Pınar TATLI SEVEN, İsmail SEVEN, Seda İFLAZOĞLU MUTLU, Mesut AKSAKAL, Gözde ARKALI, Nurgül BİRBEN, Aslıhan SUR ARSLAN

The curative effects of dietary yeast beta-1,3/1,6-glucan on oxidative stress and apoptosis in laying quails (Coturnix coturnix japonica) exposed to lead

Abstract: The objective of this study was to investigate the effects of supplementation of beta-glucan to the basal diet of laying quails exposed to lead (Pb) toxicity. A total of 112 birds were randomly divided into 4 groups. The first group was fed a corn-soybean based basal diet without any supplementation (control). The second (Pb) and third (beta-glucan) groups were supplemented with 100 mg/kg of Pb (as Pb acetate) and 100 mg/kg of beta-glucan, respectively. The fourth group (Pb + beta-glucan) was fed a basal diet supplemented with 100 mg/kg of Pb and 100 mg/kg of beta-glucan. It was determined that serum total protein, albumin, and creatinine values of the Pb + beta-glucan group partially improved (P < 0.05) with the addition of beta-glucan, but globulin and blood urea nitrogen (BUN) values were similar to the Pb group (P < 0.001). Globulin and albumin/globulin ratio were not affected by the supplements. Aspartate aminotransferase (AST) (P < 0.01) and alanine transaminase (ALT) (P < 0.001) enzyme activities in the beta-glucan and Pb + betaglucan groups were similar to the control group, unlike the Pb group. However, ALP enzyme activity was similar in all supplemented groups, unlike the control group (P < 0.01). Malondialdehyde (P < 0.001) was reduced in the liver, heart, and kidney tissues of betaglucan supplemented groups compared to the Pb group. Glutathione levels of liver and heart tissues in the Pb + beta-glucan group were significantly higher than in the Pb group (P < 0.001). Catalase and glutathione peroxidase activities were also significantly increased in all tissues by supplementation of beta-glucan as compared to the Pb group. The caspase-3 and caspase-9 protein expression levels in the liver tissue of the beta-glucan group decreased (P < 0.001) compared to the Pb group. As a result, we conclude that beta-glucan helps reduce the harmful effects of Pb toxicity in laying quails.Key words: Beta-glucan, lead toxicity, oxidative damage, apoptosis, quail

