Abstract
Lead (Pb) is one of the most common environmental pollutants and causes adverse effects on human and animal health. This study aimed to evaluate the protective role of beta-glucan against hepatic and reproductive toxicity induced by lead acetate. A total of 28 Sprague Dawley male rats were distributed into four groups (n = 7). The control group was intraperitoneally injected saline (1 ml/kg b.w.) daily for 21 days, the Pb group was intraperitoneally injected lead acetate (15 mg/kg b.w.) daily for 21 days, the beta-glucan group was orally administrated beta-glucan (50 mg/kg b.w.) daily for 21 days, and the Pb + beta-glucan group was intraperitoneally injected lead acetate (15 mg/kg b.w.) daily following the oral administration of beta-glucan (50 mg/kg b.w.) daily for 21 days. Results showed that feed intake in the Pb + beta-glucan group was significantly increased in comparison with that of the Pb group (p < 0.001). We also found that liver malondialdehyde (MDA) level was increased significantly in the Pb group (p < 0.01), while glutathione (GSH) level (p < 0.05), glutathione peroxidase (GSH-Px) (p < 0.05), and catalase (CAT) (p < 0.01) activities were reduced when they were compared with control. Moreover, Pb administration increased expression of pro-apoptotic protein Bax, the ratio of Bax/Bcl-2, and decreased the expression of the antiapoptotic protein Bcl-2 (p < 0.01). Also, Pb was found to cause a significant decrease in sperm motility (p < 0.01) and sperm concentration (p < 0.05) but increase in sperm tails and total sperm anomalies (p < 0.05). These findings were partially preserved by the administration of beta-glucan. Taken together, these results indicated that beta-glucan has the potential to alleviate the Pb-induced toxicity.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abd El-Hack ME, Abdelnour SA, Abd El-Moneim AEME, Arif M, Khafaga A, Shaheen H, Samak D, Swelum AA (2019) Putative impacts of phytogenic additives to ameliorate lead toxicity in animal feed. Environ Sci Pollut Res 26:23209–23218
Abdel-Latif MA, Abd El-Hack ME, Swelum AA, Saadeldin IM, Elbestawy AR, Shewita RS, Ba-Awadh HA, Alowaimer AN, Abd El-Hamid HS (2018) Single and combined effects of clostridium butyricum and saccharomyces cerevisiae on growth indices, intestinal health, and immunity of broilers. Animals 8:184
Aebi H (1983) Catalase. In: Bergmeyer HU (ed) Methods in enzymatic analysis. Academic Press, New York, pp 276–286
Ak Sonat F, Alcay S, Toker MB, Peker S, Ustuner B (2018) The effects of dietary restriction and administration of β-glucan from Euglena gracilis on the sperm characteristics and reproductive organs of rats. Andrologia 50:e13088
Akaras N, Abuc OO, Koc K, Bal T, Geyikoglu F, Atilay H, Erol HS, Yigit S, Gul M (2020) (1 → 3)-β-d-glucan enhances the toxicity induced by Bortezomib in rat testis. J Food Biochem 44:e13155
Alp H, Varol S, Celik M, Altas M, Evliyaoglu O, Tokgoz O, Tanrıverdi MH, Uzar E (2012) Protective effects of b glucan and gliclazide on brain tissue and sciatic nerve of diabetic rats induced by streptozosin. Exp Diabetes Res 2012:230342
Bai J, Ren Y, Li Y, Fan M, Qian H, Wang L, Wu G, Zhang H, Qi X, Xu M, Rao Z (2019) Physiological functionalities and mechanisms of β-glucans. Trends Food Sci Technol 88:57–66
Bass JJ, Wilkinson DJ, Rankin D, Phillips BE, Szewczyk NJ, Smith K, Atherton PJ (2017) An overview of technical considerations for Western blotting applications to physiological research. Scand J Med Sci Sports 27:4–25
Blaszczyk K, Wilczak J, Harasym J, Gudej S, Suchecka D, Królikowski T, Lange E, Gromadzka-Ostrowska J (2015) Impact of low and high molecular weight oat beta-glucan on oxidative stress and antioxidant defense in spleen of rats with LPS induced enteritis. Food Hydrocoll 51:272–280
Bozbulut R, Sanlier N (2019) Promising effects of β-glucans on glyceamic control in diabetes. Trends Food Sci Technol 83:159–166
