Protective effect of small peptides from Periplaneta americana on cyclophosphamide-induced premature ovarian failure.
SIRT1/p53 signaling pathway
cyclophosphamide
mice
premature ovarian failure
small peptides from Periplaneta americana
Journal
The journal of obstetrics and gynaecology research
ISSN: 1447-0756
Titre abrégé: J Obstet Gynaecol Res
Pays: Australia
ID NLM: 9612761
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
revised:
11
10
2021
received:
22
05
2021
accepted:
17
10
2021
pubmed:
4
11
2021
medline:
5
1
2022
entrez:
3
11
2021
Statut:
ppublish
Résumé
To investigate the protective effect of small peptides from Periplaneta americana (SPPA) on cyclophosphamide (CP)-induced premature ovarian failure (POF) in mice. Silent mating type information regulation 2 homolog 1 (SIRT1) /tumor-associated protein 53 (p53) signaling pathway plays an important role in delaying POF. Hematopoietic progenitor cell antigen (CD34) reflects ovarian aging from the side. However, whether SPPA inhibits POF in mice by influencing the SIRT1/p53 pathway and CD34 expression remains to be studied. Forty female Kun Ming (KM) mice were divided into four groups: a control group (normal saline, n = 10), POF model group (160 mg/kg CP, n = 10), SPPA low-dosage group (160 mg/kg CP + 100 mg/kg SPPA, n = 10), and SPPA high-dosage group (160 mg/kg CP + 200 mg/kg SPPA, n = 10). CP administration route is intraperitoneal injection, and SPPA administration route is intragastric. Eyeball enucleation blood samples and the ovaries of mice were collected by midline laparatomy and oopherectomy, and the malondialdehyde (MDA), nitric oxide (NO), superoxide dismutase (SOD), follicle-stimulating hormone (FSH), and anti-Müllerian hormone (AMH) concentrations were tested. Immunohistochemical tests for the expressions of SIRT1, p53, and CD34 were carried out. Finally, ovarian mRNA levels of SIRT1 and p53 were detected with real-time fluorescence quantification PCR (qRT-PCR). A mouse model of POF was generated using 160 mg/kg of CP. Compared with POF group, we found that plasma NO, MDA, and FSH decreased, while AMH and SOD increased in the SPPA low-dose group. Compared with the POF group, the SPPA low- and high-dosage groups achieved significant growth in the number of primordial, primary, and total number of healthy follicles at all levels, but sharp reductions in the number of atretic follicles. In addition, we found downregulated protein and mRNA expression of SIRT1, and upregulated that of p53 were observed in ovarian tissues of treated mice with POF, in immunohistochemistry experiments and qPCR experiments. In contrast, high protein and mRNA expression of SIRT1, and low that of p53 were observed in SPPA treatment groups. And the results of CD34 protein expression were consistent with that of SIRT1. In total, SPPA significantly inhibited POF caused by CP in mice via activation of the SIRT1/p53 signaling pathway in the mouse ovary.
Substances chimiques
Peptides
0
Cyclophosphamide
8N3DW7272P
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
188-199Subventions
Organisme : Fund program of Scientific Research, Ministry of Education, Yunnan Province
ID : 2021Y414
Organisme : Dali university
Organisme : Ministry of Education
Organisme : National Natural Science Foundation of China
ID : 31760719
Organisme : Laboratory Open Project of Dali University, Yunnan Province
ID : KF2021017
Informations de copyright
© 2021 Japan Society of Obstetrics and Gynecology.
