicol. 2005;20(2):239–46. https://doi.org/10.1016/j.reprotox.2005.03.006.

    Article  PubMed  CAS  Google Scholar 

  32. Hirota Y, Acar N, Tranguch S, Burnum KE, Xie H, Kodama A, et al. Uterine FK506-binding protein 52 (FKBP52)-peroxiredoxin-6 (PRDX6) signaling protects pregnancy from overt oxidative stress. Proc Natl Acad Sci U S A. 2010;107(35):15577–82. https://doi.org/10.1073/pnas.1009324107.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Adiguzel D, Sahin P, Kuscu N, Ozkavukcu S, Bektas NI, Celik-Ozenci C. Spatiotemporal expression and regulation of FoxO1 in mouse uterus during peri-implantation period. PLoS One. 2019;14(5):e0216814. https://doi.org/10.1371/journal.pone.0216814.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Sin TK, Yung BY, Siu PM. Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem. 2015;35(2):541–52. https://doi.org/10.1159/000369718.

    Article  PubMed  CAS  Google Scholar 

  35. Costa Cdos S, Rohden F, Hammes TO, Margis R, Bortolotto JW, Padoin AV, et al. Resveratrol upregulated SIRT1, FOXO1, and adiponectin and downregulated PPARgamma1-3 mRNA expression in human visceral adipocytes. Obes Surg. 2011;21(3):356–61. https://doi.org/10.1007/s11695-010-0251-7.

    Article  PubMed  Google Scholar 

  36. Brown AK, Webb AE. Regulation of FOXO factors in mammalian cells. Curr Top Dev Biol. Elsevier. 2018:165–92.

  37. Nogueiras R, Habegger KM, Chaudhary N, Finan B, Banks AS, Dietrich MO, et al. Sirtuin 1 and sirtuin 3: physiological modulators of metabolism. Physiol Rev. 2012;92(3):1479–514. https://doi.org/10.1152/physrev.00022.2011.

    Article  PubMed  CAS  Google Scholar 

  38. Lipphardt M, Song JW, Goligorsky MS. Sirtuin 1 and endothelial glycocalyx. Pflugers Arch. 2020;472(8):991–1002. https://doi.org/10.1007/s00424-020-02407-z.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Wu B, Feng JY, Yu LM, Wang YC, Chen YQ, Wei Y, et al. Icariin protects cardiomyocytes against ischaemia/reperfusion injury by attenuating sirtuin 1-dependent mitochondrial oxidative damage. Br J Pharmacol. 2018;175(21):4137–53. https://doi.org/10.1111/bph.14457.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci. 2008;4(2):89.

    PubMed  PubMed Central  CAS  Google Scholar 

  41. Li S, Zhu Z, Xue M, Yi X, Liang J, Niu C, et al. Fibroblast growth factor 21 protects the heart from angiotensin II-induced cardiac hypertrophy and dysfunction via SIRT1. Biochim Biophys Acta Mol basis Dis. 2019;1865(6):1241–52. https://doi.org/10.1016/j.bbadis.2019.01.019.

    Article  PubMed  CAS  Google Scholar 

  42. Yang L, Zhang B, Yuan Y, Li C, Wang Z. Oxidative stress and DNA damage in utero and embryo implantation of mice exposed to carbon disulfide at peri-implantation. Hum Exp Toxicol. 2014;33(4):424–34. https://doi.org/10.1177/0960327112474849.

    Article  PubMed  CAS  Google Scholar 

  43. Ruder EH, Hartman TJ, Blumberg J, Goldman MB. Oxidative stress and antioxidants: exposure and impact on female fertility. Hum Reprod Update. 2008;14(4):345–57. https://doi.org/10.1093/humupd/dmn011.

    Article  PubMed  CAS  Google Scholar 

  44. Liu G, Dong Y, Wang Z, Cao J, Chen Y. Restraint stress alters immune parameters and induces oxidative stress in the mouse uterus during embryo implantation. Stress. 2014;17(6):494–503. https://doi.org/10.3109/10253890.2014.966263.

    Article  PubMed  CAS  Google Scholar 

  45. Ait-Bali Y, Ba-M’hamed S, Bennis M. Prenatal paraquat exposure induces neurobehavioral and cognitive changes in mice offspring. Environ Toxicol Pharmacol. 2016;48:53–62. https://doi.org/10.1016/j.etap.2016.10.008.