Cetin E (2019) Pretreatment with β-glucan attenuates isoprenaline-induced myocardial injury in rats. Exp Physiol 104:505–513
Ciecierska A, Drywień ME, Hamulka J, Sadkowski T (2019) Nutraceutical functions of beta-glucans in human nutrition. Rocz Panstw Zakl Hig 70:315–324
Comiran PK, Ribeiro MC, Silva JHG, Martins KO, Santos IA, Chiaradia AEF, Silva AZ, Dekker RFH, Barbosa-Dekker AM, Alegranci P, Queiroz EAIF (2020) Botryosphaeran attenuates tumor development and the cancer cachexia syndrome in walker-256 tumor-bearing obese rats and improves the metabolic and hematological profiles of these rats. Nutr Cancer 8:1–18
El-Khadragy M, Al-Megrin WA, AlSadhan NA, Metwally DM, El-Hennamy RE, Salem FEH, Kassab RB, Abdel Moneim AE (2020) Impact of Coenzyme Q10 Administration on lead acetate-induced testicular damage in rats. Oxidative Med Cell Longev 2020:4981386
Erisir M, Benzer F, Ozkaya A, Dag U (2018) The effect of naringenin on oxidative stress in some tissues (heart, lung, brain, spleen, muscle) of lead-treated rats. Atatürk University J Vet Sci 13:34–41
Ezejiofor AN, Orisakwe OE (2019) The protective effect of Costus afer Ker Gawl aqueous leaf extract on lead-induced reproductive changes in male albino Wistar rats. JBRA Assist Reprod 23:215–224
Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress and its possible reversal by chelation therapy. Indian J Med Res 128:501–523
Graaff P, Govers C, Wichers HJ, Debets R (2018) Consumption of β-glucans to spice up T cell treatment of tumors: a review. Expert Opin Biol Ther 18:1023–1040
Hassan E, El-Neweshy M, Hassan M, Noreldin A (2019) Thymoquinone attenuates testicular and spermotoxicity following subchronic lead exposure in male rats: Possible mechanisms are involved. Life Sci 230:132–140
IBM SPSS (2013) Statistics for Windows, Version 22.0. IBM Copyright SPSS Inc., Armonk, NY.
Jacob JP, Pescatore AJ (2014) Barley β-glucan in poultry diets. Ann Transl Med 2:20
Kaur R, Sharma M, Ji D, Xu M, Agyei D (2020) Structural features, modification, and functionalities of beta-glucan. Fibers 8:1
Kaya K, Ciftci O, Aydın M, Cetin A, Basak N (2019) Favourable effect of β-glucan treatment against cisplatin-induced reproductive system damage in male rats. Andrologia 51:e13342
Khalil SR, Elhady WM, Elewab YHA, Abd El-Hameed NE, Alib SA (2018) Possible role of Arthrospira platensis in revers- ing oxidative stress-mediated liver damage in rats exposed to lead. Biomed Pharmacother 97:1259–2126
Kielkopf CL, Bauer W, Urbatsch IL (2012) Expressing cloned genes for protein production, purufication and analysis. In: Green MR, Sambrook J (eds) Molecular cloning: a laboratory manual, 4th edn. Cold Spring Harbor Laboratory Press, New York, pp 1599–1625
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958
Lowry OH, Rosenbrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Massányi P, Massányi M, Madeddu R, Stawarz R, Lukáč N (2020) Effects of cadmium, lead, and mercury on the structure and function of reproductive organs. Toxics 8:94
Mejía SMV, de Francisco A, Bohrer B (2020) A comprehensive review on cereal β-glucan: extraction, characterization, causes of degradation, and food application. Crit Rev Food Sci Nutr 60:3693–3704
Mihailovic M, Arambasic J, Uskokovic A (2013) β-Glucan administration to diabetic rats reestablishes redox balance and stimulates cellular pro-survival mechanisms. J Funct Foods 5:267–278
Mo L, Chen Y, Li W, Guo S, Wang X, An H, Zhan Y (2017) Anti-tumor effects of (1 → 3)-β-d-glucan from Saccharomyces cerevisiae in S180 tumor-bearing mice. Int J Biol Macromol 95:385–392
Mumtaz S, Ali S, Shakir HA KR, Tahir HM, Mumtaz S, Andleeb S (2020) Therapeutic role of garlic and vitamins C and E against toxicity induced by lead on various organs. Environ Sci Pollut Res 27:8953–8964
Omobowale OT, Oyagbemi AA, Akinrinde AS, Saba AB, Daramola OT, Ogunpolu BS, Olopade JO (2014) Failure of recovery from lead induced hepatoxicity and disruption of erythrocyte antioxidant defence system in Wistar rats. Environ Toxicol Pharmacol 37:1202–1211
