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Dietary supplementation with astaxanthin may ameliorate sperm parameters and DNA integrity in streptozotocin-induced diabetic rats

  • Bahmanzadeh, Maryam (Endometrium and Endometriosis Research Center, Hamadan University of Medical Sciences) ;
  • Vahidinia, Aliasghar (Nutrition Health research center, Hamadan University of Medical Sciences) ;
  • Mehdinejadiani, Shayesteh (Department of Anatomy, School of Medicine, Tehran University of Medical Sciences) ;
  • Shokri, Saeed (Department of Anatomical Sciences, School of Medicine, Zanjan University of Medical Sciences) ;
  • Alizadeh, Zohreh (Endometrium and Endometriosis Research Center, Hamadan University of Medical Sciences)
  • Received : 2016.01.05
  • Accepted : 2016.04.14
  • Published : 2016.06.23

Abstract

Objective: Diabetes mellitus (DM) is known to cause many systemic complications as well as male infertility. Astaxanthin (ASTX) is a powerful antioxidant that is involved in a variety of biologically active processes, including those with anti-diabetes effects. The present study investigates the effect of ASTX on the spermatozoa function in streptozotocin (STZ)-induced diabetic rats. Methods: We divided 30 adult rats into three groups (10 rats per group), with a control group that received corn oil mixed with chow. DM was induced by intra-peritoneal injection of STZ. Eight weeks after the STZ injection, half of the diabetic animals were used as diabetic controls, and the rest were treated with ASTX for 56 days. Then the parameters and chromatin integrity of the epididymal sperm were analyzed using chromomycin A3, toluidine blue (TB), and acridine orange (AO) staining. Results: The count, viability, and motility of the epididymal sperm were decreased significantly in the STZ group in comparison with the control group (count and viability, p<0.001; motility, p<0.01). ASTX increased normal morphology and viable spermatozoa compared to the STZ group (morphology, p=0.001; viability, p<0.05). The percentage of abnormal chromatins in TB and AO staining was higher in the STZ group compared to the control group (p<0.001). The mean percentage of TB and AO positive spermatozoa in STZ rats was significantly lower in the STZ+ASTX group (TB, p=0.001; AO, p<0.05). Conclusion: This study observed that in vivo ASTX treatment partially attenuates some detrimental effect of diabetes. Conversely, ASTX improved sperm viability, normal morphology, and DNA integrity.

