Low-moderate dietary phytoestrogens transiently disrupt spermatogenesis and the seminal plasma proteome in the ram

in Reproduction
Authors:
Kelsey R PoolUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Tayler C KentSchool of Veterinary & Life Sciences, Murdoch University, WA, Australia

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Luoyang DingUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Callum ConnollyUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Kevin J FosterUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Gereltsetseg EnkhbatUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Megan H RyanUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Dominique BlacheUWA institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia

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Correspondence should be addressed to K Pool; Email: kelsey.pool@uwa.edu.au
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In brief

Dietary phytoestrogens disrupt a specific stage of ram spermatogenesis, causing subtle decreases in sperm quality by affecting the expression of pathways involved in the structural integrity of the spermatozoa. This paper demonstrates for the first time that ram reproduction is compromised by oestrogenic pasture, whilst also providing a longitudinal model for the impact of phytoestrogens on male fertility.

Abstract

Compounds with oestrogen-like actions are now common in both the Western diet. The long-term impacts and underlying mechanisms by which oestrogenic compounds alter male reproduction, however, are unclear. To investigate this, we used a longitudinal sheep model examining the impact of oestrogenic pasture consumption on semen quality and production, testicular size, sexual behaviour and the seminal plasma proteome of Merino rams (n = 20), over a full spermatogenic cycle and in the subsequent breeding season. Throughout the study period, sexual behaviour, sperm production and motility were similar between the exposed and non-exposed rams (P > 0.05). However, between 5 and 8 weeks of exposure to dietary phytoestrogens, rams produced a higher percentage of spermatozoa with a specific malformation of the sperm midpiece and reduced DNA integrity, compared to non-exposed rams (P < 0.001). Investigation into the seminal plasma proteome revealed 93 differentially expressed proteins between phytoestrogen-exposed and control rams (P < 0.05). Exposure to phytoestrogens increased the expression of proteins involved in cellular structure development, actin cytoskeleton reorganisation, regulation of cell function and decreased expression in those related to catabolic processes. The greatest fold changes were in proteins involved in the assembly of the sperm flagella, removal of cytoplasm, spermatid development and maintenance of DNA integrity. After returning to non-oestrogenic pasture, no differences in any measure were observed between treatment groups during the subsequent breeding season. We conclude that dietary phytoestrogens can transiently disrupt specific stages of ram spermatogenesis, causing subtle decreases in sperm quality by affecting the expression of pathways involved in the structural integrity of the spermatozoa.

 

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  • Adachi T, Ono Y, Koh KB, Takashima K, Tainaka H, Matsuno Y, Nakagawa S, Todaka E, Sakurai K & Fukata H et al.2004 Long-term alteration of gene expression without morphological change in testis after neonatal exposure to genistein in mice: toxicogenomic analysis using cDNA microarray. Food and Chemical Toxicology 42 445452. (https://doi.org/10.1016/j.fct.2003.10.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Adams NR 1976 Pathological changes in the tissues of infertile ewes with clover disease. Journal of Comparative Pathology 86 2935. (https://doi.org/10.1016/0021-9975(7690024-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ajayi AF & Akhigbe RE 2020 The physiology of male reproduction: impact of drugs and their abuse on male fertility. Andrologia 52 e13672. (https://doi.org/10.1111/AND.13672)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aquila S, Santoro M, De Amicis F, Guido C, Bonofiglio D, Lanzino M, Cesario MG, Perrotta I, Sisci D & Morelli C 2013 Red wine consumption may affect sperm biology: the effects of different concentrations of the phytoestrogen myricetin on human male gamete function. Molecular Reproduction and Development 80 155165. (https://doi.org/10.1002/mrd.22145)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Assinder S, Davis R, Fenwick M & Glover A 2007 Adult-only exposure of male rats to a diet of high phytoestrogen content increases apoptosis of meiotic and post-meiotic germ cells. Reproduction 133 1119. (https://doi.org/10.1530/REP.1.01211)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bacciottini L, Falchetti A, Pampaloni B, Bartolini E, Carossino AM & Brandi ML 2007 Phytoestrogens: food or drug? Clinical Cases in Mineral and Bone Metabolism 4 123–130. (https://doi.org/10.1201/b14631-25)

    • Search Google Scholar
    • Export Citation
  • Bates D, Mächler M, Bolker BM & Walker SC 2015 Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67. (https://doi.org/10.18637/jss.v067.i01)

