DOI QR코드

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Phycocyanin alleviates alcohol-induced testicular injury in male Wistar rats

  • Oumayma Boukari (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Soumaya Ghoghbane (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Wahid Khemissi (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Thalja Lassili (Laboratory of Human and Experimental Pathological Anatomy, Pasteur Institute) ;
  • Olfa Tebourbi (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Khemais Ben Rhouma (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Mohsen Sakly (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage) ;
  • Dorsaf Hallegue (Laboratory of Integrated Physiology, Faculty of Sciences of Bizerte, University of Carthage)
  • 투고 : 2023.08.05
  • 심사 : 2023.10.10
  • 발행 : 2024.06.30

초록

Objective: Given the noteworthy implications of alcohol consumption and its association with male infertility, there has been a notable focus on investigating natural alternatives to mitigate its adverse effects. Thus, this study was conducted to assess the potential protective effect of phycocyanin extract derived from the blue algae Arthrospira (Spirulina) platensis against ethanol-induced oxidative stress, disturbances in testicular morphology, and alterations in sperm production. Methods: Male rats were divided into four groups (five rats each): the control group received a saline solution, the ethanol exposed group (EtOH) was subjected to intraperitoneal injections of 10 mL/kg of ethanol solution at a concentration of 38% (v/v), the phycocyanin alone treated group (P) received oral administration of phycocyanin at a dosage of 50 mg/kg, and the phycocyanin-cotreated group (PE) was given oral phycocyanin followed by ethanol injections. All treatments were administered over a period of 14 days. Results: Our findings demonstrated that ethanol exposure induced reproductive toxicity, characterized by reduced sperm production and viability, alterations in testicular weight and morphology, increased lipid peroxidation levels, and elevated oxidative enzyme activity. In addition, the ethanol-intoxicated group showed perturbations in serum biochemical parameters. However, the simultaneous exposure to ethanol and phycocyanin exhibited a counteractive effect against ethanol toxicity. Conclusion: The results showed that supplementation of phycocyanin prevented oxidative and testicular morphological damage-induced by ethanol and maintained normal sperm production, and viability.

키워드

과제정보

The authors express their sincere thanks to Professor Youssef Krichen, CEO of Bio Algae Tunisia, for the free supply of phycocyanin, and to Dr Sihem Ben Hassine for her technical assistance.

