[en] Taxifolin (TAX), as a natural flavonoid, has been widely focused on due to its strong anti-oxidation, anti-inflammation, anti-virus, and even anti-tumor activity. However, the effect of TAX on semen quality was unknown. The purpose of this study was to analyze the beneficial influences of adding feed additive TAX to boar semen in terms of its quality and potential mechanisms. We discovered that TAX increased sperm motility significantly in Duroc boars by the elevation of the protein levels such as ZAG, PKA, CatSper, and p-ERK for sperm quality. TAX increased the blood concentration of testosterone derivatives, antioxidants such as melatonin and betaine, unsaturated fatty acids such as DHA, and beneficial amino acids such as proline. Conversely, TAX decreased 10 different kinds of bile acids in the plasma. Moreover, TAX increased "beneficial" microbes such as Intestinimonas, Coprococcus, Butyrivibrio, and Clostridium_XlVa at the Genus level. However, TAX reduced the "harmful" intestinal bacteria such as Prevotella, Howardella, Mogibacterium, and Enterococcus. There was a very close correlation between fecal microbes, plasma metabolites, and semen parameters by the spearman correlation analysis. Therefore, the data suggest that TAX increases the semen quality of Duroc boars by benefiting the gut microbes and blood metabolites. It is supposed that TAX could be used as a kind of feed additive to increase the semen quality of boars to enhance production performance.
Disciplines :
Agriculture & agronomy
Author, co-author :
Zhou, Yexun ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Chen, Liang; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Han, Hui ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Xiong, Bohui; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Jiang, Yue; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Lei; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Sun, Haiqing; YangXiang Joint Stock Company, Guigang, China
Tan, Jiajian; YangXiang Joint Stock Company, Guigang, China
Cheng, Xiaowei; Yinuo Biopharmaceutical Co., Ltd, Harbin, China
We thank the Beijing Genomics Institute (BGI) and Shanghai LUMING Biotechnology CO., LCD for technical support.This research was supported by funding from China Academy of Agriculture Sciences, the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202006-02, ASTIPIAS07), and the State Key Laboratory of Animal Nutrition (2004DA125184G2102).
Afouda P. Durand G. A. Lagier J. C. Labas N. Cadoret F. Armstrong N. et al. (2019). Noncontiguous finished genome sequence and description of Intestinimonas massiliensis sp. nov strain GD2T, the second Intestinimonas species cultured from the human gut. Microbiology 8:e00621. doi: 10.1002/mbo3.621
Al-Asmakh M. Stukenborg J. B. Reda A. Anuar F. Strand M. L. Hedin L. et al. (2014). The gut microbiota and developmental programming of the testis in mice. PLoS One 9:103809. doi: 10.1371/journal.pone.0103809
Baptissart M. Vega A. Martinot E. Pommier A. J. Houten S. M. Marceau G. et al. (2014). Bile acids alter male fertility through G-protein-coupled bile acid receptor 1 signaling pathways in mice. Hepatology 60, 1054–1065. doi: 10.1002/hep.27204, PMID: 24798773
Baro Graf C. Ritagliati C. Stival C. Luque G. M. Gentile I. Buffone M. G. et al. (2020). Everything you ever wanted to know about PKA regulation and its involvement in mammalian sperm capacitation. Mol. Cell. Endocrinol. 518:110992. doi: 10.1016/j.mce.2020.110992, PMID: 32853743
Bomzon A. Holt S. Moore K. (1997). Bile acids, oxidative stress, and renal function in biliary obstruction. Semin. Nephrol. 17, 549–562.