Références
Kawamura K, Kawamura N, Hsueh AJ. Activation of dormant follicles: a new treatment for premature ovarian failure? Curr Opin Obstet Gynecol. 2016;28:217-22. https://doi.org/10.1097/GCO.0000000000000268
Pimenta F, Maroco J, Ramos C, Leal I. Predictors of weight variation and weight gain in peri- and post-menopausal women. J Health Psychol. 2014;19:993-1002. https://doi.org/10.1177/1359105313483153
van Rijn LE, Pop VJ, Williams GR. Low bone mineral density is related to high physiological levels of free thyroxine in peri-menopausal women. Eur J Endocrinol. 2014;170:461-8. https://doi.org/10.1530/EJE-13-0769
Massin N, Méduri G, Bachelot A, Misrahi M, Kuttenn F, Touraine P. Evaluation of different markers of the ovarian reserve in patients presenting with premature ovarian failure. Mol Cell Endocrinol. 2008;282:95-100. https://doi.org/10.1016/j.mce.2007.11.017
Weng Q, Liu Z, Li B, Liu K, Wu W, Liu H. Oxidative stress induces mouse follicular granulosa cells apoptosis via JNK/FoxO1 pathway. PLoS One. 2016;11:e167869. https://doi.org/10.1371/journal.pone.0167869
Liu ZQ, Shen M, Wu WJ, Li BJ, Weng QN, Li M, et al. Expression of PUMA in follicular granulosa cells regulated by FoxO1 activation during oxidative stress. Reprod Sci. 2015;22:696-705. https://doi.org/10.1177/1933719114556483
Tiwari M, Prasad S, Tripathi A, Pandey AN, Ali I, Singh AK, et al. Apoptosis in mammalian oocytes:a review. Apoptosis. 2015;20:1019-25. https://doi.org/10.1007/s10495-015-1136-y
Sun H, Li Y, Li X, Zhang Y. The inhibition of serine/threonine protein phosphatase type 5 mediates cantharidin toxicity to control Periplaneta americana (L.). Insects. 2020;11:682. https://doi.org/10.3390/insects11100682
Zeng C, Liao Q, Hu Y, Shen Y, Geng F, Chen L. The role of Periplaneta americana (Blattodea: Blattidae) in modern versus traditional Chinese medicine. J Med Entomol. 2019;56:1522-6. https://doi.org/10.1093/jme/tjz081
Wang Q, Kong C, Liu K, Fu R, Si H, Sui S. Protective effects of small peptides from Periplaneta americana on cyclophosphamide-induced oxidative stress in rat ovaries. Indian J Pharm Educ. 2021;55:782-92. https://doi.org/10.5530/ijper.55.3.151
Wang Q, Fu R, Kong C, Liu K, Si H, Sui S. The protective effect of small peptides from Periplaneta americana on hydrogen peroxide-induced apoptosis of granular cells. In Vitro Cell Dev Biol Anim. 2021;57:610-9. https://doi.org/10.1007/s11626-021-00586-2
Blander G, Guarente L. The Sir2 family of protein deacetylases. Annu Rev Biochem. 2004;73:417-35. https://doi.org/10.1146/annurev.biochem.73.011303.073651
Ong ALC, Ramasamy TS. Role of sirtuin1-p53 regulatory axis in aging, cancer and cellular reprogramming. Ageing Res Rev. 2018;43:64-80. https://doi.org/10.1016/j.arr.2018.02.004
Nie Z, Zhang L, Chen W, Zhang Y, Wang W, Hua R, et al. The protective effects of resveratrol pretreatment in cyclophosphamide-induced rat ovarian injury: an vivo study. Gynecol Endocrinol. 2021;17:1-6. https://doi.org/10.1080/09513590.2021.1885643
Molavi M, Razi M, Malekinejad H, Amniattalab A, Rezaie H. Vitamin E improved cypermethrin-induced damages in the ovary of rats; evidence for angiogenesis and p53 involvement. Pestic Biochem Physiol. 2014;110:27-35. https://doi.org/10.1016/j.pestbp.2014.02.004
Holyoake TL, Alcorn MJ. CD34+ positive haemopoietic cells: biology and clinical applications. Blood Rev. 1994;8:113-24. https://doi.org/10.1016/s0268-960x(05)80016-5
Li J, Long H, Cong Y, Gao H, Lyu Q, Yu S, et al. Quercetin prevents primordial follicle loss via suppression of PI3K/Akt/Foxo3a pathway activation in cyclophosphamide-treated mice. Reprod Biol Endocrinol. 2021;19:63. https://doi.org/10.1186/s12958-021-00743-y
Huang B, Ding C, Zou Q, Wang W, Li H. Cyclophosphamide regulates N6-methyladenosine and m6A RNA enzyme levels in human granulosa cells and in ovaries of a premature ovarian aging mouse model. Front Endocrinol (Lausanne). 2019;10:415. https://doi.org/10.3389/fendo.2019.00415
Zhang J, Fang L, Lu Z, Xiong J, Wu M, Shi L, et al. Are sirtuins markers of ovarian aging? Gene. 2016;575:680-6. https://doi.org/10.1016/j.gene.2015.09.043
Moore MJ. Clinical pharmacokinetics of cyclophosphamide. Clin Pharmacokinet. 1991;20:194-208. https://doi.org/10.2165/00003088-199120030-00002
Bouhifd M, Hartung T, Hogberg HT, Kleensang A, Zhao L. Review: toxicometabolomics. J Appl Toxicol. 2013;33:1365-83. https://doi.org/10.1002/jat.2874