참고문헌

  1. Skakkebaek NE, Jorgensen N, Main KM, Rajpert-De Meyts E, Leffers H, Andersson AM, et al. Is human fecundity declining? Int J Androl 2006;29:2-11. https://doi.org/10.1111/j.1365-2605.2005.00573.x
  2. Mann U, Shiff B, Patel P. Reasons for worldwide decline in male fertility. Curr Opin Urol 2020;30:296-301. https://doi.org/10.1097/MOU.0000000000000745
  3. Fainberg J, Kashanian JA. Recent advances in understanding and managing male infertility. F1000Res 2019;8:F1000 Faculty Rev-670.
  4. Mima M, Greenwald D, Ohlander S. Environmental toxins and male fertility. Curr Urol Rep 2018;19:50.
  5. Leslie SW, Soon-Sutton TL, Khan MAB. Male infertility. In: StatPearls. StatPearls Publishing; 2023 [cited 2023 Oct 20]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK562258
  6. Sansone A, Di Dato C, de Angelis C, Menafra D, Pozza C, Pivonello R, et al. Smoke, alcohol and drug addiction and male fertility. Reprod Biol Endocrinol 2018;16:3.
  7. Emanuele MA, Emanuele NV. Alcohol's effects on male reproduction. Alcohol Health Res World 1998;22:195-201.
  8. Sengupta P, Dutta S, Alahmar AT. Reductive stress and male infertility. Adv Exp Med Biol 2022;1391:311-21. https://doi.org/10.1007/978-3-031-12966-7_17
  9. Prokopieva VD, Vetlugina TP. Features of oxidative stress in alcoholism. Biomed Khim 2023;69:83-96. https://doi.org/10.18097/pbmc20236902083
  10. Akbari A, Nasiri K, Heydari M, Mosavat SH, Iraji A. The protective effect of hydroalcoholic extract of Zingiber officinale Roscoe (Ginger) on ethanol-induced reproductive toxicity in male rats. J Evid Based Complementary Altern Med 2017;22:609-17. https://doi.org/10.1177/2156587216687696
  11. Akomolafe SF, Oboh G, Akindahunsi AA, Afolayan AJ. Ethanol-induced male infertility: effects of aqueous leaf extract of Tetracarpidium conophorum. Andrologia 2017;49:e12759.
  12. Leaver RB. Male infertility: an overview of causes and treatment options. Br J Nurs 2016;25:S35-40. https://doi.org/10.12968/bjon.2016.25.18.S35
  13. Dabaja AA, Schlegel PN. Medical treatment of male infertility. Transl Androl Urol 2014;3:9-16.
  14. Pez Jaeschke D, Rocha Teixeira I, Damasceno Ferreira Marczak L, Domeneghini Mercali G. Phycocyanin from Spirulina: a review of extraction methods and stability. Food Res Int 2021;143:110314.
  15. Farooq SM, Boppana NB, Devarajan A, Sekaran SD, Shankar EM, Li C, et al. C-phycocyanin confers protection against oxalate-mediated oxidative stress and mitochondrial dysfunctions in MDCK cells. PLoS One 2014;9:e93056.
  16. Munawaroh HS, Gumilar GG, Alifia CR, Marthania M, Stellasary B, Yuliani G, et al. Photostabilization of phycocyanin from Spirulina platensis modified by formaldehyde. Process Biochem 2020;94:297-304. https://doi.org/10.1016/j.procbio.2020.04.021
  17. Fernandes R, Campos J, Serra M, Fidalgo J, Almeida H, Casas A, et al. Exploring the benefits of phycocyanin: from spirulina cultivation to its widespread applications. Pharmaceuticals (Basel) 2023;16:592.
  18. Blas-Valdivia V, Moran-Dorantes DN, Rojas-Franco P, Franco-Colin M, Mirhosseini N, Davarnejad R, et al. C-phycocyanin prevents acute myocardial infarction-induced oxidative stress, inflammation and cardiac damage. Pharm Biol 2022;60:755-63. https://doi.org/10.1080/13880209.2022.2055089
  19. Penton-Rol G, Marin-Prida J, McCarty MF. C-phycocyanin-derived phycocyanobilin as a potential nutraceutical approach for major neurodegenerative disorders and COVID-19-induced damage to the nervous system. Curr Neuropharmacol 2021;19:2250-75. https://doi.org/10.2174/1570159X19666210408123807
  20. Boonlert W, Benya-Aphikul H, Umka Welbat J, Rodsiri R. Ginseng extract G115 attenuates ethanol-induced depression in mice by increasing brain BDNF levels. Nutrients 2017;9:931.