Piomboni P, Gambera L, Serafini F, Campanella G, Morgante G, De Leo V (2008) Sperm quality improvement after natural anti-oxidant treatment of asthenoteratospermic men with leukocytospermia. Asian J Androl 10:201–206
Placer ZA, Cushman LL, Johnson BC (1966) Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal Biochem 16:359–364
Sannadi S, Ryala PK, Gottipolu RR (2013) Reversal effect of monoisoamyl dimercaptosuccinic acid (MiADMSA) for arsenic and lead induced perturbations in apoptosis and antioxidant enzymes in developing rat brain. Int J Dev Neurosci 31:586–597
Sarsilmaz M, Ozen OA, Ozyurt H (2000) The Evaluation of the enzymatic antioxidan system of liver after the subacute and subchronic inhalation of formaldehyde in rats. Van Med J 7:84–89
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192–205
Sener G, Sert G, Sehirli AO, Arpak S (2006) Pressure ulcer-induced oxidative organ injury is ameliorated by β-glucan treatment in rats. Int Immunopharmacol 6:724–732
Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85
Soleimanzadeh A, Kian M, Moradi S, Mahmoudi S (2020) Carob (Ceratonia siliqua L.) fruit hydro-alcoholic extract alleviates reproductive toxicity of lead in male mice: Evidence on sperm parameters, sex hormones, oxidative stress biomarkers and expression of Nrf2 and iNOS. Avicenna J Phytomed 10:35–49
Suchecka D, Błaszczyk K, Harasym J, Gudej S, Wilczak J, Gromadzka-Ostrowska J (2017) Impact of purified oat 1-3,1-4-b-d-glucan of different molecular weight on alleviation of inflammation parameters during gastritis. J Funct Foods 28:11–18
Sudjarwo SA, Eraiko K, Sudjarwo GW, Koerniasari (2019) The potency of chitosan-Pinus merkusii extract nanoparticle as the antioxidant and anti-caspase 3 on lead acetate-induced nephrotoxicity in rat. J Adv Pharm Technol Res 10:27–32
Taha HSA, Abdelnour SA, Alagawany M (2019) Growth performance, biochemical, cytological and molecular aspects of rabbits exposed to lead toxicity. J Anim Physiol Anim Nutr (Berl) 103:747–755
Thangarajan S, Vedagiri A, Somasundaram S, Sakthimanogaran R, Murugesan M (2018) Neuroprotective effect of morin on lead acetate- induced apoptosis by preventing cytochrome c translocation via regulation of Bax/Bcl-2 ratio. Neurotoxicol Teratol 66:35–45
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350–4354
Turk G, Atessahin A, Sonmez M, Yuce A, Ceribasi AO (2007) Lycopene protects against cyclosporine A-induced testicular toxicity in rats. Theriogenology 67:778–785
Wang H, Li D, Hu Z, Zhao S, Zheng Z, Li W (2016) Protective effects of green tea polyphenol against renal injury through ROS-mediated JNK-MAPK pathway in lead exposed rats. Mol Cell 39:508–513
Yilmaz O, Dinc H (2013) The effects of heavy metals on reproductive system. Van Vet J 24:91–94
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This work supported by the Fırat University Research Fund of Elazig, as Master thesis study Project (Project number: VF.18.13).
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PTS designed the study and wrote first draft of the manuscript. PTS, IS, SIM, OEK and GA conducted the experiments. GA performed oxidative stress and protein expression analyses. SOK performed sperm analyses. SIM, SOK, and GA analyzed the data and prepared figures. All authors read and approved the final manuscript.
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This study was conducted with the ethics committee approval of Fırat University Animals Experiments Local Ethics Committee dated 11.07.2018, with a decision no. 131 and protocol no 2018/67.
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Tatli Seven, P., Iflazoglu Mutlu, S., Seven, I. et al. Protective role of yeast beta-glucan on lead acetate-induced hepatic and reproductive toxicity in rats. Environ Sci Pollut Res 28, 53668–53678 (2021). https://doi.org/10.1007/s11356-021-14398-0
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DOI: https://doi.org/10.1007/s11356-021-14398-0