Bucak M. N. Keskin N. Ili P. Bodu M. Akalın P. P. Öztürk A. E. et al. (2020). Decreasing glycerol content by co-supplementation of trehalose and taxifolin hydrate in ram semen extender: microscopic, oxidative stress, and gene expression analyses. Cryobiology 96, 19–29. doi: 10.1016/j.cryobiol.2020.09.001, PMID: 32890464
Bunay J. Gallardo L. M. Torres-Fuentes J. L. Aguirre-Arias M. V. Orellana R. Sepúlveda N. et al. (2021). A decrease of docosahexaenoic acid in testes of mice fed a high-fat diet is associated with impaired sperm acrosome reaction and fertility. Asian J. Androl. 23, 306–313. doi: 10.4103/aja.aja_76_20, PMID: 33269725
Centola G. M. Blanchard A. Demick J. Li S. Eisenberg M. L. (2016). Decline in sperm count and motility in young adult men from 2003 to 2013: observations from a U.S sperm bank. Andrology 4, 270–276. doi: 10.1111/andr.12149, PMID: 26789272
Checa Vizcaíno M. A. González-Comadran M. Jacquemin B. (2016). Outdoor air pollution and human infertility: a systematic review. Fertil. Steril. 106, 897–904.e1. doi: 10.1016/j.fertnstert.2016.07.1110, PMID: 27513553
Chen X. Huang J. Hu Z. Zhang Q. Li X. Huang D. (2017). Protective effects of dihydroquercetin on an APAP-induced acute liver injury mouse model. Int. J. Clin. Exp. Pathol. 10, 10223–10232.
Chi H. Chun K. Son H. Kim J. Kim G. Roh S. (2013). Effect of genistein administration on the recovery of spermatogenesis in the busulfan-treated rat testis. Clin. Exp. Reprod. Med. 40, 60–66. doi: 10.5653/cerm.2013.40.2.60, PMID: 23875161
Dai Z. Wu Z. Hang S. Zhu W. Wu G. (2015). Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction. Mol. Hum. Reprod. 21, 389–409. doi: 10.1093/molehr/gav003, PMID: 25609213
Dawra V. Yadav B. Yadav S. (2015). Effect of glutamine supplementation and replacement of tris-egg yolk based extender with defatted cow milk on spermatozoa quality after equilibration and thawing. Vet. World. 8, 1027–1031. doi: 10.14202/vetworld.2015.1027-1031, PMID: 27047193
Ding N. Zhang X. Zhang X. D. Jing J. Liu S. S. Mu Y. P. et al. (2020). Impairment of spermatogenesis and sperm motility by the high-fat diet-induced dysbiosis of gut microbes. Gut 69, 2259–2260. doi: 10.1136/gutjnl-2020-321220, PMID: 32276951
Dong H. Wu D. Xu S. Li Q. Fang Z. Che L. et al. (2016). Effect of dietary supplementation with amino acids on boar sperm quality and fertility. Anim. Reprod. Sci. 172, 182–189. doi: 10.1016/j.anireprosci.2016.08.003, PMID: 27509874
Duracka M. Lukac N. Kacaniova M. Kantor A. Hleba L. Ondruska L. et al. (2019). Antibiotics versus natural biomolecules: the case of in vitro induced bacteriospermia by enterococcus Faecalis in rabbit semen. Molecules 24:4329. doi: 10.3390/molecules24234329, PMID: 31783504
Elsheikh N. A. H. Omer N. A. Yi-Ru W. Mei-Qian K. Ilyas A. Abdurahim Y. et al. (2020). Protective effect of betaine against lead-induced testicular toxicity in male mice. Andrologia 52:13600. doi: 10.1111/and.13600
Farahani L. Tharakan T. Yap T. Ramsay J. W. Jayasena C. N. Minhas S. (2021). The semen microbiome and its impact on sperm function and male fertility. Andrology 9, 115–144. doi: 10.1111/andr.12886, PMID: 32794312