    • Search Google Scholar
    • Export Citation
  • Bernecic NC, Gadella BM, Leahy T & de Graaf SP 2019 Novel methods to detect capacitation-related changes in spermatozoa. Theriogenology 137 5666. (https://doi.org/10.1016/j.theriogenology.2019.05.038)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Braun RE 2001 Packaging paternal chromosomes with protamine. Nature Genetics 28 1012. (https://doi.org/10.1038/ng0501-10)

  • Camargo M, Intasqui P & Bertolla RP 2018 Understanding the seminal plasma proteome and its role in male fertility. Basic and Clinical Andrology 28 6. (https://doi.org/10.1186/S12610-018-0071-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cardoso JR & Báo SN 2007 Effects of chronic exposure to soy meal containing diet or soy derived isoflavones supplement on semen production and reproductive system of male rabbits. Animal Reproduction Science 97 237245. (https://doi.org/10.1016/j.anireprosci.2006.01.014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Carreau S & Levallet J 2000 Testicular estrogens and male reproduction. News in Physiological Sciences 15 195198. (https://doi.org/10.1152/physiologyonline.2000.15.4.195)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cederroth CR, Zimmermann C, Beny JL, Schaad O, Combepine C, Descombes P, Doerge DR, Pralong FP, Vassalli JD & & Nef S 2010 Potential detrimental effects of a phytoestrogen-rich diet on male fertility in mice. Molecular and Cellular Endocrinology 321 152160. (https://doi.org/10.1016/j.mce.2010.02.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cemeli E, Schmid TE & Anderson D 2004 Modulation by flavonoids of DNA damage induced by estrogen-like compounds. Environmental and Molecular Mutagenesis 44 420426. (https://doi.org/10.1002/EM.20071)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chavarro JE, Toth TL, Sadio SM & Hauser R 2008 Soy food and isoflavone intake in relation to semen quality parameters among men from an infertility clinic. Human Reproduction 23 25842590. (https://doi.org/10.1093/humrep/den243)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Christensen RHB 2017. Ordinal–Regression Models for Ordinal Data.

  • Ded L, Dostalova P, Dorosh A, Dvorakova-Hortova K & & Peknicova J 2010 Effect of estrogens on boar sperm capacitation in vitro. Reproductive Biology and Endocrinology 8 87. (https://doi.org/10.1186/1477-7827-8-87)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dhamad AE, Zhou Z, Zhou J & Du Y 2016 Systematic proteomic identification of the heat shock proteins (Hsp) that interact with estrogen receptor alpha (ERα) and biochemical characterization of the ERα-Hsp70 interaction. PLoS One 11 e0160312. (https://doi.org/10.1371/JOURNAL.PONE.0160312)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Evans G & Maxwell WMC 1987 Salamons’ Artificial Insemination of Sheep and Goats, Salamons’ Artificial Insemination of Sheep and Goats. Sydney: Butterworths.

    • Search Google Scholar
    • Export Citation
  • Evenson D & Jost L 2000 Sperm chromatin structure assay is useful for fertility assessment. Methods in Cell Science 22 169189. (https://doi.org/10.1023/A:1009844109023)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Foster K, Ryan M & & Kidd D 2022 Oestrogenic subterranean Clover Guide - Identification and Remediation Series Number 1833-7236. Available at: https://library.dpird.wa.gov.au/bulletins/278/

    • Search Google Scholar
    • Export Citation
  • Francis CM & Millington AJ 1965 Varietal variation in the isoflavone content of subterranean clover: its estimation by a microtechnique. Australian Journal of Agricultural Research 16 557564. (https://doi.org/10.1071/AR9650557)

    • Search Google Scholar
    • Export Citation
  • Fraser LR, Beyret E, Milligan SR & Adeoya-Osiguwa SA 2006 Effects of estrogenic xenobiotics on human and mouse spermatozoa. Human Reproduction 21 11841193. (https://doi.org/10.1093/humrep/dei486)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gimeno-Martos S, González-Arto M, Casao A, Gallego M, Cebrián-Pérez JA, Muiño-Blanco T & Pérez-Pé R 2017 Steroid hormone receptors and direct effects of steroid hormones on ram spermatozoa. Reproduction 154 469481. (https://doi.org/10.1530/REP-17-0177)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hess RA 2003 Estrogen in the adult male reproductive tract: a review. Reproductive Biology and Endocrinology 1 114. (https://doi.org/10.1186/1477-7827-1-52/FIGURES/7)

