Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of cholesterol and Lactobacillus acidophilus on testicular function

  • Ciftci, Gulay (Department of Biochemistry, Faculty of Veterinary Medicine, University of Ondokuz Mayis) ;
  • Tuna, Elif (Department of Biochemistry, Faculty of Veterinary Medicine, University of Ondokuz Mayis)
  • Received : 2020.12.12
  • Accepted : 2021.05.17
  • Published : 2021.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: In this study, the effects of Lactobacillus acidophilus on testosterone (TES), follicle-stimulating hormone (FSH), luteinizing hormone (LH), androgen-binding protein (ABP), factor-associated apoptosis (FAS), and total cholesterol (TC), as well as histopathological changes, were investigated in male rats fed a high-cholesterol diet. Methods: The study included three groups. The control (C) group was fed standard-diet for 8 weeks. The hypercholesterolemia (HC) group was fed a 2% cholesterol-diet for 8 weeks. The therapeutic group (HCL) was fed a 2% cholesterol-diet for 8 weeks and administered L. acidophilus for the last 4 weeks. FSH, TES, and FAS levels in testicular tissue were determined using an enzyme-linked immunosorbent assay (ELISA), while another sample was examined histopathologically. LH and ABP levels were determined using ELISA, and serum TC levels were assessed via an autoanalyzer. Results: In the HC group, the TC levels were significantly higher and the LH levels were lower (p<0.05) than in the C group. The ABP levels were lower (p>0.05). In the HCL group, the LH and ABP levels were higher (p>0.05) and the TC level significantly lower (p<0.05) than in the HC group. The TES and FSH levels were lower, and the FAS levels were higher, in the HC than in the C group (p<0.05). In the HCL group, levels of all three resembled control levels. Histologically, in the testicular tissue of the HC group, the cells in the tubular wall exhibited atrophy, vacuolization, and reduced wall structure integrity. However, in the HCL group, these deteriorations were largely reversed. Conclusion: Supplementary dietary administration of an L. acidophilus to hypercholesterolemic male rats positively impacted testicular tissue and male fertility hormone levels.

Keywords

Acknowledgement

This research was supported by the Scientific Research Projects Commission of Ondokuz Mayis University (Contract Grand No. PYO-VET.1904.16.019).

