Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Quercetin Affects Spermatogenesis-Related Genes of Mouse Exposed to High-Cholesterol Diet

  • Yang, Changwon (Institute of Animal Molecular Biotechnology and Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Bae, Hyocheol (Institute of Animal Molecular Biotechnology and Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Song, Gwonhwa (Institute of Animal Molecular Biotechnology and Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Lim, Whasun (Department of Food and Nutrition, College of Science and Technology, Kookmin University)
  • Received : 2020.03.03
  • Accepted : 2020.03.10
  • Published : 2020.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

A high-cholesterol diet can reduce male fertility. However, it is not known whether a high-cholesterol diet can regulate the expression of genes involved in sperm maturation and sperm fertilizing ability. Quercetin, a natural product, is known to have cytoprotective effects by regulating lipid metabolism in various cell types. This study aimed to confirm the expression of genes involved in sperm maturation in the testes of mice fed a high-cholesterol diet and to determine whether quercetin can reverse the genetic regulation of cholesterol. Mice were divided into groups fed a normal chow diet and a high-cholesterol diet. Mice fed the high-cholesterol diet were dose-dependently supplemented with quercetin for 6 weeks. Investigations using quantitative PCR and in situ hybridization revealed that the high-cholesterol diet alters the expression of genes associated with sperm maturation in the testes of mice, and this was reversed with the supplementation of quercetin. In addition, the high-cholesterol diet regulated the expression of genes related to lipid metabolism in the liver of mice. Under a high-cholesterol diet, quercetin can improve male fertility by regulating the expression of genes involved in sperm maturation.

