nach oben

International Urology and Nephrology

Erschienen in:

16.06.2017 | Urology - Original Paper

Ameliorative effect of omega-3 on spermatogenesis, testicular antioxidant status and preimplantation embryo development in streptozotocin-induced diabetes in rats

verfasst von: Mehdi Khavarimehr, Vahid Nejati, Mazdak Razi, Gholamreza Najafi

Erschienen in: International Urology and Nephrology | Ausgabe 9/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

The present study was done to determine the ameliorative effect of polyunsaturated fatty acid omega-3 against experimental diabetes-induced damages on testicular tissue, sperm parameters and preimplantation embryo development in rat model.

Methods

Thirty-two mature male rats were divided into two control and test groups. The experimental diabetes (50 mg kg⁻¹ streptozotocin, ip) was induced in test group and subdivided into non-treated diabetic, 300 and 600 mg kg⁻¹ omega-3-treated (orally by gavage) groups. The rats in control group received 0.5 ml saline using intra-gastric gavage. Following 45 days, general histopathological changes, serum level of testosterone, inhibin B, glucose, and sperm parameters, testicular total antioxidant capacity (TAC) and malondialdehyde (MDA) content were analyzed. The mitochondria-dependent apoptosis was investigated by assessing the Bcl-2 and caspase-3 expression as well as DNA fragmentation. Finally, the in vitro fertilization (IVF) potential was examined by evaluating preimplantation embryo developing.

Results

The omega-3 significantly ameliorated the diabetes-induced histological damages, diminished serum level of glucose, testicular MDA content, and enhanced the serum testosterone, inhibin B and testicular TAC. The animals in omega-3-treated groups exhibited a significant (p < 0.05) up-regulation in Bcl-2, as well as remarkable (p < 0.05) down-regulation in caspase-3 expression compared to non-treated diabetic rats. Moreover, the omega-3 maintained DNA integrity, improved sperm quality as well as preimplantation embryo development.

Conclusion

Our data showed that the omega-3 (especially at 600 mg kg⁻¹ dose level) effectively ameliorates the experimental diabetes-induced infertility in rats by up-regulating the testicular endocrine and antioxidant statuses, preventing mitochondria-dependent apoptosis pathway and potentially improving the sperm quality.

Nathan DM (1993) Long-term complications of diabetes mellitus. N Engl J Med 328(23):1676–1685CrossRefPubMed

Fujii J, Iuchi Y, Matsuki S, Ishii T (2003) Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues. Asian J Androl 5(3):231–242PubMed

Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52(1):102–110CrossRefPubMed

Eizirik DL, Colli ML, Ortis F (2009) The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 5(4):219–226CrossRefPubMed

Rother KI (2007) Diabetes treatment-bridging the divide. N Engl J Med 356(15):1499–1501CrossRefPubMedPubMedCentral

Scarano WR, Messias AG, Oliva SU, Klinefelter GR, Kempinas WG (2006) Sexual behaviour, sperm quantity and quality after short-term streptozotocin-induced hyperglycaemia in rats. Int J Androl 29:482–488CrossRefPubMed

Armagan A, Uz E, Yilmaz HR, Soyupek S, Oksay T, Ozcelik N (2006) Effects of melatonin on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat testis. Asian J Androl 8:595–600CrossRefPubMed

Karaca T, Demirtas S, Karaboga I, Ayvazz S (2015) Protective effects of royal jelly against testicular damage in streptozotocin-induced diabetic rats. Turk J Med Sci 45(1):27–32CrossRefPubMed

Chandel A, Dhindsa S, Topiwala S, Chaudhuri A, Dandona P (2008) Testosterone concentration in young patients with diabetes. Diabetes Care 31(10):2013–2017CrossRefPubMedPubMedCentral

10.

Jiang X, Zhang C, Xin Y, Huang Z, Tan Y, Huang Y, Wang Y, Feng W, Li X, Li W, Qu Y, Cai L (2013) Protective effect of FGF21 on type 1 diabetes-induced testicular apoptotic cell death probably via both mitochondrial- and endoplasmic reticulum stress-dependent pathways in the mouse model. Toxicol Lett 219(1):65–76CrossRefPubMed

11.

Kam PC, Ferch NI (2000) Apoptosis: mechanisms and clinical implications. Anaesthesia 55(11):1081–1093CrossRefPubMed

12.

Hotchkiss RS, Strasser A, McDunn JE, Swanson PE (2009) Cell death. N Engl J Med 361(16):1570–1583CrossRefPubMedPubMedCentral

13.

D’Emilio A, Biagiotti L, Burattini S, Battistelli M, Canonico B, Evangelisti C, Ferri P, Papa S, Martelli AM, Falcieri E (2010) Morphological and biochemical patterns in skeletal muscle apoptosis. Histol Histopathol 25(1):21–32PubMed

14.

Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87(7):1157–1180CrossRefPubMed

15.

Shukla KK, Mahdi AA, Rajender S (2012) Apoptosis, spermatogenesis and male infertility. Front Biosci (Elite Ed) 4:746–754CrossRef

16.

Vujkovic M, de Vries JH, Dohle GR, Bonsel GJ, Lindemans J, Macklon NS, van der Spek PJ, Steegers EA, Steegers-Theunissen RP (2009) Associations between dietary patterns and semen quality in men undergoing IVF/ICSI treatment. Hum Reprod 24(6):1304–1312CrossRefPubMed

17.

Mendiola J, Torres-Cantero AM, Vioque J, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, Bernabeu R (2010) A low intake of antioxidant nutrients is associated with poor semen quality in patients attending fertility clinics. Fertil Steril 93(4):1128–1133CrossRefPubMed

18.

Mazza M, Pomponi M, Janiri L, Bria P, Mazza S (2007) Omega-3 fatty acids and antioxidants in neurological and psychiatric diseases: an overview. Prog Neuropsychopharmacol Biol Psychiatry 31(1):12–26. doi:10.1016/j.pnpbp.2006.07.010 CrossRefPubMed

19.

Roqueta-Rivera M, Stroud CK, Haschek WM, Akare SJ, Segre M, Brush RS, Agbaga MP, Anderson RE, Hess RA, Nakamura MT (2010) Docosahexaenoic acid supplementation fully restores fertility and spermatogenesis in male delta-6 desaturase-null mice. J Lipid Res 51(2):360–367. doi:10.1194/jlr.M001180 CrossRefPubMedPubMedCentral

20.

Lenzi A, Gandini L, Maresca V, Rago R, Sgro P, Dondero F, Picardo M (2000) Fatty acid composition of spermatozoa and immature germ cells. Mol Hum Reprod 6(3):226–231CrossRefPubMed

21.

Rejraji H, Sion B, Prensier G, Carreras M, Motta C, Frenoux JM, Vericel E, Grizard G, Vernet P, Drevet JR (2006) Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod 74(6):1104–1113CrossRefPubMed

22.

Kesavulu MM, Kameswararao B, Apparao C, Kumar EG, Harinarayan CV (2002) Effect of omega-3 fatty acids on lipid peroxidation and antioxidant enzyme status in type 2 diabetic patients. Diabetes Metab 28(1):20–26PubMed

23.

Tabei SM, Fakher S, Djalali M, Javanbakht MH, Zarei M, Derakhshanian H, Sadeghi MR, Mostafavi E, Kargar F (2015) Effect of vitamins A, E, C and omega-3 fatty acids supplementation on the level of catalase and superoxide dismutase activities in streptozotocin-induced diabetic rats. Bratisl Lek Listy 116(2):115–118PubMed

24.

Ganong WF (1967) Neuroendocrinology, vol 2. Academic Press, New York

25.

Yan L, Bai XL, Fang ZF, Che LQ, Xu SY, Wu D (2013) Effect of different dietary omega-3/omega-6 fatty acid ratios on reproduction in male rats. Lipids Health Dis 12:33. doi:10.1186/1476-511x-12-33 CrossRefPubMedPubMedCentral

26.

Uygur R, Aktas C, Tulubas F, Uygur E, Kanter M, Erboga M, Caglar V, Topcu B, Ozen OA (2014) Protective effects of fish omega-3 fatty acids on doxorubicin-induced testicular apoptosis and oxidative damage in rats. Andrologia 46(8):917–926. doi:10.1111/and.12173 CrossRefPubMed

27.

Khosravanian N, Razi M, Farokhi F, Khosravanian H (2014) Testosterone and vitamin E administration up-regulated varicocele-reduced Hsp70-2 protein expression and ameliorated biochemical alterations. J Assist Reprod Genet 31:341–354CrossRefPubMedPubMedCentral

28.

Kermer P, Klocker N, Labes M, Thomsen S, Srinivasan A, Bahr M (1999) Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett 453(3):361–364CrossRefPubMed

29.

Soleimani Asl S, Farhadi MH, Moosavizadeh K, Samadi Kuchak Saraei A, Soleimani M, Jamei SB, Joghataei MT, Samzadeh-Kermani A, Hashemi-Nasl H, Mehdizadeh M (2012) Evaluation of Bcl-2 family gene expression in hippocampus of 3, 4-methylenedioxymethamphetamine treated rats. Cell J 13(4):275–280PubMed

30.

Pant N, Srivastava SP (2003) Testicular and spermatotoxic effects of quinalphos in rats. J Appl Toxicol 23:271–274CrossRefPubMed

31.