  21. Salama A, Hussein RA, Mettwally WS, Helmy MS, Ali GH. C-phycocyanin isolated from Microcystis aeruginosa Kutzing mitigates renal injury induced by potassium dichromate via toll-like receptor-4 down regulation in rats. Egypt J Chem 2021;64:3439-50. https://doi.org/10.21608/ejchem.2021.63657.3362
  22. Oumayma B, Wahid K, Soumaya G, Olfa T, Ben Rhouma K, Mohsen S, et al. Phycocyanin improved alcohol-induced hepatorenal toxicity and behavior impairment in Wistar rats. Drug Chem Toxicol 2023;46:1187-92. https://doi.org/10.1080/01480545.2022.2139843
  23. Besley MA, Eliarson R, Gallegosm AJ, Moghissi KS, Paulsen CA, Prasad MR. Laboratory manual for the examination of human semen and semen-cervical mucus interaction. WHO Press; 1980.
  24. Dorsaf H, Sabrine M, Zaineb BB, Olfa T, Mohsen S, Khemais BR. Reproductive toxicity of Carlina gummifera L. incense inhalation in adult male Wistar rats. J Hum Reprod Sci 2022;15:12-20. https://doi.org/10.4103/jhrs.jhrs_149_21
  25. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54. https://doi.org/10.1016/0003-2697(76)90527-3
  26. Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972;247:3170-5. https://doi.org/10.1016/S0021-9258(19)45228-9
  27. Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121-6. https://doi.org/10.1016/S0076-6879(84)05016-3
  28. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 1990;186:421-31. https://doi.org/10.1016/0076-6879(90)86135-I
  29. Jabri MA, Rtibi K, Sebai H. Chamomile decoction mitigates high fat diet-induced anxiety-like behavior, neuroinflammation and cerebral ROS overload. Nutr Neurosci 2022;25:1350-61. https://doi.org/10.1080/1028415X.2020.1859727
  30. Shield KD, Parry C, Rehm J. Chronic diseases and conditions related to alcohol use. Alcohol Res 2013;35:155-73.
  31. Avila MA, Marthos GC, Oliveira LG, Figueiredo EC, Giusti-Paiva A, Vilela FC. Effect of prenatal ethanol exposure on sexual motivation in adult rats. Alcohol 2016;54:11-6. https://doi.org/10.1016/j.alcohol.2016.05.002
  32. Condorelli RA, Calogero AE, Vicari E, La Vignera S. Chronic consumption of alcohol and sperm parameters: our experience and the main evidences. Andrologia 2015;47:368-79. https://doi.org/10.1111/and.12284
  33. Milat AM, Mudnic I, Grkovic I, Kljucevic N, Grga M, Jercic I, et al. Effects of white wine consumption on weight in rats: do polyphenols matter? Oxid Med Cell Longev 2017;2017:8315803.
  34. Shyngle KB. Chronic intake of separate and combined alcohol and nicotine on body maintenance among albino rats. J Hum Ecol 2006;19:21-4. https://doi.org/10.1080/09709274.2006.11905852
  35. Xie Y, Li W, Zhu L, Zhai S, Qin S, Du Z. Effects of phycocyanin in modulating the intestinal microbiota of mice. Microbiologyopen 2019;8:e00825.
  36. Lonnie M, Hooker E, Brunstrom JM, Corfe BM, Green MA, Watson AW, et al. Protein for life: review of optimal protein intake, sustainable dietary sources and the effect on appetite in ageing adults. Nutrients 2018;10:360.
  37. Husain A, Alouffi S, Khanam A, Akasha R, Farooqui A, Ahmad S. Therapeutic efficacy of natural product 'C-phycocyanin' in alleviating streptozotocin-induced diabetes via the inhibition of glycation reaction in rats. Int J Mol Sci 2022;23:14235.
  38. Walker WH. Androgen actions in the testis and the regulation of spermatogenesis. Adv Exp Med Biol 2021;1288:175-203. https://doi.org/10.1007/978-3-030-77779-1_9
  39. Yang FH, Dong XL, Liu GX, Teng L, Wang L, Zhu F, et al. The protective effect of C-phycocyanin in male mouse reproductive system. Food Funct 2022;13:2631-46. https://doi.org/10.1039/D1FO03741B
  40. Briseno-Bugarin J, Hernandez-Ochoa I, Araujo-Padilla X, Mojica-Villegas MA, Montano-Gonzalez RI, Gutierrez-Salmean G, et al. Phycobiliproteins ameliorate gonadal toxicity in male mice treated with cyclophosphamide. Nutrients 2021;13:2616.
