Supplementation of spermidine enhances the quality of postovulatory aged porcine oocytes.
Apoptosis
Autophagy
Oocyte quality
Postovulatory aging
ROS
Spermidine
Journal
Cell communication and signaling : CCS
ISSN: 1478-811X
Titre abrégé: Cell Commun Signal
Pays: England
ID NLM: 101170464
Informations de publication
Date de publication:
15 Oct 2024
15 Oct 2024
Historique:
received:
14
06
2024
accepted:
06
10
2024
medline:
16
10
2024
pubmed:
16
10
2024
entrez:
15
10
2024
Statut:
epublish
Résumé
Spermidine (SPD) is an intermediate compound in the polyamine metabolism which takes critical part in a variety of cellular processes. In particular, it has been reported to exert anti-aging effects, suppress the age-related diseases, and extend lifespan across species. However, whether it has the favorable influence on the quality of postovulatory aged oocytes remains elusive. Immunostaining and fluorescence intensity measurement were used to evaluate the effects of postovulatory aging and SPD supplementation on the oocyte fragmentation, spindle/chromosome structure, actin polymerization, dynamics of cortical granules (CGs) and ovastacin, mitochondrial distribution and function, as well as autophagy levels. In addition, in vitro sperm binding assay and in vitro fertilization (IVF) experiment were applied to assess the impacts of postovulatory aging and SPD supplementation on the sperm binding ability and fertilization capacity of oocytes. Here, we showed that supplementation of SPD during postovulatory aging could relieve the deterioration of porcine oocytes. Specifically, we found that postovulatory aging impaired the oocyte quality by damaging the morphological integrity of oocytes, maintenance of spindle/chromosome structure, and dynamics of actin cytoskeleton. Postovulatory aging also weakened the sperm binding ability and fertilization capacity of oocytes by compromising the distribution pattern of CGs and their content ovastacin. Notably, supplementation of SPD attenuated these defects in postovulatory aged porcine oocytes via strengthening mitochondrial function, eliminating excessive reactive oxygen species (ROS), inhibiting apoptosis, and enhancing autophagy levels. Altogether, our findings demonstrate that SPD supplementation is a feasible approach to ameliorate the quality of postovulatory aged oocytes, which can be potentially applied to the human assisted reproductive technology (ART) and in vitro production of animal embryos.
Sections du résumé
BACKGROUND
BACKGROUND
Spermidine (SPD) is an intermediate compound in the polyamine metabolism which takes critical part in a variety of cellular processes. In particular, it has been reported to exert anti-aging effects, suppress the age-related diseases, and extend lifespan across species. However, whether it has the favorable influence on the quality of postovulatory aged oocytes remains elusive.
METHODS
METHODS
Immunostaining and fluorescence intensity measurement were used to evaluate the effects of postovulatory aging and SPD supplementation on the oocyte fragmentation, spindle/chromosome structure, actin polymerization, dynamics of cortical granules (CGs) and ovastacin, mitochondrial distribution and function, as well as autophagy levels. In addition, in vitro sperm binding assay and in vitro fertilization (IVF) experiment were applied to assess the impacts of postovulatory aging and SPD supplementation on the sperm binding ability and fertilization capacity of oocytes.
RESULTS
RESULTS
Here, we showed that supplementation of SPD during postovulatory aging could relieve the deterioration of porcine oocytes. Specifically, we found that postovulatory aging impaired the oocyte quality by damaging the morphological integrity of oocytes, maintenance of spindle/chromosome structure, and dynamics of actin cytoskeleton. Postovulatory aging also weakened the sperm binding ability and fertilization capacity of oocytes by compromising the distribution pattern of CGs and their content ovastacin. Notably, supplementation of SPD attenuated these defects in postovulatory aged porcine oocytes via strengthening mitochondrial function, eliminating excessive reactive oxygen species (ROS), inhibiting apoptosis, and enhancing autophagy levels.
CONCLUSION
CONCLUSIONS
Altogether, our findings demonstrate that SPD supplementation is a feasible approach to ameliorate the quality of postovulatory aged oocytes, which can be potentially applied to the human assisted reproductive technology (ART) and in vitro production of animal embryos.
Identifiants
pubmed: 39407270
doi: 10.1186/s12964-024-01881-7
pii: 10.1186/s12964-024-01881-7
doi:
Substances chimiques
Spermidine
U87FK77H25
Reactive Oxygen Species
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
499Subventions
Organisme : National Key Research and Development Program of China
ID : 2023YFD1300502
Informations de copyright
© 2024. The Author(s).