Keywords

References

  1. Ugarte M, Brown M, Hollywood KA, Cooper GJ, Bishop PN, Dunn WB. Metabolomic analysis of rat serum in streptozotocin-induced diabetes and after treatment with oral triethylenetetramine (TETA). Genome Med 2012;4:35. https://doi.org/10.1186/gm334
  2. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047-53. https://doi.org/10.2337/diacare.27.5.1047
  3. La Vignera S, Condorelli R, Vicari E, D’Agata R, Calogero AE. Diabetes mellitus and sperm parameters. J Androl 2012;33:145-53. https://doi.org/10.2164/jandrol.111.013193
  4. Mallidis C, Czerwiec A, Filippi S, O’Neill J, Maggi M, McClure N. Spermatogenic and sperm quality differences in an experimental model of metabolic syndrome and hypogonadal hypogonadism. Reproduction 2011;142:63-71. https://doi.org/10.1530/REP-10-0472
  5. Sexton WJ, Jarow JP. Effect of diabetes mellitus upon male reproductive function. Urology 1997;49:508-13. https://doi.org/10.1016/S0090-4295(96)00573-0
  6. Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc Diabetol 2005;4:5. https://doi.org/10.1186/1475-2840-4-5
  7. Agarwal A. Role of oxidative stress in male infertility and antioxidant supplementation [Internet]. Cleveland: American Center for Reproductive Medicine; 2005 [cited 2016 May 16]. Available from: https://www.clevelandclinic.org/reproductiveresearchcenter/docs/agradoc174.pdf.
  8. Evans MD, Dizdaroglu M, Cooke MS. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 2004;567:1-61. https://doi.org/10.1016/j.mrrev.2003.11.001
  9. Agbaje IM, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, et al. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod 2007;22:1871-7. https://doi.org/10.1093/humrep/dem077
  10. Mangoli E, Talebi AR, Anvari M, Pourentezari M. Effects of experimentally-induced diabetes on sperm parameters and chromatin quality in mice. Iran J Reprod Med 2013;11:53-60.
  11. Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol 2006;250:66-9. https://doi.org/10.1016/j.mce.2005.12.026
  12. Lewis SE. Is sperm evaluation useful in predicting human fertility? Reproduction 2007;134:31-40. https://doi.org/10.1530/REP-07-0152
  13. Sadi G, Eryilmaz N, Tutuncuoglu E, Cingir S, Guray T. Changes in expression profiles of antioxidant enzymes in diabetic rat kidneys. Diabetes Metab Res Rev 2012;28:228-35. https://doi.org/10.1002/dmrr.1302
  14. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Lund DD, Yorek MA. Effect of antioxidant treatment of streptozotocin-induced diabetic rats on endoneurial blood flow, motor nerve conduction velocity, and vascular reactivity of epineurial arterioles of the sciatic nerve. Diabetes 2001;50:1927-37. https://doi.org/10.2337/diabetes.50.8.1927
  15. Sadi G, Yilmaz O, Guray T. Effect of vitamin C and lipoic acid on streptozotocin-induced diabetes gene expression: mRNA and protein expressions of Cu-Zn SOD and catalase. Mol Cell Biochem 2008;309:109-16. https://doi.org/10.1007/s11010-007-9648-6
  16. Hughes CM, Lewis SE, McKelvey-Martin VJ, Thompson W. The effects of antioxidant supplementation during Percoll preparation on human sperm DNA integrity. Hum Reprod 1998;13:1240-7. https://doi.org/10.1093/humrep/13.5.1240
  17. Comhaire FH, El Garem Y, Mahmoud A, Eertmans F, Schoonjans F. Combined conventional/antioxidant “Astaxanthin” treatment for male infertility: a double blind, randomized trial. Asian J Androl 2005;7:257-62. https://doi.org/10.1111/j.1745-7262.2005.00047.x
  18. Ikeuchi M, Koyama T, Takahashi J, Yazawa K. Effects of astaxanthin in obese mice fed a high-fat diet. Biosci Biotechnol Biochem 2007;71:893-9. https://doi.org/10.1271/bbb.60521
  19. Naguib YM. Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 2000;48:1150-4. https://doi.org/10.1021/jf991106k
  20. Naito Y, Uchiyama K, Aoi W, Hasegawa G, Nakamura N, Yoshida N, et al. Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors 2004;20:49-59. https://doi.org/10.1002/biof.5520200105
  21. Shrilatha B, Muralidhara. Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences. Reprod Toxicol 2007;23:578-87. https://doi.org/10.1016/j.reprotox.2007.02.001
  22. Abeeleh MA, Ismail ZB, Alzaben KR, Abu-Halaweh SA, Al-Essa MK, Abuabeeleh J, et al. Induction of diabetes mellitus in rats using intraperitoneal streptozotocin: a comparison between 2 strains of rats. Eur J Sci Res 2009;32:398-402.
  23. Soudamani S, Yuvaraj S, Malini T, Balasubramanian K. Experimental diabetes has adverse effects on the differentiation of ventral prostate during sexual maturation of rats. Anat Rec A Discov Mol Cell Evol Biol 2005;287:1281-9.
  24. Yuan JP, Peng J, Yin K, Wang JH. Potential health-promoting effects of astaxanthin: a high-value carotenoid mostly from microalgae. Mol Nutr Food Res 2011;55:150-65. https://doi.org/10.1002/mnfr.201000414
  25. Hussein G, Sankawa U, Goto H, Matsumoto K, Watanabe H. Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod 2006;69:443-9. https://doi.org/10.1021/np050354+
  26. Rosiepen G, Weinbauer GF, Schlatt S, Behre HM, Nieschlag E. Duration of the cycle of the seminiferous epithelium, estimated by the 5-bromodeoxyuridine technique, in laboratory and feral rats. J Reprod Fertil 1994;100:299-306. https://doi.org/10.1530/jrf.0.1000299
  27. Yama OE, Duru FI. Temporal adaptation in the testes of rat administered single dose Momordica charantia for three interrupted spermatogenic cycles: cytometric quantification. Middle East Fertil Soc J 2011;16:194-9. https://doi.org/10.1016/j.mefs.2011.07.001
  28. Frode TS, Medeiros YS. Animal models to test drugs with potential antidiabetic activity. J Ethnopharmacol 2008;115:173-83. https://doi.org/10.1016/j.jep.2007.10.038