Niehaus WG, Samuelsson B (1968) Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 6:126–130CrossRefPubMed

32.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMed

33.

Gholirad S, Razi M, Hassani Bafrani H (2016) Tracing of zinc and iron in experimentally induced varicocele: correlation with oxidative, nitrosative and carbonyl stress. Andrologia. doi:10.1111/and.12687 PubMed

34.

Razi M, Sadrkhanloo RA, Malekinejad H, Sarafzadeh-Rezaei F (2011) Varicocele time-dependently affects DNA integrity of sperm cells: evidence for lower in vitro fertilization rate in varicocele-positive rats. Int J Fertil Steril 5(3):174–185PubMedPubMedCentral

35.

Zambrano E, Rodriguez-Gonzalez GL, Guzman C, Garcia-Becerra R, Boeck L, Diaz L, Menjivar M, Larrea F, Nathanielsz PW (2005) A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol 563(Pt 1):275–284. doi:10.1113/jphysiol.2004.078543 CrossRefPubMed

36.

Auger J, Mesbah M, Huber C, Dadoune JP (1990) Aniline blue staining as a marker of sperm chromatin defects associated with different semen characteristics discriminates between proven fertile and suspected infertile men. Int J Androl 13(6):452–462CrossRefPubMed

37.

Ballester J, Munoz MC, Dominguez J, Rigau T, Guinovart JJ, Rodriguez-Gil JE (2004) Insulin-dependent diabetes affects testicular function by FSH- and LH-linked mechanisms. J Androl 25(5):706–719CrossRefPubMed

38.

Navarro-Casado L, Juncos-Tobarra MA, Chafer-Rudilla M, de Onzono LI, Blazquez-Cabrera JA, Miralles-Garcia JM (2010) Effect of experimental diabetes and STZ on male fertility capacity. Study in rats. J Androl 31(6):584–592. doi:10.2164/jandrol.108.007260 CrossRefPubMed

39.

Kanter M, Aktas C, Erboga M (2012) Protective effects of quercetin against apoptosis and oxidative stress in streptozotocin-induced diabetic rat testis. Food Chem Toxicol 50(3–4):719–725. doi:10.1016/j.fct.2011.11.051 CrossRefPubMed

40.

Smith LB, Walker WH (2014) The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 30:2–13CrossRefPubMed

41.

Walker WH, Cheng J (2005) FSH and testosterone signaling in Sertoli cells. Reproduction 130(1):15–28. doi:10.1530/rep.1.00358 CrossRefPubMed

42.

Fix C, Jordan C, Cano P, Walker WH (2004) Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells. PNAS 101(30):10919–10924CrossRefPubMedPubMedCentral

43.

Holdcraft RW, Braun RE (2004) Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development 131(2):459–467. doi:10.1242/dev.00957 CrossRefPubMed

44.

Pierik FH, Vreeburg JT, Stijnen T, De Jong FH, Weber RF (1998) Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab 83(9):3110–3114. doi:10.1210/jcem.83.9.5121 CrossRefPubMed

45.

O’Connor AE, De Kretser DM (2004) Inhibins in normal male physiology. Semin Reprod Med 22(3):177–185. doi:10.1055/s-2004-831893 CrossRefPubMed

46.

Suresh Y, Das UN (2003) Long-chain polyunsaturated fatty acids and chemically induced diabetes mellitus. Effect of omega-3 fatty acids. Nutrition 19(3):213–228CrossRefPubMed

47.

Altinkilic S, Naziroglu M, Uguz AC, Ozcankaya R (2010) Fish oil and antipsychotic drug risperidone modulate oxidative stress in PC12 cell membranes through regulation of cytosolic calcium ion release and antioxidant system. J Membr Biol 235(3):211–218. doi:10.1007/s00232-010-9267-0 CrossRefPubMed

48.

Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183. doi:10.1146/annurev.pharmtox.47.120505.105122 CrossRefPubMed

49.

Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84. doi:10.1016/j.biocel.2006.07.001 CrossRefPubMed

50.

Circu ML, Moyer MP, Harrison L, Aw TY (2009) Contribution of glutathione status to oxidant-induced mitochondrial DNA damage in colonic epithelial cells. Free Radic Biol Med 47(8):1190–1198. doi:10.1016/j.freeradbiomed.2009.07.032 CrossRefPubMedPubMedCentral

51.

Rachek LI, Yuzefovych LV, Ledoux SP, Julie NL, Wilson GL (2009) Troglitazone, but not rosiglitazone, damages mitochondrial DNA and induces mitochondrial dysfunction and cell death in human hepatocytes. Toxicol Appl Pharmacol 240(3):348–354. doi:10.1016/j.taap.2009.07.021 CrossRefPubMedPubMedCentral

52.