Keywords

References

  1. Abdel Aziz RL, Abdel-Wahab A, Abo El-Ela FI, Hassan NEY, El-Nahass ES, Ibrahim MA, Khalil AAY. 2018. Dose- dependent ameliorative effects of quercetin and l-Carnitine against atrazine- induced reproductive toxicity in adult male Albino rats. Biomed. Pharmacother. 102:855-864. https://doi.org/10.1016/j.biopha.2018.03.136
  2. Brito AF, Ribeiro M, Abrantes AM, Pires AS, Teixo RJ, Tralhao JG, Botelho MF. 2015. Quercetin in cancer treatment, alone or in combination with conventional Therapeutics? Curr. Med. Chem. 22:3025-3039. https://doi.org/10.2174/0929867322666150812145435
  3. Carrasco-Pozo C, Tan KN, Reyes-Farias M, De La Jara N, Ngo ST, Garcia-Diaz DF, Llanos P, Cires MJ, Borges K. 2016. The deleterious effect of cholesterol and protection by quercetin on mitochondrial bioenergetics of pancreatic ${\beta}$-cells, glycemic control and inflammation: in vitro and in vivo studies. Redox Biol. 9:229-243. https://doi.org/10.1016/j.redox.2016.08.007
  4. Cavallini G. 2006. Male idiopathic oligoasthenoteratozoospermia. Asian J. Androl. 8:143-157. https://doi.org/10.1111/j.1745-7262.2006.00123.x
  5. Cho C, Bunch DO, Faure JE, Goulding EH, Eddy EM, Primakoff P, Myles DG. 1998. Fertilization defects in sperm from mice lacking fertilin beta. Science 281:1857-1859. https://doi.org/10.1126/science.281.5384.1857
  6. Damiano F, Giannotti L, Gnoni GV, Siculella L, Gnoni A. 2019. Quercetin inhibition of SREBPs and ChREBP expression results in reduced cholesterol and fatty acid synthesis in C6 glioma cells. Int. J. Biochem. Cell Biol. 117:105618. https://doi.org/10.1016/j.biocel.2019.105618
  7. Doege H, Baillie RA, Ortegon AM, Tsang B, Wu Q, Punreddy S, Hirsch D, Watson N, Gimeno RE, Stahl A. 2006. Targeted deletion of FATP5 reveals multiple functions in liver metabolism: alterations in hepatic lipid homeostasis. Gastroenterology 130:1245-1258. https://doi.org/10.1053/j.gastro.2006.02.006
  8. Edwards DR, Handsley MM, Pennington CJ. 2008. The ADAM metalloproteinases. Mol. Aspects Med. 29:258-289. https://doi.org/10.1016/j.mam.2008.08.001
  9. Goldstein JL, DeBose-Boyd RA, Brown MS. 2006. Protein sensors for membrane sterols. Cell 124:35-46. https://doi.org/10.1016/j.cell.2005.12.022
  10. Irvin MR, Aslibekyan S, Hidalgo B, Arnett D. 2014. CPT1A: the future of heart disease detection and personalized medicine? Clin. Lipidol. 9:9-12. https://doi.org/10.2217/clp.13.75
  11. Izawa H, Kohara M, Aizawa K, Suganuma H, Inakuma T, Watanabe G, Taya K, Sagai M. 2008. Alleviative effects of quercetin and onion on male reproductive toxicity induced by diesel exhaust particles. Biosci. Biotechnol. Biochem. 72:1235-1241. https://doi.org/10.1271/bbb.70705
  12. Jaiswal MK, Agrawal V, Katara GK, Pamarthy S, Kulshrestha A, Chaouat G, Gilman-Sachs A, Beaman KD. 2015. Male fertility and apoptosis in normal spermatogenesis are regulated by vacuolar-ATPase isoform a2. J. Reprod. Immunol. 112:38-45. https://doi.org/10.1016/j.jri.2015.07.003
  13. Kim E, Yamashita M, Nakanishi T, Park KE, Kimura M, Kashiwabara S, Baba T. 2006. Mouse sperm lacking ADAM1b/ ADAM2 fertilin can fuse with the egg plasma membrane and effect fertilization. J. Biol. Chem. 281:5634-5639. https://doi.org/10.1074/jbc.M510558200
  14. Kim T, Oh J, Woo JM, Choi E, Im SH, Yoo YJ, Kim DH, Nishimura H, Cho C. 2006. Expression and relationship of male reproductive ADAMs in mouse. Biol. Reprod. 74:744-750. https://doi.org/10.1095/biolreprod.105.048892
  15. Leisegang K, Udodong A, Bouic PJ, Henkel RR. 2014. Effect of the metabolic syndrome on male reproductive function: a case-controlled pilot study. Andrologia 46:167-176. https://doi.org/10.1111/and.12060
  16. Lim W, Bae H, Sohn JY, Jeong W, Kim SH, Song G. 2015. Dietary cholesterol affects expression of prostatic acid phosphatase in reproductive organs of male rats. Biochem. Biophys. Res. Commun. 456:421-427. https://doi.org/10.1016/j.bbrc.2014.11.100
  17. Lim W, Bae H, Song G. 2016. Differential expression of apolipoprotein D in male reproductive system of rats by high-fat diet. Andrology 4:1115-1122. https://doi.org/10.1111/andr.12250
  18. Liu Y, Liang C, Gao Y, Jiang S, He Y, Han Y, Olfati A, Manthari RK, Wang J, Zhang J. 2019. Fluoride interferes with the sperm fertilizing ability via downregulated SPAM1, ACR, and PRSS21 expression in rat epididymis. J. Agric. Food Chem. 67:5240-5249. https://doi.org/10.1021/acs.jafc.9b01114
  19. Lotti F, Corona G, Degli Innocenti S, Filimberti E, Scognamiglio V, Vignozzi L, Forti G, Maggi M. 2013. Seminal, ultrasound and psychobiological parameters correlate with metabolic syndrome in male members of infertile couples. Andrology 1:229-239. https://doi.org/10.1111/j.2047-2927.2012.00031.x
  20. Lu Y, Harada M, Kamijo Y, Nakajima T, Tanaka N, Sugiyama E, Kyogashima M, Gonzalez FJ, Aoyama T. 2019. Peroxisome proliferator-activated receptor ${\alpha}$ attenuates high-cholesterol diet-induced toxicity and pro-thrombotic effects in mice. Arch. Toxicol. 93:149-161. https://doi.org/10.1007/s00204-018-2335-4