    • Search Google Scholar
    • Export Citation
  • Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS & Lubahn DB 1997 A role for oestrogens in the male reproductive system. Nature 390 509512. (https://doi.org/10.1038/37352)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hochereau-De Reviers MT, Monet-Kuntz C & & Courot M 1987 Spermatogenesis and Sertoli cell numbers and function inn rams and bulls. Journal of Reproduction and Fertility 34 (Supplement)101114.

    • Search Google Scholar
    • Export Citation
  • Intasqui P, Camargo M, Antoniassi MP, Cedenho AP, Carvalho VM, Cardozo KHM, Zylbersztejn DS & Bertolla RP 2016 Association between the seminal plasma proteome and sperm functional traits. Fertility and Sterility 105 617628. (https://doi.org/10.1016/J.FERTNSTERT.2015.11.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jefferson WN, Patisaul HB & Williams CJ 2012 Reproductive consequences of developmental phytoestrogen exposure. Reproduction 143 247260. (https://doi.org/10.1530/REP-11-0369)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jin W, Arai KY, Watanabe G, Suzuki AK, Takahashi S & & Taya K 2005 The stimulatory role of estrogen on sperm motility in the male golden hamster (Mesocricetus auratus). Journal of Andrology 26 478484. (https://doi.org/10.2164/jandrol.04167)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kostelac D, Rechkemmer G & Briviba K 2003 Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. Journal of Agricultural and Food Chemistry 51 76327635. (https://doi.org/10.1021/JF034427B)

    • Search Google Scholar
    • Export Citation
  • Kuhnle GGC, Dell’Aquila C, Aspinall SM, Runswick SA, Mulligan AA & Bingham SA 2008 Phytoestrogen content of foods of animal origin: dairy products, eggs, meat, fish, and seafood. Journal of Agricultural and Food Chemistry 56 1009910104. (https://doi.org/10.1021/JF801344X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kuiper GGJM, Lemmen JG, Carlsson B, Corton JC, Safe SH, Van Der Saag PT, Van Der Burg B & Gustafsson JA 1998 Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139 42524263. (https://doi.org/10.1210/endo.139.10.6216)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kumar M, Sarma DK, Shubham S, Kumawat M, Verma V, Prakash A & Tiwari R 2020 Environmental endocrine-disrupting chemical exposure: role in non-communicable diseases. Frontiers in Public Health 8 549. (https://doi.org/10.3389/FPUBH.2020.553850/BIBTEX)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lamas-Toranzo I, Hamze JG, Bianchi E, Fernández-Fuertes B, Pérez-Cerezales S, Laguna-Barraza R, Fernández-González R, Lonergan P, Gutiérrez-Adán A & Wright GJ et al.2020 TMEM95 is a sperm membrane protein essential for mammalian fertilization. eLife 9 118. (https://doi.org/10.7554/eLife.53913)

    • Search Google Scholar
    • Export Citation
  • Levin ER 2009 Plasma membrane estrogen receptors. Trends in Endocrinology and Metabolism 20 477–482. (https://doi.org/10.1016/J.TEM.2009.06.009)

    • Search Google Scholar
    • Export Citation
  • Lightfoot RJ & Adams NR 1979 Changes in cervical histology in ewes following prolonged grazing on oestrogenic subterranean clover. Journal of Comparative Pathology 89 367373. (https://doi.org/10.1016/0021-9975(7990026-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Little DL & Frensham AB 1993 A rod-point technique for estimating botanical composition of pastures. Australian Journal of Experimental Agriculture 33 871875. (https://doi.org/10.1071/EA9930871)

    • Search Google Scholar
    • Export Citation
  • Lu R, Guo C, Tao XQ, Liu HY, Shi SS, Lin CY & Yao B 2011 Protective effect of annexin 5 on human sperm membrane and DNA integrity. Zhonghua Nan Ke Xue 17 1720.