    Article  PubMed  CAS  Google Scholar 

  46. Almeida LL, Teixeira AAC, Soares AF, Cunha FMD, Silva VADJ, Vieira Filho LD, et al. Effects of melatonin in rats in the initial third stage of pregnancy exposed to sub-lethal doses of herbicides. Acta Histochem. 2017;119(3):220–7. https://doi.org/10.1016/j.acthis.2017.01.003.

    Article  PubMed  CAS  Google Scholar 

  47. Michan S, Juan AM, Hurst CG, Cui Z, Evans LP, Hatton CJ et al. Sirtuin1 over-expression does not impact retinal vascular and neuronal degeneration in a mouse model of oxygen-induced retinopathy. PloS one. 2014;9(1):e85031. https://doi.org/10.1371/journal.pone.0085031.

  48. Wan X, Wen JJ, Koo SJ, Liang LY, Garg NJ. SIRT1-PGC1alpha-NFkappaB pathway of oxidative and inflammatory stress during trypanosoma cruzi infection: benefits of SIRT1-targeted therapy in improving heart function in chagas disease. PLoS Pathog. 2016;12(10):e1005954. https://doi.org/10.1371/journal.ppat.1005954.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Nguyen LT, Mak CH, Chen H, Zaky AA, Wong MG, Pollock CA, et al. SIRT1 attenuates kidney disorders in male offspring due to maternal high-fat diet. Nutrients. 2019;11(1):146.

    Article  CAS  PubMed Central  Google Scholar 

  50. Yanagisawa S, Baker JR, Vuppusetty C, Koga T, Colley T, Fenwick P et al. The dynamic shuttling of SIRT1 between cytoplasm and nuclei in bronchial epithelial cells by single and repeated cigarette smoke exposure. PloS one. 2018;13(3):e0193921. https://doi.org/10.1371/journal.pone.0193921.

  51. Jin Q, Yan T, Ge X, Sun C, Shi X, Zhai Q. Cytoplasm-localized SIRT1 enhances apoptosis. J Cell Physiol. 2007;213(1):88–97. https://doi.org/10.1002/jcp.21091.

    Article  PubMed  CAS  Google Scholar 

  52. Hwang JW, Yao H, Caito S, Sundar IK, Rahman I. Redox regulation of SIRT1 in inflammation and cellular senescence. Free Radic Biol Med. 2013;61:95–110. https://doi.org/10.1016/j.freeradbiomed.2013.03.015.

    Article  PubMed  CAS  Google Scholar 

  53. Ding YW, Zhao GJ, Li XL, Hong GL, Li MF, Qiu QM, et al. SIRT1 exerts protective effects against paraquat-induced injury in mouse type II alveolar epithelial cells by deacetylating NRF2 in vitro. Int J Mol Med. 2016;37(4):1049–58. https://doi.org/10.3892/ijmm.2016.2503.

    Article  PubMed  CAS  Google Scholar 

  54. He J, Zhang A, Song Z, Guo S, Chen Y, Liu Z, et al. The resistant effect of SIRT1 in oxidative stress-induced senescence of rat nucleus pulposus cell is regulated by Akt-FoxO1 pathway. Biosci Rep. 2019;39. https://doi.org/10.1042/BSR20190112.

  55. Caito S, Rajendrasozhan S, Cook S, Chung S, Yao H, Friedman AE, et al. SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J. 2010;24(9):3145–59. https://doi.org/10.1096/fj.09-151308.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Li S, Zhao G, Chen L, Ding Y, Lian J, Hong G, et al. Resveratrol protects mice from paraquat-induced lung injury: the important role of SIRT1 and NRF2 antioxidant pathways. Mol Med Rep. 2016;13(2):1833–8. https://doi.org/10.3892/mmr.2015.4710.

    Article  PubMed  CAS  Google Scholar 

  57. Komatsu T, Park S, Hayashi H, Mori R, Yamaza H, Shimokawa I. Mechanisms of calorie restriction: a review of genes required for the life-extending and tumor-inhibiting effects of calorie restriction. Nutrients. 2019;11(12). https://doi.org/10.3390/nu11123068.