Fukui Y. (1960). Studies on the chemical constituents of the plants of coniferae and allied orders. XL. Yakugaku zasshi 80, 752–756. doi: 10.1248/yakushi1947.80.6_752
Galochkina A. V. Anikin V. B. Babkin V. A. Ostrouhova L. A. Zarubaev V. V. (2016b). Virus-inhibiting activity of dihydroquercetin, a flavonoid from Larix sibirica, against coxsackievirus B4 in a model of viral pancreatitis. Arch. Virol. 164, 929–938. doi: 10.1007/s00705-016-2749-3
Galochkina A. V. Zarubaev V. Kiselev O. Babkin V. Ostroukhova L. (2016a). Antiviral activity of the dihydroquercetin during the Coxsackievirus b4 replication in vitro. Vopr. Virusol. 61, 27–31. doi: 10.18821/0507-4088-2016-61-1-27-31
Ganjalikhan Hakemi S. Sharififar F. Haghpanah T. Babaee A. Eftekhar-Vaghefi S. H. (2019). The effects of olive leaf extract on the testis, sperm quality and testicular germ cell apoptosis in male rats exposed to busulfan. Int. J. Fertil. Steril. 13, 57–65. doi: 10.22074/ijfs.2019.5520, PMID: 30644246
Guo L. Wu Y. Wang C. Wei H. Tan J. Sun H. et al. (2020). Gut microbiological disorders reduce semen utilization rate in duroc boars. Front. Microbiol. 11:581926. doi: 10.3389/fmicb.2020.581926, PMID: 33133051
Guo H. Zhang X. Cui Y. Zhou H. Xu D. Shan T. et al. (2015). Taxifolin protects against cardiac hypertrophy and fibrosis during biomechanical stress of pressure overload. Toxicol. Appl. Pharmacol. 287, 168–177. doi: 10.1016/j.taap.2015.06.002, PMID: 26051872
Gustiene S. Zaborskiene G. Rokaityte A. Riešute R. (2019). Effect of biofermentation with taxifolin on physicochemical and microbiological parameters of cold-smoked pork sausages. Food Technol. Biotechnol. 57, 481–489. doi: 10.17113/ftb.57.04.19.6250, PMID: 32123510
Hale B. J. Fernandez R. F. Kim S. Q. Diaz V. D. Jackson S. N. Liu L. et al. (2019). Acyl-CoA synthetase 6 enriches seminiferous tubules with the ω-3 fatty acid docosahexaenoic acid and is required for male fertility in the mouse. J. Biol. Chem. 294, 14394–14405. doi: 10.1074/jbc.RA119.009972, PMID: 31399511
Han X. Zhang P. Shen W. Zhao Y. Zhang H. (2019). Estrogen receptor-related DNA and histone methylation may be involved in the transgenerational disruption in spermatogenesis by selective toxic chemicals. Front. Pharmacol. 10:1012. doi: 10.3389/fphar.2019.01012, PMID: 31572187
Han H. Zhong R. Zhou Y. Xiong B. Chen L. Jiang Y. et al. (2021). Hydroxytyrosol benefits boar semen quality via improving gut microbiota and blood Metabolome. Front. Nutr. 8:815922. doi: 10.3389/fnut.2021.815922
Hou J. Hu M. Zhang L. Gao Y. Ma L. Xu Q. (2021). Dietary Taxifolin protects against dextran sulfate sodium-induced colitis via NF-κB signaling, enhancing intestinal barrier and modulating gut microbiota. Front. Immunol. 11:631809. doi: 10.3389/fimmu.2020.631809, PMID: 33664740
Impellizzeri D. Talero E. Siracusa R. Alcaide A. Cordaro M. Maria Zubelia J. et al. (2015). Protective effect of polyphenols in an inflammatory process associated with experimental pulmonary fibrosis in mice. Br. J. Nutr. 114, 853–865. doi: 10.1017/S0007114515002597, PMID: 26334388