PDF

___

1. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy Metals toxicity and the environment. In: Luch A (editor). Molecular, Clinical and Environmental Toxicology (Volume 3: Environmental Toxicology). Berlin, Germany: Springer, Basel; 2012. pp. 133-164.
2. Wani AL, Ara A, Usmani JA. Lead toxicity: a review. Interdisciplinary Toxicology 2015; 8 (2): 55-64. doi: 10.1515/ intox-2015-0009
3. Sharma R, Panwar K, Mogra S. Effects of prenatal and neonatal exposure to lead on white blood cells in Swiss mice. Journal of Cell and Molecular Biology 2012; 10 (1): 33-40.
4. Assi MA, Hezmee MN, Haron AW, Sabri MY, Rajion MA. The detrimental effects of lead on human and animal health. Veterinary World 2016; 9 (6): 660-671. doi: 10.14202/ vetworld.2016.660-671
5. Volman JJ, Ramakers D, Plat J. Dietary modulation of immune function by beta-glucans. Physiology & Behavior 2009; 94 (2): 276-284. doi: 10.1016/j.physbeh.2007.11.045
6. Bashir KMI, Choi JS. Clinical and physiological perspectives of β-glucans: the past, present, and future. International Journal of Molecular Sciences 2017; 18 (9):1906.doi: 10.3390/ ijms18091906
7. Kaur R, Sharma M, Ji D, Xu M, Agyei D. Structural features, modification, and functionalities of beta-glucan. Fibers 2020; 8 (1): 1.doi: 10.3390/fib8010001
8. Zhu F, Du B, Xu B. A critical review on production and industrial applications of beta-glucans. Food Hydrocolloid 2016; 52: 275-288.doi: 10.1016/j.foodhyd.2015.07.003
9. Wang Q, Sheng X, Shi A, Hu H, Yang Y et al. β-Glucans: Relationships between modification, conformation and functional activities. Molecules 2017; 22 (2): 257. doi:10.3390/ molecules22020257
10. Yuan H, Lan P, He Y, Li C, Ma X. Effect of the modifications on the physicochemical and biological properties of β-glucan—a critical review. Molecules 2020; 25 (1): 57.doi: 10.3390/ molecules25010057.
11. Lucia M, Andre JM, Gontier K, Diot N, Veiga J et al. Trace element concentrations (mercury, cadmium, copper, zinc, lead, aluminium, nickel, arsenic, and selenium) in some aquatic birds of the Southwest Atlantic Coast of France. Archives of Environmental Contamination and Toxicology 2010; 58 (3): 844-853. doi: 10.1007/s00244-009-9393-9
12. Pain DJ, Mateo R, Green RE. Effects of lead from ammunition on birds and other wildlife: A review and update. Ambio 2019; 48 (9): 935-953.doi: 10.1007/s13280-019-01159-0.
13. Ahmed WM, Abdel-Hameed AR, Moghazy FME. Some reproductive and health aspects of female buffaloes in relation to blood lead concentration. International Journal of Dairy Science 2008; 3 (2): 63-70. doi:10.3923/ijds.2008.63.70
14. Burki TK. Nigeria’s lead poisoning crisis could leave a long legacy. Lancet 2012; 379 (9818): 792. doi: 10.1016/s0140- 6736(12)60332-8.
15. McDowell LR. Minerals in Animal and Human Nutrition. 2nd ed. Amsterdam, Netherlands: Elsevier Science BV; 2003.
16. Seven I, Aksu T, Tatli Seven P. The effects of propolis on biochemical parameters and activity of antioxidant enzymes in broilers exposed to lead-induced oxidative stress. Asian Australasian Journal of Animal Sciences 2010; 23 (11): 1482- 1489. doi: 10.5713/ajas.2010.10009
17. Seven I, Aksu T, Tatlı Seven P. The effects of propolis and vitamin C supplemented feed on performance, nutrient utilization and carcass characteristics in broilers exposed to lead. Livestock Science 2012; 148 (1-2): 10-15.doi:10.1016/j. livsci.2012.05.001
18. Xu LH, Mu FF, Zhao JH, He Q, Cao CL et al. Lead induces apoptosis and histone hyperacetylation in rat cardiovascular tissues. PLoS ONE 2015; 10 (6): e0129091. doi:10.1371/journal. pone.0129091
19. Yuan C, Song HH, Jiang YJ, Azzam MMM, Zhu S et al. Effects of lead contamination in feed on laying performance, lead retention of organs and eggs, protein metabolism, and hormone levels of laying hens. The Journal of Applied Poultry Research 2013; 22 (4): 878-884. doi: 10.3382/japr.2013-00801
20. Ahamed M, Siddiqui MKJ. Low level lead exposure and oxidative stress: Current opinions. Clinica Chimica Acta 2007; 383 (1-2): 57-64. doi: 10.1016/j.cca.2007.04.024
21. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology 2000; 7 (3): 153-163. doi:10.1016/S0928- 4680(00)00053-5
22. Loh KP, Huang SH, De Silva R, Tan BKH, Zhu YZ. Oxidative stress: apoptosis in neuronal injury. Current Alzheimer Research 2006; 3 (4): 327-337. doi: 10.2174/156720506778249515
23. Kayali H, Ozdag MF, Kahraman S, Aydin A, Gonul E et al. The antioxidant effect of beta-glucan on oxidative stress status in experimental spinal cord injury in rats. Neurosurgical Review. 2005; 28 (4): 298-302. doi: 10.1007/s10143-005-0389-2
24. Tatli Seven P, Yilmaz S, Seven I, Tuna Kelestemur G. Effects of propolis in animals exposed oxidative stress. In: Lushchak VI (editor). Oxidative Stress - Environmental Induction and Dietary Antioxidants. 1st ed. Rijeka, Croatia: InTECH; 2012. pp. 267-288.
25. Şener G, Toklu H, Ercan F, Erkanlı G. Protective effect of b-glucan againts oxidative organ injury in rat model of sepsis. International Immunopharmacology 2005; 5 (9): 1387-1396. doi: 10.1016/j.intimp.2005.03.007
26. NRC (National Research Council). Nutrient Requirement of Poultry. 9th ed. Washington DC, USA: National Academy Press, 1994.
27. Alagawany M, Abd El-Hack ME, Farag MR, Elnesr SS, ElKholy MS et al. Dietary supplementation of yucca schidigera extract enhances productive and reproductive performances, blood profile, immune function, and antioxidant status in laying Japanese quails exposed to lead in the diet. Poultry Science 2018; 97 (9): 3126-3137.doi: 10.3382/ps/pey186