Références
Wang Q, Sun Q. Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reprod Fertil Dev. 2006;19(1):1–12.
doi: 10.1071/RD06103
Miao Y, Kikuchi K, Sun Q, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15(5):573–85.
doi: 10.1093/humupd/dmp014
pubmed: 19429634
Di Nisio V, Antonouli S, Damdimopoulou P, Salumets A, Cecconi S. In vivo and in vitro postovulatory aging: when time works against oocyte quality? J Assist Reprod Genet. 2022;39(4):905–18.
doi: 10.1007/s10815-022-02418-y
pubmed: 35312936
Mailhes JB, Young D, London SN. Postovulatory ageing of mouse oocytes in Vivo and premature centromere separation and Aneuploidy. Biol Reprod. 1998;58(5):1206–10.
doi: 10.1095/biolreprod58.5.1206
pubmed: 9603254
Díaz H, Esponda P. Ageing-induced changes in the cortical granules of mouse eggs. Zygote. 2004;12(2):95–103.
doi: 10.1017/S0967199404002680
pubmed: 15460103
Fukuda A, Roudebush WE, Thatcher SS. Influences of in vitro oocyte aging on microfertilization in the mouse with reference to zona hardening. J Assist Reprod Genet. 1992;9(4):378–83.
doi: 10.1007/BF01203963
pubmed: 1472818
Takahashi T, Takahashi E, Igarashi H, Tezuka N, Kurachi H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev. 2003;66(2):143–52.
doi: 10.1002/mrd.10341
pubmed: 12950101
Liang X, Zhu J, Miao Y, Liu J, Wei L, Lu S, et al. Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochem Biophys Res Commun. 2008;371(1):16–21.
doi: 10.1016/j.bbrc.2008.03.105
pubmed: 18381202
Perez GI, Tilly JL. Cumulus cells are required for the increased apoptotic potential in oocytes of aged mice. Hum Reprod. 1997;12(12):2781–83.
doi: 10.1093/humrep/12.12.2781
pubmed: 9455852
Badenas J, Santaló J, Calafell JM, Estop AM, Egozcue J. Effect of the degree of maturation of mouse oocytes at fertilization: a source of chromosome imbalance. Gamete Res. 1989;24(2):205–18.
doi: 10.1002/mrd.1120240208
pubmed: 2793059
Pool TB, Martin JE, Ellsworth LR, Perez JB, Atiee SH. Zygote intrafallopian transfer with donor rescue: a new option for severe male factor infertility. Fertil Steril. 1990;54(1):166–68.
doi: 10.1016/S0015-0282(16)53656-5
pubmed: 2358083
Blandau RJ. The female factor in fertility and infertility: I. effects of delayed fertilization on the development of the Pronuclei in Rat Ova. Fertil Steril. 1952;3(5):349–65.
doi: 10.1016/S0015-0282(16)31020-2
pubmed: 12998674
Marston JH, Chang MC, THE FERTILIZABLE LIFE OF OVA, AND THEIR MORPHOLOGY FOLLOWING DELAYED INSEMINATION IN MATURE AND IMMATURE MICE. J Exp Zool. 1964;155:237–51.
doi: 10.1002/jez.1401550211
pubmed: 14131458
Tarín JJ, Pérez-Albalá S, Pérez-Hoyos S, Cano A. Postovulatory aging of oocytes decreases reproductive fitness and longevity of offspring. Biol Reprod. 2002;66(2):495–99.
doi: 10.1095/biolreprod66.2.495
pubmed: 11804967
Tarín JJ, Pérez-Albalá S, Aguilar A, Miñarro J, Hermenegildo C, Cano A. Long-Term effects of Postovulatory aging of mouse oocytes on offspring: a two-generational Study1. Biol Reprod. 1999;61(5):1347–55.
doi: 10.1095/biolreprod61.5.1347
pubmed: 10529284
Muñoz-Esparza NC, Latorre-Moratalla ML, Comas-Basté O, Toro-Funes N, Veciana-Nogués MT, Vidal-Carou MC. Polyamines in Food. Front Nutr. 2019;6:108.
doi: 10.3389/fnut.2019.00108
pubmed: 31355206
pmcid: 6637774
Larqué E, Sabater-Molina M, Zamora S. Biological significance of dietary polyamines. Nutrition. 2007;23(1):87–95.
doi: 10.1016/j.nut.2006.09.006
pubmed: 17113752
Madeo F, Eisenberg T, Pietrocola F, Kroemer G. Spermidine in health and disease. Science. 2018;359(6374):eaan2788.
doi: 10.1126/science.aan2788
pubmed: 29371440
Eisenberg T, Abdellatif M, Schroeder S, Primessnig U, Stekovic S, Pendl T, et al. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat Med. 2016;22(12):1428–38.
doi: 10.1038/nm.4222
pubmed: 27841876
pmcid: 5806691
Madeo F, Carmona-Gutierrez D, Kepp O, Kroemer G. Spermidine delays aging in humans. Aging-US. 2018;10(8):2209–11.
doi: 10.18632/aging.101517
Bhukel A, Madeo F, Sigrist SJ. Spermidine boosts autophagy to protect from synapse aging. Autophagy. 2017;13(2):444–45.