Ince S. Ozer M. Kadioglu B. G. Kuzucu M. Ozkaraca M. Gezer A. et al. (2020). The effect of taxifolin on oxidative ovarian damage and reproductive dysfunctions induced by antipsychotic drugs in female rats. J. Obstet. Gynaecol. Res. 47, 2140–2148. doi: 10.1111/jog.14769
Jomová K. Hudecova L. Lauro P. Simunkova M. Alwasel S. H. Alhazza I. M. et al. (2019). A switch between antioxidant and prooxidant properties of the phenolic compounds yyricetin, morin, 3′,4′-dihydroxyflavone, taxifolin and 4-hydroxy-coumarin in the presence of copper (II) ions: a spectroscopic, absorption titration and DNA damage study. Molecules 24:4335. doi: 10.3390/molecules24234335, PMID: 31783535
Jung S. Kim H. Lee B. Choi S. Kim H. Choi Y. et al. (2015). Effects of Korean red ginseng extract on busulfan-induced dysfunction of the male reproductive system. J. Ginseng Res. 39, 243–249. doi: 10.1016/j.jgr.2015.01.002, PMID: 26199556
Keshavarzian A. Green S. J. Engen P. A. Voigt R. M. Naqib A. Forsyth C. B. et al. (2015). Colonic bacterial composition in Parkinson's disease. Mov. Disord. 30, 1351–1360. doi: 10.1002/mds.26307, PMID: 26179554
Leisegang K. Sengupta P. Agarwal A. Henkel R. (2021). Obesity and male infertility: mechanisms and management. Andrologia 53:e13617. doi: 10.1111/and.13617, PMID: 32399992
Lektemur Alpan A. Kızıldağ A. Özdede M. Karakan N. C. Özmen Ö. (2020). The effects of taxifolin on alveolar bone in experimental periodontitis in rats. Arch. Oral Biol. 117:104823. doi: 10.1016/j.archoralbio.2020.104823, PMID: 32593876
Levine H. Jørgensen N. Martino-Andrade A. Mendiola J. Weksler-Derri D. Mindlis I. et al. (2017). Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum. Reprod. Update 23, 646–659. doi: 10.1093/humupd/dmx022, PMID: 28981654
Li J. Mao R. Zhou Q. Ding L. Tao J. Ran M. M. et al. (2016). Exposure to bisphenol a (BPA) in Wistar rats reduces sperm quality with disruption of ERK signal pathway. Toxicol. Mech. Methods 26, 180–188. doi: 10.3109/15376516.2016.1139024
Li Q. Pu Y. Lu H. Zhao N. Wang Y. Guo Y. et al. (2020). Porphyromonas, Treponema, and Mogibacterium promote IL8/IFNγ/TNFα-based pro-inflammation in patients with medication-related osteonecrosis of the jaw. J. Oral Microbiol. 13:1851112. doi: 10.1080/20002297.2020.1851112, PMID: 33391627
Li X. Xie H. Jiang Q. Wei G. Lin L. Li C. et al. (2017). The mechanism of (+) taxifolin's protective antioxidant effect for OH-treated bone marrow-derived mesenchymal stem cells. Cell. Mol. Biol. Lett. 22:31. doi: 10.1186/s11658-017-0066-9, PMID: 29299033
Li Z. Yu Y. Li Y. Ma F. Fang Y. Ni C. et al. (2020). Taxifolin attenuates the developmental testicular toxicity induced by di-n-butyl phthalate in fetal male rats. Food Chem. Toxicol. 142:111482. doi: 10.1016/j.fct.2020.111482, PMID: 32525071
Lishko P. V. Kirichok Y. Ren D. Navarro B. Chung J. J. Clapham D. E. (2012). The control of male fertility by spermatozoan ion channels. Annu. Rev. Physiol. 74, 453–475. doi: 10.1146/annurev-physiol-020911-153258, PMID: 22017176
Liu X. Liu W. Ding C. Zhao Y. Chen X. Ling D. et al. (2021a). Taxifolin, extracted from waste larix olgensis roots, attenuates CCl4-induced liver fibrosis by regulating the PI3K/AKT/mTOR and TGF-β1/Smads signaling pathways. Drug Des. Devel. Ther. 15, 871–887. doi: 10.2147/DDDT.S281369, PMID: 33664566