  • Lundh TJO, Pettersson HI & Martinsson KA 1990 Comparative levels of free and conjugated plant estrogens in blood plasma of sheep and cattle fed estrogenic silage. Journal of Agricultural and Food Chemistry 38 15301534. (https://doi.org/10.1021/jf00097a022)

    • Search Google Scholar
    • Export Citation
  • Marshall T 1973 Clover Disease : What Do We Know and What Can We Do. Journal of the Department of Agriculture. Western Australia: Series, 4 14.

    • Search Google Scholar
    • Export Citation
  • Martin GB, Blache D, Miller DW & Vercoe PE 2010 Interactions between nutrition and reproduction in the management of the mature male ruminant. Animal 4 12141226. (https://doi.org/10.1017/S1751731109991674)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Menzel VA, Hinsch E, Hägele W & Hinsch KD 2007 Effect of genistein on acrosome reaction and zona pellucida binding independent of protein tyrosine kinase inhibition in bull. Asian Journal of Andrology 9 650658. (https://doi.org/10.1111/j.1745-7262.2007.00240.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mitchell JH, Cawood E, Kinniburgh D, Provan A, Collins AR & Irvine DS 2001 Effect of a phytoestrogen food supplement on reproductive health in normal males. Clinical Science 100 613618. (https://doi.org/10.1042/CS20000212)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mohamed el-SA, Park YJ, Song WH, Shin DH, You YA, Ryu BY & Pang MG 2011 Xenoestrogenic compounds promote capacitation and an acrosome reaction in porcine sperm. Theriogenology 75 11611169. (https://doi.org/10.1016/j.theriogenology.2010.11.028)

    • Search Google Scholar
    • Export Citation
  • Moutsatsou P 2007 The spectrum of phytoestrogens in nature: our knowledge is expanding. Hormones (Athens) 6 173193.

  • Mumford SL, Kim S, Chen Z, Boyd Barr D & Buck Louis GM 2015 Urinary phytoestrogens are associated with subtle indicators of semen quality among male partners of couples desiring pregnancy. Journal of Nutrition 145 25352541. (https://doi.org/10.3945/jn.115.214973)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Munuce MJ, Marini PE & Teijeiro JM 2019 Expression profile and distribution of annexin A1, A2 and A5 in human semen. Andrologia 51 e13224. (https://doi.org/10.1111/AND.13224)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nagata C, Inaba S, Kawakami N, Kakizoe T & Shimizu H 2000 Inverse association of soy product intake with serum androgen and estrogen concentrations in Japanese men. Nutrition and Cancer 36 1418. (https://doi.org/10.1207/S15327914NC3601_3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pasek RC, Malarkey E, Berbari NF, Sharma N, Kesterson RA, Tres LL, Kierszenbaum AL & Yoder BK 2016 Coiled-coil domain containing 42 (Ccdc42) is necessary for proper sperm development and male fertility in the mouse. Developmental Biology 412 208218. (https://doi.org/10.1016/J.YDBIO.2016.01.042)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pini T, Leahy T, Soleilhavoup C, Tsikis G, Labas V, Combes-Soia L, Harichaux G, Rickard JP, Druart X & de Graaf SP 2016 Proteomic investigation of ram spermatozoa and the proteins conferred by seminal plasma. Journal of Proteome Research 15 37003711. (https://doi.org/10.1021/acs.jproteome.6b00530)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pool KR, Chazal F, Smith JT & Blache D 2022 Estrogenic pastures: A source of endocrine disruption in sheep reproduction. Frontiers in Endocrinology (Lausanne) 0 712. (https://doi.org/10.3389/FENDO.2022.880861)

    • Search Google Scholar
    • Export Citation
  • Pool KR, Kent TC & Blache D 2021 Oestrogenic metabolite equol negatively impacts the functionality of ram spermatozoa in vitro. Theriogenology 172 216222. (https://doi.org/10.1016/j.theriogenology.2021.07.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pool KR, Rickard JP, Pini T & de Graaf SP 2020 Exogenous melatonin advances the ram breeding season and increases testicular function. Scientific Reports 10 9711. (https://doi.org/10.1038/s41598-020-66594-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Prossnitz ER & Arterburn JB 2015 International union of basic and Clinical Pharmacology. XCVII. G Protein-Coupled Estrogen Receptor and Its Pharmacologic Modulators. Pharmacological Reviews 67 505540. (https://doi.org/10.1124/PR.114.009712)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • R Core Team 2017. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/