  29. Bahmanzadeh M, Abolhassani F, Amidi F, Ejtemaiemehr Sh, Salehi M, Abbasi M. The effects of nitric oxide synthase inhibitor (L-NAME) on epididymal sperm count, motility, and morphology in varicocelized rat. Daru 2008;16:23-8.
  30. Shokri S, Hemadi M, Bayat G, Bahmanzadeh M, Jafari-Anarkooli I, Mashkani B. Combination of running exercise and high dose of anabolic androgenic steroid, nandrolone decanoate, increases protamine deficiency and DNA damage in rat spermatozoa. Andrologia 2014;46:184-90. https://doi.org/10.1111/and.12061
  31. Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, et al. Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report. ILSI Risk Science Institute Expert Working Group on Sperm Evaluation. Reprod Toxicol 1996;10:237-44. https://doi.org/10.1016/0890-6238(96)00028-7
  32. Nasr-Esfahani MH, Razavi S, Mardani M. Relation between different human sperm nuclear maturity tests and in vitro fertilization. J Assist Reprod Genet 2001;18:219-25.
  33. Erenpreiss J, Jepson K, Giwercman A, Tsarev I, Erenpreisa J, Spano M. Toluidine blue cytometry test for sperm DNA conformation: comparison with the flow cytometric sperm chromatin structure and TUNEL assays. Hum Reprod 2004;19:2277-82. https://doi.org/10.1093/humrep/deh417
  34. Sadeghi MR, Lakpour N, Heidari-Vala H, Hodjat M, Amirjannati N, Hossaini Jadda H, et al. Relationship between sperm chromatin status and ICSI outcome in men with obstructive azoospermia and unexplained infertile normozoospermia. Rom J Morphol Embryol 2011;52:645-51.
  35. Jee BC, Suh CS, Shin MS, Lee HJ, Lee JH, Kim SH. Sperm nuclear DNA fragmentation and chromatin structure in one-day-old ejaculated sperm. Clin Exp Reprod Med 2011;38:82-6. https://doi.org/10.5653/cerm.2011.38.2.82
  36. La Vignera S, Vicari E, Condorelli R, D'Agata R, Calogero AE. Ultrasound characterization of the seminal vesicles in infertile patients with type 2 diabetes mellitus. Eur J Radiol 2011;80:e64-7. https://doi.org/10.1016/j.ejrad.2010.08.001
  37. Ding GL, Liu Y, Liu ME, Pan JX, Guo MX, Sheng JZ, et al. The effects of diabetes on male fertility and epigenetic regulation during spermatogenesis. Asian J Androl 2015;17:948-53. https://doi.org/10.4103/1008-682X.150844
  38. Jangir RN, Jain GC. Diabetes mellitus induced impairment of male reproductive functions: a review. Curr Diabetes Rev 2014;10:147-57. https://doi.org/10.2174/1573399810666140606111745
  39. Karimi J, Goodarzi MT, Tavilani H, Khodadadi I, Amiri I. Increased receptor for advanced glycation end products in spermatozoa of diabetic men and its association with sperm nuclear DNA fragmentation. Andrologia 2012;44 Suppl 1:280-6. https://doi.org/10.1111/j.1439-0272.2011.01178.x
  40. Hisatomi A, Sakuma S, Fujiwara M, Seki J. Effect of tacrolimus on the cauda epididymis in rats: analysis of epididymal biochemical markers or antioxidant defense enzymes. Toxicology 2008;243:23-30. https://doi.org/10.1016/j.tox.2007.09.017
  41. El-Agamey A, Lowe GM, McGarvey DJ, Mortensen A, Phillip DM, Truscott TG, et al. Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 2004;430:37-48. https://doi.org/10.1016/j.abb.2004.03.007
  42. Kim JH, Nam SW, Kim BW, Kim WJ, Choi YH. Astaxanthin improves the proliferative capacity as well as the osteogenic and adipogenic differentiation potential in neural stem cells. Food Chem Toxicol 2010;48:1741-5. https://doi.org/10.1016/j.fct.2010.04.002
  43. Sila A, Kamoun Z, Ghlissi Z, Makni M, Nasri M, Sahnoun Z, et al. Ability of natural astaxanthin from shrimp by-products to attenuate liver oxidative stress in diabetic rats. Pharmacol Rep 2015;67:310-6.
  44. Dong LY, Jin J, Lu G, Kang XL. Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress. Mar Drugs 2013;11:960-74. https://doi.org/10.3390/md11030960
  45. Tripathi DN, Jena GB. Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells. Toxicology 2008;248:96-103. https://doi.org/10.1016/j.tox.2008.03.015
  46. Dona G, Kozuh I, Brunati AM, Andrisani A, Ambrosini G, Bonanni G, et al. Effect of astaxanthin on human sperm capacitation. Mar Drugs 2013;11:1909-19. https://doi.org/10.3390/md11061909
  47. Mansour N, McNiven MA, Richardson GF. The effect of dietary supplementation with blueberry, alpha-tocopherol or astaxanthin on oxidative stability of Arctic char (Salvelinus alpinus) semen. Theriogenology 2006;66:373-82. https://doi.org/10.1016/j.theriogenology.2005.12.002
  48. Park CH, Xu FH, Roh SS, Song YO, Uebaba K, Noh JS, et al. Astaxanthin and Corni Fructus protect against diabetes-induced oxidative stress, inflammation, and advanced glycation end product in livers of streptozotocin-induced diabetic rats. J Med Food 2015;18:337-44. https://doi.org/10.1089/jmf.2014.3174
  49. Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, et al. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 1998;59:1037-46. https://doi.org/10.1095/biolreprod59.5.1037
  50. Alves MG, Martins AD, Rato L, Moreira PI, Socorro S, Oliveira PF. Molecular mechanisms beyond glucose transport in diabetesrelated male infertility. Biochim Biophys Acta 2013;1832:626-35. https://doi.org/10.1016/j.bbadis.2013.01.011
  51. Talebi AR, Mangoli E, Nahangi H, Anvari M, Pourentezari M, Halvaei I. Vitamin C attenuates detrimental effects of diabetes mellitus on sperm parameters, chromatin quality and rate of apoptosis in mice. Eur J Obstet Gynecol Reprod Biol 2014;181:32-6. https://doi.org/10.1016/j.ejogrb.2014.07.007
  52. Ghosh A, Jana K, Pakhira BP, Ghosh D. Antiapoptotic efficacy of seed of Eugenia jambolana on testicular germ cell in experimental diabetic rat: a genomic study. Andrologia 2016;48:282-92. https://doi.org/10.1111/and.12444

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