  58. Zhang T, Kraus WL. SIRT1-dependent regulation of chromatin and transcription: linking NAD(+) metabolism and signaling to the control of cellular functions. Biochim Biophys Acta. 2010;1804(8):1666–75. https://doi.org/10.1016/j.bbapap.2009.10.022.

    Article  PubMed  CAS  Google Scholar 

  59. Daitoku H, Hatta M, Matsuzaki H, Aratani S, Ohshima T, Miyagishi M, et al. Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A. 2004;101(27):10042–7. https://doi.org/10.1073/pnas.0400593101.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Song S, Chu L, Liang H, Chen J, Liang J, Huang Z, et al. Protective effects of dioscin against doxorubicin-induced hepatotoxicity via regulation of Sirt1/FOXO1/NF-kappab Signal. Front Pharmacol. 2019;10:1030. https://doi.org/10.3389/fphar.2019.01030.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Qiang L, Banks AS, Accili D. Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J Biol Chem. 2010;285(35):27396–401. https://doi.org/10.1074/jbc.M110.140228.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Qiao L, Shao J. SIRT1 regulates adiponectin gene expression through Foxo1-C/enhancer-binding protein alpha transcriptional complex. J Biol Chem. 2006;281(52):39915–24. https://doi.org/10.1074/jbc.M607215200.

    Article  PubMed  CAS  Google Scholar 

  63. Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8(4):333–41. https://doi.org/10.1016/j.cmet.2008.08.014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Shao D, Zhai P, Del Re DP, Sciarretta S, Yabuta N, Nojima H, et al. A functional interaction between Hippo-YAP signalling and FoxO1 mediates the oxidative stress response. Nat Commun. 2014;5(1):1–10.

    Google Scholar 

  65. Ramandeep K, Kapil G, Harkiran K. Correlation of enhanced oxidative stress with altered thyroid profile: probable role in spontaneous abortion. Int J Appl Basic Med Res. 2017;7(1):20–5. https://doi.org/10.4103/2229-516X.198514.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Sugino N, Karube-Harada A, Sakata A, Takiguchi S, Kato H. Different mechanisms for the induction of copper-zinc superoxide dismutase and manganese superoxide dismutase by progesterone in human endometrial stromal cells. Hum Reprod. 2002;17(7):1709–14. https://doi.org/10.1093/humrep/17.7.1709.

    Article  PubMed  CAS  Google Scholar 

  67. Sugino N. The role of oxygen radical-mediated signaling pathways in endometrial function. Placenta. 2007;28(Suppl A):S133–6. https://doi.org/10.1016/j.placenta.2006.12.002.

    Article  PubMed  CAS  Google Scholar 

  68. Li J, Qi J, Yao G, Zhu Q, Li X, Xu R, et al. Deficiency of sirtuin 1 impedes endometrial decidualization in recurrent implantation failure patients. Front Cell Dev Biol. 2021;9:598364. https://doi.org/10.3389/fcell.2021.598364.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by The Scientific Research Projects Coordination Unit of Akdeniz University (Project Number: TYL-2017-2427)

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Authors and Affiliations

  1. Department of Histology and Embryology, Faculty of Medicine, Akdeniz University, Antalya, Turkey

    Kubra Aksu, Ezgi Golal, Ismail Ustunel & Nuray Acar

  2. Department of Medical Biochemistry, Faculty of Medicine, Akdeniz University, Antalya, Turkey

    Mutay Aydın Aslan

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  1. Kubra Aksu
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  2. Ezgi Golal
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  3. Mutay Aydın Aslan
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  4. Ismail Ustunel
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KA: investigation, formal analysis, writing – original draft, visualization; EG: formal analysis; MAA: investigation, formal analysis; IU: review and editing; NA: conceptualization, writing – review and editing, funding acquisition

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Correspondence to Nuray Acar.

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The experimental protocol was approved by the Animal Care and Use Committee of Akdeniz University Faculty of Medicine (Number of the Ethical Approval 2017.02.15).

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Aksu, K., Golal, E., Aslan, M.A. et al. The investigation of the role of sirtuin-1 on embryo implantation in oxidative stress–induced mice. J Assist Reprod Genet 38, 2349–2361 (2021). https://doi.org/10.1007/s10815-021-02229-7

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