Hagenbuchner J, Kuznetsov A, Hermann M, Hausott B, Obexer P, Ausserlechner MJ (2012) FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J Cell Sci 125(Pt 5):1191–1203. doi:10.1242/jcs.092098 CrossRefPubMed

53.

McIlwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5(4):a008656. doi:10.1101/cshperspect.a008656 CrossRefPubMedPubMedCentral

54.

Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. doi:10.1080/01926230701320337 CrossRefPubMedPubMedCentral

55.

Marsden VS, O’Connor L, O’Reilly LA, Silke J, Metcalf D, Ekert PG, Huang DC, Cecconi F, Kuida K, Tomaselli KJ, Roy S, Nicholson DW, Vaux DL, Bouillet P, Adams JM, Strasser A (2002) Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature 419(6907):634–637. doi:10.1038/nature01101 CrossRefPubMed

56.

Youle Richard J, Strasser Andreas (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59CrossRefPubMed

57.

French DB, Sabanegh ES Jr, Goldfarb J, Desai N (2010) Does severe teratozoospermia affect blastocyst formation, live birth rate, and other clinical outcome parameters in ICSI cycles? Fertil Steril 93(4):1097–1103. doi:10.1016/j.fertnstert.2008.10.051 CrossRefPubMed

58.

Ghirelli-Filho M, Mizrahi FE, Pompeo AC, Glina S (2012) Influence of strict sperm morphology on the results of classic in vitro fertilization. Int Braz J Urol 38(4):519–528CrossRefPubMed

59.

Agarwal A, Hamada A, Esteves SC (2012) Insight into oxidative stress in varicocele-associated male infertility: part 1. Nat Rev Urol 9:678–690CrossRefPubMed

60.

Pacey AA (2006) Is quality assurance in semen analysis still really necessary? A view from the andrology laboratory. Hum Reprod 21(5):1105–1109. doi:10.1093/humrep/dei460 CrossRefPubMed

61.

Nikbakht R, Saharkhiz N (2011) The influence of sperm morphology, total motile sperm count of semen and the number of motile sperm inseminated in sperm samples on the success of intrauterine insemination. Int J Fertil Steril 5(3):168–173PubMedPubMedCentral

62.

Tavalaee M, Razavi S, Nasr-Esfahani MH (2007) Effects of sperm acrosomal integrity and protamine deficiency on in vitro fertilization and pregnancy rate. IJFS 1(1):27–34

63.

Tarozzi N, Bizzaro D, Flamigni C, Borini A (2007) Clinical relevance of sperm DNA damage in assisted reproduction. Reprod Biomed Online 14(6):746–757CrossRefPubMed

Titel: Ameliorative effect of omega-3 on spermatogenesis, testicular antioxidant status and preimplantation embryo development in streptozotocin-induced diabetes in rats
verfasst von: Mehdi Khavarimehr
Vahid Nejati
Mazdak Razi
Gholamreza Najafi
Publikationsdatum: 16.06.2017
Verlag: Springer Netherlands
Erschienen in: International Urology and Nephrology / Ausgabe 9/2017
Print ISSN: 0301-1623
Elektronische ISSN: 1573-2584
DOI: https://doi.org/10.1007/s11255-017-1636-5

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

18.04.2024 | Wirbelsäulenmetastase | Nachrichten

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Ameliorative effect of omega-3 on spermatogenesis, testicular antioxidant status and preimplantation embryo development in streptozotocin-induced diabetes in rats

Abstract

Purpose

Methods

Results

Conclusion

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Stereotaktische Radiatio schlägt konventionelle Bestrahlung

Denken Sie bei starker Blutung auch an die Hemmkörper-Hämophilie

Adjuvante Brustkrebstherapie: Doppelt hält besser

Delir kann Demenz begünstigen

Update Innere Medizin

Springer Medizin

Abstract

Purpose

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 9/2017

Ultrasonic evaluation of renal cortex arterial area enables differentiation between hypertensive and glomerulonephritis-related chronic kidney disease

Dietary and commercialized fructose: Sweet or sour?

Low vascularization of the nephrogenic zone of the fetal kidney suggests a major role for hypoxia in human nephrogenesis

The prognostic significance of preoperatively assessed AST/ALT (De Ritis) ratio on survival in patients underwent radical cystectomy

Effects of long-term treatment with haloperidol, clozapine and aripiprazole on mice isolated vas deferens

From novice to expert: analyzing the learning curve for MRI-transrectal ultrasonography fusion-guided transrectal prostate biopsy

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Stereotaktische Radiatio schlägt konventionelle Bestrahlung

Denken Sie bei starker Blutung auch an die Hemmkörper-Hämophilie

Adjuvante Brustkrebstherapie: Doppelt hält besser

Delir kann Demenz begünstigen

Update Innere Medizin