Sui S, He B, Jia Y, Li R, Cai D, Li X, et al. Maternal protein restriction during gestation and lactation programs offspring ovarian steroidogenesis and folliculogenesis in the prepubertal gilts. J Steroid Biochem Mol Biol. 2014;143:267-76. https://doi.org/10.1016/j.jsbmb.2014.04.010
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
Lopez SG, Luderer U. Effects of cyclophosphamide and buthionine sulfoximine on ovarian glutathione and apoptosis. Free Radic Biol Med. 2004;36:1366-77. https://doi.org/10.1016/j.freeradbiomed.2004.02.067
Jutiviboonsuk A, Salang L, Eamudomkarn N, Mahakkanukrauh A, Suwannaroj S, Foocharoen C. Prevalence and clinical associations with premature ovarian insufficiency, early menopause, and low ovarian reserve in systemic sclerosis. Clin Rheumatol. 2021;40:2267-75. https://doi.org/10.1007/s10067-020-05522-5
Khedr NF. Protective effect of mirtazapine and hesperidin on cyclophosphamide-induced oxidative damage and infertility in rat ovaries. Exp Biol Med (Maywood). 2015;240:1682-9. https://doi.org/10.1177/1535370215576304
Farokhi F, Sadrkhanlou R, Hasanzadeh S. Morphological and morphometrical study of cyclophosphamide-induced changes in the ovary and uterus in the Syrian mice. Iran J Vet Res. 2007;8:337-42. https://doi.org/10.22099/IJVR.2007.11
Pascuali N, Scotti L, Di Pietro M, et al. Ceramide-1-phosphate has protective properties against cyclophosphamide-induced ovarian damage in a mice model of premature ovarian failure. Hum Reprod. 2018;33:844-59. https://doi.org/10.1093/humrep/dey045
Wathes DC, Abayasekara DR, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod. 2007;77:190-201. https://doi.org/10.1095/biolreprod.107.060558
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
Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med. 2008;44:1295-304. https://doi.org/10.1016/j.freeradbiomed.2007.11.014
Salih SM, Ringelstetter AK, Elsarrag MZ, Abbott DH, Roti ECR. Dexrazoxane abrogates acute doxorubicin toxicity in marmoset ovary. Biol Reprod. 2015;92:73. https://doi.org/10.1095/biolreprod.114.119495
Pandir D, Kara O, Kara M. Protective effect of bilberry (Vaccinium myrtillus L.) on cisplatin induced ovarian damage in rat. Cytotechnology. 2014;66:677-85. https://doi.org/10.1007/s10616-013-9621-z
Gleicher N, Weghofer A, Barad DH. Defining ovarian reserve to better understand ovarian aging. Reprod Biol Endocrinol. 2011;9:23. https://doi.org/10.1186/1477-7827-9-23
Zhang H, Luo Q, Lu X, Yin N, Zhou D, Zhang L, et al. Effects of hPMSCs on granulosa cell apoptosis and AMH expression and their role in the restoration of ovary function in premature ovarian failure mice. Stem Cell Res Ther. 2018;9:20. https://doi.org/10.1186/s13287-017-0745-5
Ding C, Zou Q, Wang F, Wu H, Wang W, Li H, et al. HGF and BFGF secretion by human adipose-derived stem cells improves ovarian function during natural aging via activation of the SIRT1/FOXO1 signaling pathway. Cell Physiol Biochem. 2018;45:1316-32. https://doi.org/10.1159/000487559
Ma R, Liang W, Sun Q, Qiu X, Lin Y, Ge X, et al. Sirt1/Nrf2 pathway is involved in oocyte aging by regulating cyclin B1. Aging (Albany NY). 2018;10:2991-3004. https://doi.org/10.18632/aging.101609
Chen C, Zhou M, Ge Y, Wang X. SIRT1 and aging related signaling pathways. Mech Ageing Dev. 2020;187:111215. https://doi.org/10.1016/j.mad.2020.111215
Liang M, Yao G, Yin M, Lü M, Tian H, Liu L, et al. Transcriptional cooperation between p53 and NF-κB p65 regulates microRNA-224 transcription in mouse ovarian granulosa cells. Mol Cell Endocrinol. 2013;370:119-29. https://doi.org/10.1016/j.mce.2013.02.014
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;101:10042-7. https://doi.org/10.1073/pnas.0400593101
Lambert AJ, Brand MD. Research on mitochondria and aging, 2006-2007. Aging Cell. 2007;6:417-20. https://doi.org/10.1111/j.1474-9726.2007.00316.x
Mantel C, Broxmeyer HE. Sirtuin 1, stem cells, aging, and stem cell aging. Curr Opin Hematol. 2008;15:326-31. https://doi.org/10.1097/MOH.0b013e3283043819
Mahjabeen S, Hatipoglu MK, Benbrook DM, Kosanke SD, Garcia-Contreras D, Garcia-Contreras L. Influence of the estrus cycle of the mouse on the disposition of SHetA2 after vaginal administration. Eur J Pharm Biopharm. 2018;130:272-80. https://doi.org/10.1016/j.ejpb.2018.07.004