    • Search Google Scholar
    • Export Citation
  • Rietjens IMCM, Louisse J & Beekmann K 2017 The potential health effects of dietary phytoestrogens. British Journal of Pharmacology 174 12631280. (https://doi.org/10.1111/bph.13622)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rochira V, Madeo B, Diazzi C, Zirilli L, Daniele S & & Carani C 2016 Estrogens and male reproduction . South Dartmouth, MA: Endotext.Available at : www.endotext.org

    • Search Google Scholar
    • Export Citation
  • Saunders PTK, Sharpe RM, Williams K, Macpherson S, Urquart H, Irvine DS & Millar MR 2001 Differential expression of oestrogen receptor α and β proteins in the testes and male reproductive system of human and non-human primates. Molecular Human Reproduction 7 227236. (https://doi.org/10.1093/molehr/7.3.227)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schiller V, Wichmann A, Kriehuber R, Schäfers C, Fischer R & Fenske M 2013 Transcriptome alterations in zebrafish embryos after exposure to environmental estrogens and anti-androgens can reveal endocrine disruption. Reproductive Toxicology 42 210223. (https://doi.org/10.1016/J.REPROTOX.2013.09.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T & Chang W 2022 David: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Research 50 W216W221. (https://doi.org/10.1093/NAR/GKAC194)

    • Search Google Scholar
    • Export Citation
  • Sierens J, Hartley JA, Campbell MJ, Leathem AJC & Woodside v. JV 2002 In vitro isoflavone supplementation reduces hydrogen peroxide-induced DNA damage in sperm. Teratogenesis, Carcinogenesis, and Mutagenesis 22 227234. (https://doi.org/10.1002/TCM.10015)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stern JE, Gardner S, Quirk D & Wira CR 1992 Secretory immune system of the male reproductive tract: effects of dihydrotestosterone and estradiol on IgA and secretory component levels. Journal of Reproductive Immunology 22 7385. (https://doi.org/10.1016/0165-0378(9290007-Q)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A & Tsafou KP et al.2015 STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Research 43 D447D452. (https://doi.org/10.1093/NAR/GKU1003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M & Cox J 2016 The Perseus computational platform for comprehensive analysis of (prote)omics data. Nature Methods 13 731740. (https://doi.org/10.1038/nmeth.3901)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van Tilburg M, Sousa S, Lobo MDP, Monteiro-Azevedo ACOM, Azevedo RA, Araújo AA & Moura AA 2021 Mapping the major proteome of reproductive fluids and sperm membranes of rams: from the cauda epididymis to ejaculation. Theriogenology 159 98107. (https://doi.org/10.1016/J.THERIOGENOLOGY.2020.10.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang X, Lin C, Zhao X, Liu A, Zhu J, Li X & Song L 2014 Acylglycerol kinase promotes cell proliferation and tumorigenicity in breast cancer via suppression of the FOXO1 transcription factor. Molecular Cancer 13 112. (https://doi.org/10.1186/1476-4598-13-106/FIGURES/6)

    • Search Google Scholar
    • Export Citation
  • Wira CR, Fahey v. JV, Sentman CL, Pioli PA & Shen L 2005 Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunological Reviews 206 306335. (https://doi.org/10.1111/J.0105-2896.2005.00287.X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yuan G, Liu Y, Liu G, Wei L, Wen Y, Huang S, Guo Y, Zou F & Cheng J 2019 Associations between semen phytoestrogens concentrations and semen quality in Chinese men. Environment International 129 136144. (https://doi.org/10.1016/j.envint.2019.04.076)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang Y, Liu C, Wu B, Li L, Li W & Yuan L 2021 The missing linker between SUN5 and PMFBP1 in sperm head-tail coupling apparatus. Nature Communications 12 4926. (https://doi.org/10.1038/S41467-021-25227-W)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zheng H, Stratton CJ, Morozumi K, Jin J, Yanagimachi R & Yan W 2007 Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility. Proceedings of the National Academy of Sciences of the United States of America 104 68526857. (https://doi.org/10.1073/pnas.0701669104)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhou Q, Nie R, Prins GS, Saunders PTK, Katzenellenbogen BS & Hess RA 2002 Localization of androgen and estrogen receptors in adult male mouse reproductive tract. Journal of Andrology 23 870881. (https://doi.org/10.1002/j.1939-4640.2002.tb02345.x)

    • PubMed
    • Search Google Scholar
    • Export Citation