References

  1. Levitan I, Singh DK, Rosenhouse-Dantsker A. Cholesterol binding to ion channels. Front Physiol 2014;5:65. https://doi.org/10.3389/fphys.2014.00065
  2. Sulimovici S, Boyd GS. The effect of ascorbic acid in vitro on the rat ovarian cholesterol side chain cleavage enzyme system. Steroids 1968;12:127-49. https://doi.org/10.1016/S0039-128X(68)80085-6
  3. Chapman MJ, Le Goff W, Guerin M, Kontush A. Cholesteryl ester transfer protein: at the heart of the action of lipid-modulating therapy with statins, fibrates, niacin, and cholesteryl ester transfer protein inhibitors. Eur Heart J 2010;31:149-64. https://doi.org/10.1093/eurheartj/ehp399
  4. Ashrafi I, Kohram H, Ardabili FF. Antioxidative effects of melatonin on kinetics, microscopic and oxidative parameters of cryopreserved bull spermatozoa. Anim Reprod Sci 2013;139:25-30. https://doi.org/10.1016/j.anireprosci.2013.03.016
  5. Gupta RS, Dixit VP. Effect of dietary cholesterol on spermatogenesis. Z Ernahrungswiss 1988;27:236-43. https://doi.org/10.1007/BF02019512
  6. Rolfe RD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr 2000;130(2S Suppl):396S-402S. https://doi.org/10.1093/jn/130.2.396S
  7. De Boever P, Wouters R, Verschaeve L, Berckmans P, Schoeters G, Verstraete W. Protective effect of the bile salt hydrolase-active Lactobacillus reuteri against bile salt cytotoxicity. Appl Microbiol Biotechnol 2000;53:709-14. https://doi.org/10.1007/s002530000330
  8. Park SC, Hwang MH, Kim YH, Kim JC, Song JC, Lee KW, et al. Comparison of pH and bile resistance of Lactobacillus acidophilus strains isolated from rat, pig, chicken, and human sources. World J Microbiol Biotechnol 2006;22:35-7. https://doi.org/10.1007/s11274-005-4856-2
  9. Onody A, Csonka C, Giricz Z, Ferdinandy P. Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc Res 2003;58:663-70. https://doi.org/10.1016/S0008-6363(03)00330-4
  10. Wang L, Zhou B, Zhou X, Wang Y, Wang H, Jia S, et al. Combined lowering effects of rosuvastatin and L. acidophilus on cholesterol levels in rat. J Microbiol Biotechnol 2019;29:473-81. https://doi.org/10.4014/jmb.1806.06004
  11. Lim W, Bae H, Sohn JY, Jeong W, Kim SH, Song G. Dietary cholesterol affects expression of prostatic acid phosphatase in reproductive organs of male rats. Biochem Biophys Res Commun 2015;456:421-7. https://doi.org/10.1016/j.bbrc.2014.11.100
  12. Chen Z, Peng B, Wang S, Peng X. Rapid screening of highly efficient vaccine candidates by immunoproteomics. Proteomics 2004;4:3203-13. https://doi.org/10.1002/pmic.200300844
  13. Bashandy AE. Effect of fixed oil of nigella sativa on male fertility in normal and hyperlipidemic rats. Int J Pharmacol 2007;3:27-33. https://doi.org/10.3923/ijp.2007.27.33
  14. Prasad K, Kalra J. Experimental atherosclerosis and oxygen free radicals. Angiology 1989;40:835-43. https://doi.org/10.1177/000331978904000911
  15. Kailasapathy K, Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 2000;78:80-8. https://doi.org/10.1046/j.1440-1711.2000.00886.x
  16. Huang Y, Wang J, Cheng Y, Zheng Y. The hypocholesterolaemic effects of Lactobacillus acidophilus American type culture collection 4356 in rats are mediated by the down-regulation of Niemann-Pick C1-like 1. Br J Nutr 2010;104:807-12. https://doi.org/10.1017/S0007114510001285
  17. Tomaro-Duchesneau C, Saha S, Malhotra M, Jones ML, Labbe A, Rodes L, et al. Effect of orally administered L. fermentum NCIMB 5221 on markers of metabolic syndrome: an in vivo analysis using ZDF rats. Appl Microbiol Biotechnol 2014;98:115-26. https://doi.org/10.1007/s00253-013-5252-8
  18. Liu Y, Zhao F, Liu J, Wang H, Han X, Zhang Y, et al. Selection of cholesterol-lowering lactic acid bacteria and its effects on rats fed with high-cholesterol diet. Curr Microbiol 2017;74:623-31. https://doi.org/10.1007/s00284-017-1230-1
  19. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V, et al. Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci 2011;94:3288-94. https://doi.org/10.3168/jds.2010-4128
  20. Walker DK, Gilliland SE. Relationship among bile tolerance, bile salt deconjugation, and assimilation of cholesterol by Lactobacillus acidophilus. J Dairy Sci 1993;76:956-61. https://doi.org/10.3168/jds.S0022-0302(93)77422-6
  21. Dambekodi PC, Gilliland SE. Incorporation of cholesterol into the cellular membrane of Bifidobacterium longum. J Dairy Sci 1998;81:1818-24. https://doi.org/10.3168/jds.S0022-0302(98)75751-0
  22. Lye HS, Rahmat-Ali GR, Liong MT. Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int Dairy J 2010;20:169-75. https://doi.org/10.1016/j.idairyj.2009.10.003
  23. Zhang N, Zhang H, Zhang X, Zhang B, Wang F, Wang C, et al. The relationship between endogenous testosterone and lipid profile in middle-aged and elderly Chinese men. Eur J Endocrinol 2014;170:487-94. https://doi.org/10.1530/EJE-13-0802