Liu Y. Qu F. Cao X. Chen G. Guo Q. Ying X. et al. (2012). Con A-binding protein Zn-2-glycoprotein on human sperm membrane is related to acrosome reaction and sperm fertility. Int. J. Androl. 35, 145–157. doi: 10.1111/j.1365-2605.2011.01195.x, PMID: 21790656
Liu X. Zhao Y. Zhu H. Wu M. Zheng Y. Yang M. et al. (2021b). Taxifolin retards the D-galactose-induced aging process through inhibiting Nrf2-mediated oxidative stress and regulating the gut microbiota in mice. Food Funct. 10:1039. doi: 10.1039/d1fo01349a
Louis G. F. Lewis A. J. Weldon W. C. Miller P. S. Kittok R. J. Stroup W. W. (1994). The effect of protein intake on boar libido, semen characteristics, and plasma hormone concentrations. J. Anim. Sci. 72, 2038–2050. doi: 10.2527/1994.7282038x, PMID: 7982833
Ma D. Han P. Song M. Zhang H. Shen W. Huang G. et al. (2021). β-carotene rescues busulfan disrupted spermatogenesis through elevation in testicular antioxidant capability. Front. Pharmacol. 12:593953. doi: 10.3389/fphar.2021.593953, PMID: 33658940
Malivindi R. Santoro M. De Rose D. Panza S. Gervasi S. Rago V. et al. (2018). Activated-farnesoid X receptor (FXR) expressed in human sperm alters its fertilising ability. Reproduction 156, 249–259. doi: 10.1530/REP-18-0203
Moon C. D. Pacheco D. M. Kelly W. J. Leahy S. C. Li D. Kopecny J. et al. (2008). Reclassification of clostridium proteoclasticum as Butyrivibrio proteoclasticus comb. nov., a butyrate-producing ruminal bacterium. Int. J. Syst. Evol. Microbiol. 58, 2041–2045. doi: 10.1099/ijs.0.65845-0, PMID: 18768601
Nekrasov R. V. Bogolyubova N. V. Semenova A. A. Nasonova V. V. Polishchuk E. K. (2021). Dihydroquercetin influence on clinical and biochemical blood parameters of pigs under conditions of stress load. Vopr. Pitan. 90, 74–84. doi: 10.33029/0042-8833-2021-90-1-74-84, PMID: 33740330
Olia Bagheri F. Alizadeh A. Sadighi Gilani M. A. Shahhoseini M. (2021). Role of peroxisome proliferator-activated receptor gamma (PPARγ) in the regulation of fatty acid metabolism related gene expressions in testis of men with impaired spermatogenesis. Reprod. Biol. 21:100543. doi: 10.1016/j.repbio.2021.100543, PMID: 34492575
O'Shea C. J. Doyle D. N. Heim G. O'Doherty J. (2015). Effect of maternal dietary supplementation of laminarin and fucoidan, independently or in combination, on pig growth performance and aspects of intestinal health. J. Ani. Feed Sci. 204, 28–41. doi: 10.1016/j.anifeedsci.2015.02.007
Pang J. Zhou Q. Sun X. Li L. Zhou B. Zeng F. et al. (2017). Effect of low-dose zearalenone exposure on reproductive capacity of male mice. Toxicol. Appl. Pharmacol. 333, 60–67. doi: 10.1016/j.taap.2017.08.011, PMID: 28837831
Qu F. Ying X. Guo W. Guo Q. Chen G. Liu Y. et al. (2007). The role of Zn-alpha2 glycoprotein in sperm motility is mediated by changes in cyclic AMP. Reproduction 134, 569–576. doi: 10.1530/REP-07-0145, PMID: 17890292
Rato L. Alves M. G. Socorro S. Duarte A. I. Cavaco J. E. Oliveira P. F. (2012). Metabolic regulation is important for spermatogenesis. Nat. Rev. Urol. 9, 330–338. doi: 10.1038/nrurol.2012.77