28. Farag MR, Alagawany M, Abd El-Hack ME, El-Sayed SAA, Ahmed SYA et al. Yucca schidigera extract modulates the lead-induced oxidative damage, nephropathy and altered inflammatory response and glucose homeostasis in Japanese quails. Ecotoxicology and Environmental Safety 2018; 156: 311-321.doi: 10.1016/j.ecoenv.2018.03.010
29. Moon SH, Lee I, Feng X, Lee HY, Kim J et al. Effect of dietary Beta-glucan on the performance of broilers and the quality of broiler breast meat. Asian-Australasian Journal of Animal Sciences 2016; 29 (3): 384-389.doi: 10.5713/ajas.15.0141
30. Zhu M, Wu S. The growth performance and nonspecific immunity of loach paramisgurnusdabryanus as affected by dietary β-1,3-glucan. Fish & Shellfish Immunology 2018; 83: 368-372. doi: 10.1016/j.fsi.2018.09.049
31. Lowry OH, Rosenbrough NJ, Farr AL, Randal RJ. Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 1951; 193 (1): 265-275.
32. Placer ZA, Cushman LL, Johnson BC. Estimation of product of lipid peroxidation (malonyldialdehyde) in biochemical systems. Analytical Biochemistry 1966; 16 (2): 359-364. doi:10.1016/0003-2697(66)90167-9
33. Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analytical Biochemistry 1968; 25 (1):192-205. doi:10.1016/0003-2697(68)90092-4
34. Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium-deficient rat liver. Biochemical and Biophysical Research Communications 1976; 71 (1): 952-958.doi: 10.1016/0006-291x(76)90747-6 35. Goth LA. Simple method for determination of serum catalase activity and revision of reference range. Clinica Chimica Acta 1991; 196 (2-3): 143-151. doi: 10.1016/0009-8981(91)90067-M
36. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH et al. Measurement of protein using bicinchoninic acid. Analytical Biochemistry 1985; 150 (1): 76-85.doi: 10.1016/0003-2697(85)90442-7
37. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227 (5259): 680-685.doi:10.1038/227680a0
38. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 1979; 76 (9): 4350-4354.doi: 10.1073/pnas.76.9.4350
39. Kielkopf CL, Bauer W, Urbatsch IL. Expressing cloned genes for protein production, purification and analysis. In: Green MR, Sambrook J (editors). Molecular Cloning: A Laboratory Manual. 4thed. New York, USA: Cold Spring Harbor Laboratory Press; 2012. pp. 1599-1625.
40. Bass JJ, Wilkinson DJ, Rankin D, Phillips BE, Szewczyk NJ et al. An overview of technical considerations for Western blotting applications to physiological research. Scandinavian Journal of Medicine and Science in Sports 2017; 27 (1): 4-25.doi: 10.1111/ sms.12702
41. SPSS. IBM SPSS Statisticsfor Windows, version22.0. NY, Armonk, USA: IBM; 2013.
42. Hui CA. Concentrations of chromium, manganese, and lead in air and in avian eggs. Environmental Pollution 2002; 120 (2): 201-206.doi:10.1016/S0269-7491(02)00158-6
43. Kou H, Ya J, Gao X, Zhao H. The effects of chronic lead exposure on the liver of female Japanese quail (Coturnix japonica): Histopathological damages, oxidative stress and AMP-activated protein kinase based lipid metabolism disorder. Ecotoxicology and Environmental Safety 2020; 190;110055. doi: 10.1016/j.ecoenv.2019.110055
44. Flora SJS. Nutritional components modify metal absorption, toxic response and chelation therapy. Journal of Nutritional & Environmental Medicine 2009; 12 (1): 53-67. doi:10.1080/13590840220123361
45. Flora G, Gupta D, Tiwari A. Toxicity of lead: A review with recent updates. Interdisciplinary Toxicology 2012; 5 (2): 47-58. doi: 10.2478/v10102-012-0009-2
46. Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biology 2013; 14 (1): 32.doi: 10.1186/1471-2121-14-32.
47. Yedjou CG, Milner JN, Howard CB, Tchounwou BP. Basic apoptotic mechanisms of lead toxicity in human leukemia (Hl-60) cells. International Journal of Environmental Research and Public Health 2010; 7 (5): 2008-2017. doi:10.3390/ ijerph7052008
48. Kofuji K, Aoki A, Tsubaki K, Konishi M, Isobe Y et al. Antioxidant Activity of β-Glucan. ISRN Pharmaceutics 2012; 2012:125864. doi: 10.5402/2012/125864
49. Bahakaim ASA, Mousa SMM, Soliman MM. Effect of mannan oligosaccharides and β-glucans on productive performance, egg quality and blood biochemical and hematological parameters of laying Japanese quail. Egyptian Poultry Science Journal, 2015; 35 (4): 1109-1122.
50. Mousa SMM, Soliman MM, Bahakaim ASA. Effect of mannan oligosaccharides and β-glucans on productive performance and some physiological and immunological parameters of growing Japanese quail chicks. Egyptian Poultry Science Journal, 2014; 34 (2): 433-451.
51. Gu K, Zhao L, Wang L, Bu D, Liu N et al. Effects of dietary supplementation of yeast beta-glucan on performance, serum biochemical indices and antioxidant capacity of transition dairy cows. Chinese Journal of Animal Nutrition 2018; 30 (6): 2164-2171.
52. Shan-bai DHX, Xiao-bo HU. Study on antitumor and antioxidant activities of yeast beta-1,3-glucan hydrolysates in vivo. Journal of Huazhong Agricultural University 2007; 26 (6): 871-874.
53. Tang Q, Huang G. Progress in polysaccharide derivatization and properties. Mini Reviews in Medicinal Chemistry 2016; 16 (15): 1244-1257. doi: 10.2174/138955751699916061216400 3
54. Guo W, Gu X, Tong Y, Wang X, Wu J et al. Protective effects of mannan/β-glucans from yeast cell wall on the deoxyniyalenolinduced oxidative stress and autophagy in IPEC-J2 cells. International Journal of Biological Macromolecules 2019; 135: 619-629.doi:10.1016/j.ijbiomac.2019.05.180
55. Lockshin RA. Programmed cell death: history and future of a concept. Journal de la Société de Biologie 2005; 199 (63): 169- 173. doi: 10.1051/jbio:2005017