  21. Majumdar SS and Bhattacharya I. 2013. Genomic and postgenomic leads toward regulation of spermatogenesis. Prog. Biophys. Mol. Biol. 113:409-422. https://doi.org/10.1016/j.pbiomolbio.2013.01.002
  22. Martin GG, Atshaves BP, McIntosh AL, Mackie JT, Kier AB, Schroeder F. 2006. Liver fatty acid binding protein gene ablation potentiates hepatic cholesterol accumulation in cholesterol-fed female mice. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G36-G48. https://doi.org/10.1152/ajpgi.00510.2004
  23. Martin-Deleon PA. 2011. Germ-cell hyaluronidases: their roles in sperm function. Int. J. Androl. 34(5 Pt 2):e306-e318. https://doi.org/10.1111/j.1365-2605.2010.01138.x
  24. Mbikay M, Mayne J, Sirois F, Fedoryak O, Raymond A, Noad J, Chretien M. 2018. Mice fed a high-cholesterol diet supplemented with quercetin-3-glucoside show attenuated hyperlipidemia and hyperinsulinemia associated with differential regulation of PCSK9 and LDLR in their liver and pancreas. Mol. Nutr. Food Res. 62:e1700729.
  25. Mi Y, Tu L, Wang H, Zeng W, Zhang C. 2013. Supplementation with quercetin attenuates 4-nitrophenol-induced testicular toxicity in adult male mice. Anat. Rec. (Hoboken) 296:1650-1657. https://doi.org/10.1002/ar.22765
  26. Nassir F, Wilson B, Han X, Gross RW, Abumrad NA. 2007. CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J. Biol. Chem. 282:19493-19501. https://doi.org/10.1074/jbc.M703330200
  27. Newberry EP, Xie Y, Kennedy S, Han X, Buhman KK, Luo J, Gross RW, Davidson NO. 2003. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 278:51664-51672. https://doi.org/10.1074/jbc.m309377200
  28. Saartok T, Dahlberg E, Gustafsson JA. 1984. Relative binding affinity of anabolic-androgenic steroids: comparison of the binding to the androgen receptors in skeletal muscle and in prostate, as well as to sex hormone-binding globulin. Endocrinology 114:2100-2106. https://doi.org/10.1210/endo-114-6-2100
  29. Saez Lancellotti TE, Boarelli PV, Monclus MA, Cabrillana ME, Clementi MA, Espinola LS, Cid Barria JL, Vincenti AE, Santi AG, Fornes MW. 2010. Hypercholesterolemia impaired sperm functionality in rabbits. PLoS One 5:e13457. https://doi.org/10.1371/journal.pone.0013457
  30. Samova S, Patel CN, Doctor H, Pandya HA, Verma RJ. 2018. The effect of bisphenol A on testicular steroidogenesis and its amelioration by quercetin: an in vivo and in silico approach. Toxicol. Res. (Camb) 7:22-31. https://doi.org/10.1039/C7TX00161D
  31. Schiza C, Korbakis D, Jarvi K, Diamandis EP, Drabovich AP. 2019. Identification of TEX101-associated proteins through proteomic measurement of human spermatozoa homozygous for the missense variant rs35033974. Mol. Cell. Proteomics 18:338-351. https://doi.org/10.1074/mcp.ra118.001170
  32. Sharma S, Ahmad S, Afjal MA, Habib H, Parvez S, Raisuddin S. 2019. Dichotomy of bisphenol A-induced expression of peroxisome proliferator-activated receptors in hepatic and testicular tissues in mice. Chemosphere 236:124264. https://doi.org/10.1016/j.chemosphere.2019.06.234
  33. Ujah GA, Nna VU, Agah MI, Omue LO, Leku CB, Osim EE. 2018. Effect of quercetin on cadmium chloride-induced impairments in sexual behaviour and steroidogenesis in male Wistar rats. Andrologia 50.
  34. Wang F, Chen Z, Ren X, Tian Y, Wang F, Liu C, Jin P, Li Z, Zhang F, Zhu B. 2017. Hormone-sensitive lipase deficiency alters gene expression and cholesterol content of mouse testis. Reproduction 153:175-185. https://doi.org/10.1530/REP-16-0484
  35. Wang HJ, Wang Q, Lv ZM, Wang CL, Li CP, Rong YL. 2015. Resveratrol appears to protect against oxidative stress and steroidogenesis collapse in mice fed high-calorie and highcholesterol diet. Andrologia 47:59-65. https://doi.org/10.1111/and.12231
  36. Wechsler A, Brafman A, Shafir M, Heverin M, Gottlieb H, Damari G, Gozlan-Kelner S, Spivak I, Moshkin O, Fridman E, Becker Y, Skaliter R, Einat P, Faerman A, Bjorkhem I, Feinstein E. 2003. Generation of viable cholesterol-free mice. Science 302:2087. https://doi.org/10.1126/science.1090776
  37. Woolveridge I, Bryden AA, Taylor MF, George NJ, Wu FC, Morris ID. 1998. Apoptosis and expression of apoptotic regulators in the human testis following short- and long-term antiandrogen treatment. Mol. Hum. Reprod. 4:701-707. https://doi.org/10.1093/molehr/4.7.701
  38. Yokoyama S. 2000. Release of cellular cholesterol: molecular mechanism for cholesterol homeostasis in cells and in the body. Biochim. Biophys. Acta 1529:231-244. https://doi.org/10.1016/S1388-1981(00)00152-9
  39. Zhang D, Tong X, VanDommelen K, Gupta N, Stamper K, Brady GF, Meng Z, Lin J, Rui L, Omary MB, Yin L. 2017. Lipogenic transcription factor ChREBP mediates fructose-induced metabolic adaptations to prevent hepatotoxicity. J. Clin. Invest. 127:2855-2867. https://doi.org/10.1172/JCI89934