Razak S. Afsar T. Ullah A. Almajwal A. Alkholief M. Alshamsan A. et al. (2018). Taxifolin, a natural flavonoid interacts with cell cycle regulators causes cell cycle arrest and causes tumor regression by activating Wnt/β-catenin signaling pathway. BMC Cancer 18:1043. doi: 10.1186/s12885-018-4959-4, PMID: 30367624
Sanjo H. Yao T. Katagiri K. Sato T. Matsumura T. Komeya M. et al. (2020). Antioxidant vitamins and lysophospholipids are critical for inducing mouse spermatogenesis under organ culture conditions. FASEB J. 37, 9480–9487. doi: 10.1096/fj.202000245R
Singh M. Talimoa Mollier R. Sharma P. R. Kadirvel G. Doley S. Sanjukta R. K. et al. (2021). Dietary flaxseed oil improve boar semen quality, antioxidant status and in-vivo fertility in humid sub-tropical region of North East India. Theriogenology 159, 123–131. doi: 10.1016/j.theriogenology.2020.10.023, PMID: 33137633
Skakkebaek N. E. Rajpert-De Meyts E. Louis G. M. B. Toppari J. Andersson A. M. Eisenberg M. L. et al. (2016). Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol. Rev. 96, 55–97. doi: 10.1152/physrev.00017.2015, PMID: 26582516
Smith L. B. Walker W. H. (2014). The regulation of spermatogenesis by androgens. Semin. Cell Dev. Biol. 30, 2–13. doi: 10.1016/j.semcdb.2014.02.012, PMID: 24598768
Su H. Wang W. J. Zheng G. D. Yin Z. P. Li J. E. Chen L. L. et al. (2022). The anti-obesity and gut microbiota modulating effects of taxifolin in C57BL/6J mice fed with a high-fat diet. J. Sci. Food Agric. 102, 1598–1608. doi: 10.1002/jsfa.11496
Sun S. Meng Q. Bai Y. Cao C. Li J. Cheng B. et al. (2021). Lycopene improves maternal reproductive performance by modulating milk composition and placental antioxidative and immune status. Food Funct. 10:1039. doi: 10.1039/d1fo01595h
Topal F. Nar M. Gocer H. Kalin P. Kocyigit U. M. Gülçin İ. et al. (2016). Antioxidant activity of taxifolin: an activity-structure relationship. J. Enzyme Inhib. Med. Chem. 31, 674–683. doi: 10.3109/14756366.2015.1057723, PMID: 26147349
Turck D. Castenmiller J. De Henauw S. Hirsch-Ernst K. I. Kearney J. Maciuk A. et al. (2020). Safety of hot water extract of fruits and peduncles of Hovenia dulcis as a novel food pursuant to Regulation 1(EU) 2015/2283. EFSA J. 18:6196. doi: 10.2903/j.efsa.2020.6196
Vakalopoulos I. Dimou P. Anagnostou I. Zeginiadou T. (2015). Impact of cancer and cancer treatment on male fertility. Hormones (Athens) 14, 579–589. doi: 10.14310/horm.2002.1620
Virtanen H. E. Jørgensen N. Toppari J. (2017). Semen quality in the 21st century. Nat. Rev. Urol. 14, 120–130. doi: 10.1038/nrurol.2016.261, PMID: 28050014
Wan F. Zhong R. Wang M. Zhou Y. Chen Y. Yi B. et al. (2021). Caffeic acid supplement alleviates colonic inflammation and oxidative stress potentially through improved gut microbiota community in mice. Front. Microbiol. 12:784211. doi: 10.3389/fmicb.2021.784211, PMID: 34867926
Wang M. Liu X. Chang G. Chen Y. An G. Yan L. et al. (2018). Single-cell RNA sequencing analysis reveals sequential cell fate transition during human spermatogenesis. Cell Stem Cell 23, 599–614.e4. doi: 10.1016/j.stem.2018.08.007, PMID: 30174296
WHO. WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th Edn. Cambridge: Cambridge University Press (2010).