  24. Lee CE, Kang JS, Kim KI. Effects of gender, gonadectomy and sex hormones on growth and plasma cholesterol level in rats. Ann Nutr Metab 2008;53:1-5. https://doi.org/10.1159/000152867
  25. Hatch NW, Srodulski SJ, Chan HW, Zhang X, Tannock LR, King VL. Endogenous androgen deficiency enhances diet-induced hypercholesterolemia and atherosclerosis in low-density lipoprotein receptor-deficient mice. Gend Med 2012;9:319-28. https://doi.org/10.1016/j.genm.2012.08.003
  26. Hardy MP, Gao HB, Dong Q, Ge R, Wang Q, Chai WR, et al. Stress hormone and male reproductive function. Cell Tissue Res 2005; 322:147-53. https://doi.org/10.1007/s00441-005-0006-2
  27. Poutahidis T, Springer A, Levkovich T, Qi P, Varian BJ, Lakritz JR, et al. Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS One 2014;9:e84877. https://doi.org/10.1371/journal.pone.0084877
  28. Ghoneim MA, Moselhy SS. Antioxidant status and hormonal profile reflected by experimental feeding of probiotics. Toxicol Ind Health 2016;32:741-50. https://doi.org/10.1177/0748233713506768
  29. Jones R, Mann T, Sherins R. Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril 1979;31:531-7. https://doi.org/10.1016/s0015-0282(16)43999-3
  30. Padron RS, Mas J, Zamora R, Riverol F, Licea M, Mallea L, et al. Lipids and testicular function. Int Urol Nephrol 1989;21:515-9. https://doi.org/10.1007/BF02549590
  31. Ramirez-Torres MA, Carrera A, Zambrana M. High incidence of hyperestrogenemia and dyslipidemia in a group of infertile men. Ginecol Obstet Mex 2000;68:224-9.
  32. Yamamoto Y, Shimamoto K, Sofikitis N, Miyagawa I. Effects of hypercholesterolaemia on Leydig and Sertoli cell secretory function and the overall sperm fertilizing capacity in the rabbit. Hum Reprod 1999;14:1516-21. https://doi.org/10.1093/humrep/14.6.1516
  33. Tanaka M, Nakaya S, Kumai T, Watanabe M, Matsumoto N, Kobayashi S. Impaired testicular function in rats with diet-induced hypercholesterolemia and/or streptozotocin-induced diabetes mellitus. Endocr Res 2001;27:109-17. https://doi.org/10.1081/ERC-100107174
  34. Shalaby MA, el-Zorba HY, Kamel GM. Effect of alpha-tocopherol and simvastatin on male fertility in hypercholesterolemic rats. Pharmacol Res 2004;50:137-42. https://doi.org/10.1016/j.phrs.2003.10.013
  35. Saez Lancellotti TE, Boarelli PV, Monclus MA, Cabrillana ME, Clementi MA, Espinola LS, et al. Hypercholesterolemia impaired sperm functionality in rabbits. PLoS One 2010;5:e13457. https://doi.org/10.1371/journal.pone.0013457
  36. Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, et al. Selenium-enriched probiotics improves murine male fertility compromised by high fat diet. Biol Trace Elem Res 2012;147:251-60. https://doi.org/10.1007/s12011-011-9308-2
  37. Bataineh HN, Nusier MK. Effect of cholesterol diet on reproductive function in male albino rats. Saudi Med J 2005;26:398-404.
  38. Kangasniemi M, Kaipia A, Toppari J, Perheentupa A, Huhtaniemi I, Parvinen M. Cellular regulation of follicle-stimulating hormone (FSH) binding in rat seminiferous tubules. J Androl 1990;11:336-43.
  39. Sluka P, O'Donnell L, Bartles JR, Stanton PG. FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo. J Endocrinol 2006;189:381-95. https://doi.org/10.1677/joe.1.06634
  40. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, De Kretser DM, Pratis K, et al. Hormonal regulation of spermatogenesis in primates and man: insights for development of the male hormonal contraceptive. J Androl 2002;23:149-62.
  41. Hammond GL, Underhill DA, Rykse HM, Smith CL. The human sex hormone-binding globulin gene contains exons for androgen-binding protein and two other testicular messenger RNAs. Mol Endocrinol 1989;3:1869-76. https://doi.org/10.1210/mend-3-11-1869
  42. Dardmeh F, Alipour H, Gazerani P, van der Horst G, Brandsborg E, Nielsen HI. Lactobacillus rhamnosus PB01 (DSM 14870) supplementation affects markers of sperm kinematic parameters in a diet-induced obesity mice model. PLoS One 2017;12:e0185964. https://doi.org/10.1371/journal.pone.0185964
  43. Zarei A, Ashtiyani SC, Vaezi GH. A study on the effects of the hydroalcholic extract of the aerial parts of Alhagi camelorum on prolactin and pituitary-gonadal activity in rats with hypercholesterolemia. Arch Ital Urol Androl 2014;86:188-92. https://doi.org/10.4081/aiua.2014.3.188
  44. Alzubaidi NA, Al Diwan MA. The effect of taurine on reproductive efficiency in male rats fed high cholesterol diet. Basrah J Vet Res 2013;12:30-40. https://doi.org/10.33762/bvetr.2013.76186
  45. Zhang K, Lv Z, Jia X, Huang D. Melatonin prevents testicular damage in hyperlipidaemic mice. Andrologia 2012;44:230-6. https://doi.org/10.1111/j.1439-0272.2012.01272.x
  46. Fang X, Xu QY, Jia C, Peng YF. Metformin improves epididymal sperm quality and antioxidant function of the testis in diet-induced obesity rats. Zhonghua Nan Ke Xue 2012;18:146-9.