  41. Leite LN, do Vale GT, Simplicio JA, De Martinis BS, Carneiro FS, Tirapelli CR. Ethanol-induced erectile dysfunction and increased expression of pro-inflammatory proteins in the rat cavernosal smooth muscle are mediated by NADPH oxidase-derived reactive oxygen species. Eur J Pharmacol 2017;804:82-93. https://doi.org/10.1016/j.ejphar.2017.03.024
  42. Kumar N, Singh AK. Trends of male factor infertility, an important cause of infertility: a review of literature. J Hum Reprod Sci 2015;8:191-6. https://doi.org/10.4103/0974-1208.170370
  43. Tangsrisakda N, Iamsaard S. Effect of ethanol on the changes in testicular protein expression in adult male rats. Andrologia 2020;52:e13784.
  44. Smith SJ, Lopresti AL, Fairchild TJ. The effects of alcohol on testosterone synthesis in men: a review. Expert Rev Endocrinol Metab 2023;18:155-66. https://doi.org/10.1080/17446651.2023.2184797
  45. Chiao YB, Van Thiel DH. Characterization of rat testicular alcohol dehydrogenase. Alcohol Alcohol 1986;21:9-15.
  46. Villaverde AI, Netherton J, Baker MA. From past to present: the link between reactive oxygen species in sperm and male infertility. Antioxidants (Basel) 2019;8:616.
  47. Montano-Gonzalez RI, Gutierrez-Salmean G, Mojica-Villegas MA, Cristobal-Luna JM, Briseno-Bugarin J, Chamorro-Cevallos G. Phycobiliproteins extract from Spirulina protects against single-dose cadmium-induced reproductive toxicity in male mice. Environ Sci Pollut Res Int 2022;29:17441-55. https://doi.org/10.1007/s11356-021-16668-3
  48. Dosumu OO, Duru FI, Osinubi AA, Oremosu AA, Noronha CC. Influence of virgin coconut oil (VCNO) on oxidative stress, serum testosterone and gonadotropic hormones (FSH, LH) in chronic ethanol ingestion. Agric Biol J N Am 2010;1:1126-32. https://doi.org/10.5251/abjna.2010.1.6.1126.1132
  49. Uysal M, Kutalp G, Ozdemirler G, Aykac G. Ethanol-induced changes in lipid peroxidation and glutathione content in rat brain. Drug Alcohol Depend 1989;23:227-30. https://doi.org/10.1016/0376-8716(89)90085-9
  50. Albano E. Alcohol, oxidative stress and free radical damage. Proc Nutr Soc 2006;65:278-90. https://doi.org/10.1079/PNS2006496
  51. Oei HH, Zoganas HC, McCord JM, Schaffer SW. Role of acetaldehyde and xanthine oxidase in ethanol-induced oxidative stress. Res Commun Chem Pathol Pharmacol 1986;51:195-203.
  52. Ayala A, Munoz MF, Arguelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014;2014:360438.
  53. Bhat VB, Madyastha KM. C-phycocyanin: a potent peroxyl radical scavenger in vivo and in vitro. Biochem Biophys Res Commun 2000;275:20-5. https://doi.org/10.1006/bbrc.2000.3270
  54. Younus H. Therapeutic potentials of superoxide dismutase. Int J Health Sci (Qassim) 2018;12:88-93.
  55. Nandi A, Yan LJ, Jana CK, Das N. Role of catalase in oxidative stress- and age-associated degenerative diseases. Oxid Med Cell Longev 2019;2019:9613090.
  56. Dosumu OO, Akinola OB, Akang EN. Alcohol-induced testicular oxidative stress and cholesterol homeostasis in rats: the therapeutic potential of virgin coconut oil. Middle East Fertil Soc J 2012;17:122-8. https://doi.org/10.1016/j.mefs.2011.12.005
  57. Owembabazi E, Nkomozepi P, Calvey T, Mbajiorgu EF. Co-administration of alcohol and combination antiretroviral therapy (cART) in male Sprague Dawley rats: a study on testicular morphology, oxidative and cytokines perturbations. Anat Cell Biol 2023;56:236-51. https://doi.org/10.5115/acb.22.229
  58. Akhilender Naidu K, Sarada R, Manoj G, Khan MY, Mahadeva Swamy M, Viswanatha S, et al. Toxicity assessment of phycocyanin: a blue colorant from blue green alga Spirulina platensis. Food Biotechnol 1999;13:51-66. https://doi.org/10.1080/08905439609549961
  59. Grover P, Bhatnagar A, Kumari N, Narayan Bhatt A, Kumar Nishad D, Purkayastha J. C-Phycocyanin: a novel protein from Spirulina platensis: in vivo toxicity, antioxidant and immunomodulatory studies. Saudi J Biol Sci 2021;28:1853-9. https://doi.org/10.1016/j.sjbs.2020.12.037