Wu Y. Chi X. Zhang Q. Chen F. Deng X. (2018). Characterization of the salivary microbiome in people with obesity. PeerJ 6:e4458. doi: 10.7717/peerj.4458, PMID: 29576948
Wu Y. Lai W. Liu Z. Wei H. Zhou Y. Tan J. et al. (2019). Serum and seminal plasma element concentrations in relation to semen quality in Duroc boars. Biol. Trace Elem. Res. 189, 85–94. doi: 10.1007/s12011-018-1459-y, PMID: 30069693
Xu Y. Fan Y. Fan W. Jing J. Xue K. Zhang X. et al. (2018). RNASET2 impairs the sperm motility via PKA/PI3K/calcium signal pathways. Reproduction 155, 383–392. doi: 10.1530/REP-17-0746, PMID: 29581387
Xu D. Liu L. Zhao Y. Yang L. Cheng J. Hua R. et al. (2020). Melatonin protects mouse testes from palmitic acid-induced lipotoxicity by attenuating oxidative stress and DNA damage in a SIRT1-dependent manner. J. Pineal Res. 69:12690. doi: 10.1111/jpi.12690
Yu S. Zhao Y. Zhang F. L. Li Y. Q. Shen W. Sun Z. Y. (2020). Chestnut polysaccharides benefit spermatogenesis through improvement in the expression of important genes. Aging (Albany NY) 12, 11431–11445. doi: 10.18632/aging.103205, PMID: 32568099
Zhang P. Feng Y. Li L. Ge W. Yu S. Hao Y. et al. (2021). Improvement in sperm quality and spermatogenesis following faecal microbiota transplantation from alginate oligosaccharide dosed mice. Gut 70, 222–225. doi: 10.1136/gutjnl-2020-320992, PMID: 32303608
Zhang X. Li D. Dong C. Shi J. Sun Y. Ye B. et al. (2020). Molybdenum sulfide-based electrochemical platform for high sensitive detection of taxifolin in Chinese medicine. Anal. Chim. Acta 1099, 85–93. doi: 10.1016/j.aca.2019.11.057, PMID: 31986281
Zhang P. Liu J. Xiong B. Zhang C. Kang B. Gao Y. et al. (2020). Microbiota from alginate oligosaccharide dosed mice successfully mitigated small intestinal mucositis. Microbiome 8:112. doi: 10.1186/s40168-020-00886-x, PMID: 32711581
Zhang C. Xiong B. Chen L. Ge W. Yin S. Feng Y. et al. (2021). Rescue of male fertility following faecal microbiota transplantation from alginate oligosaccharide-dosed mice. Gut 70, 2213–2215. doi: 10.1136/gutjnl-2020-323593, PMID: 33443023
Zhang W. Zhao Y. Zhang P. Hao Y. Yu S. Min L. et al. (2018). Decrease in male mouse fertility by hydrogen sulfide and/or ammonia can be inheritable. Chemosphere 194, 147–157. doi: 10.1016/j.chemosphere.2017.11.164, PMID: 29202267
Zhang P. Zhao Y. Zhang H. Liu J. Feng Y. Yin S. et al. (2019). Low dose chlorothalonil impairs mouse spermatogenesis through the intertwining of estrogen receptor pathways with histone and DNA methylation. Chemosphere 230, 384–395. doi: 10.1016/j.chemosphere.2019.05.029, PMID: 31112861
Zhao Y. Zhang P. Ge W. Feng Y. Li L. Sun Z. et al. (2020). Alginate oligosaccharides improve germ cell development and testicular microenvironment to rescue busulfan disrupted spermatogenesis. Theranostics 10, 3308–3324. doi: 10.7150/thno.43189, PMID: 32194870
Zhao Y. Zhang W. D. Liu X. Q. Zhang P. F. Hao Y. N. Li L. et al. (2016). Hydrogen sulfide and/or ammonia reduces spermatozoa motility through AMPK/AKT related pathways. Sci. Rep. 6:37884. doi: 10.1038/srep37884, PMID: 27883089
Zhou Q. Wang M. Yuan Y. Wang X. Fu R. Wan H. et al. (2016). Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 18, 330–340. doi: 10.1016/j.stem.2016.01.017, PMID: 26923202
Zhu W. Su Z. Xu W. Sun H. X. Gao J. F. Tu D. F. et al. (2021). Garlic skin induces shifts in the rumen microbiome and metabolome of fattening lambs. Animal 15:100216. doi: 10.1016/j.animal.2021.100216, PMID: 34051409