doi: 10.1080/15548627.2016.1265193
pubmed: 28026976
Jing Y, Yan J, Wang Q, Chen H, Ma X, Yin J, et al. Spermidine ameliorates the neuronal aging by improving the mitochondrial function in vitro. Exp Gerontol. 2018;108:77–86.
doi: 10.1016/j.exger.2018.04.005
pubmed: 29649571
Yuan X, Tian G, Pei X, Hu X, Wu J. Spermidine induces cytoprotective autophagy of female germline stem cells in vitro and ameliorates aging caused by oxidative stress through upregulated sequestosome-1/p62 expression. Cell Biosci. 2021;11(1):107.
doi: 10.1186/s13578-021-00614-4
pubmed: 34099041
Zhang Y, Bai J, Cui Z, Li Y, Gao Q, Miao Y, et al. Polyamine metabolite spermidine rejuvenates oocyte quality by enhancing mitophagy during female reproductive aging. Nat Aging. 2023;3(11):1372–86.
doi: 10.1038/s43587-023-00498-8
pubmed: 37845508
Tao Y, Liu XJ. Deficiency of ovarian ornithine decarboxylase contributes to aging-related egg aneuploidy in mice. Aging Cell. 2013;12(1):42–9.
doi: 10.1111/acel.12016
pubmed: 23061827
Tao Y, Liu D, Mo G, Wang H, Liu X. Peri-ovulatory putrescine supplementation reduces embryo resorption in older mice. Hum Reprod. 2015;30(8):1867–75.
doi: 10.1093/humrep/dev130
pubmed: 26082481
Miao Y, Cui Z, Zhu X, Gao Q, Xiong B. Supplementation of nicotinamide mononucleotide improves the quality of postovulatory aged porcine oocytes. J Mol Cell Biol. 2022;14(4):mjac025.
doi: 10.1093/jmcb/mjac025
pubmed: 35438155
Wang R, Chen J, Cui Z, Li Y, Gao Q, Miao Y, et al. Exposure to diisononyl phthalate deteriorates the quality of porcine oocytes by inducing the apoptosis. Ecotox Environ Safe. 2023;254:114768.
doi: 10.1016/j.ecoenv.2023.114768
Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146(6):R217–27.
doi: 10.1530/REP-13-0111
pubmed: 23950493
Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 2009;11(11):1305–14.
doi: 10.1038/ncb1975
pubmed: 19801973
Gupta VK, Scheunemann L, Eisenberg T, Mertel S, Bhukel A, Koemans TS, et al. Restoring polyamines protects from age-induced memory impairment in an autophagy-dependent manner. Nat Neurosci. 2013;16(10):1453–60.
doi: 10.1038/nn.3512
pubmed: 23995066
Zwighaft Z, Aviram R, Shalev M, Rousso-Noori L, Kraut-Cohen J, Golik M, et al. Circadian clock control by Polyamine Levels through a mechanism that declines with age. Cell Metab. 2015;22(5):874–85.
doi: 10.1016/j.cmet.2015.09.011
pubmed: 26456331
Jaenne J, Raina A, Siimes M, SPERMIDINE, AND SPERMINE IN RAT TISSUES AT DIFFERENT AGES. Acta Physiol Scand. 1964;62:352–58.
doi: 10.1111/j.1748-1716.1964.tb10433.x
pubmed: 14252570
Pekar T, Wendzel A, Flak W, Kremer A, Pauschenwein-Frantsich S, Gschaider A, et al. Spermidine in dementia: relation to age and memory performance. Wien Klin Wochen. 2020;132(1–2):42–6.
doi: 10.1007/s00508-019-01588-7
Hofer SJ, Simon AK, Bergmann M, Eisenberg T, Kroemer G, Madeo F. Mechanisms of spermidine-induced autophagy and geroprotection. Nat Aging. 2022;2(12):1112–29.
doi: 10.1038/s43587-022-00322-9
pubmed: 37118547
Partridge L, Fuentealba M, Kennedy BK. The quest to slow ageing through drug discovery. Nat Rev Drug Discovery. 2020;19(8):513–32.
doi: 10.1038/s41573-020-0067-7
pubmed: 32467649
Niu C, Jiang D, Guo Y, Wang Z, Ling W, An X, et al. Spermidine suppresses oxidative stress and ferroptosis by Nrf2/HO-1/GPX4 and Akt/FHC/ACSL4 pathway to alleviate ovarian damage. Life Sci. 2023;332:122109.
doi: 10.1016/j.lfs.2023.122109
pubmed: 37741320
Jiang D, Jiang Y, Long S, Chen Z, Li Y, Mo G, et al. Spermidine at supraphysiological doses induces oxidative stress and granulosa cell apoptosis in mouse ovaries. Theriogenology. 2021;168:25–32.
doi: 10.1016/j.theriogenology.2021.03.026
pubmed: 33845261