DOI QR코드

DOI QR Code

The impaired redox status and activated nuclear factor-erythroid 2-related factor 2/antioxidant response element pathway in wooden breast myopathy in broiler chickens

  • Pan, Xiaona (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Zhang, Lin (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Xing, Tong (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Li, Jiaolong (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Gao, Feng (College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2019.12.13
  • Accepted : 2020.04.06
  • Published : 2021.04.01

Abstract

Objective: Wooden breast (WB) is a novel myopathy affecting modern broiler chickens, which causes substantial economic losses in the poultry industry. The objective of this study was to evaluate the effect of WB abnormality on meat quality, redox status, as well as the expression of genes of the nuclear factor-erythroid 2-related factor 2 (Nrf2) pathway. Methods: A total of 80 broilers (Ross 308, 42 days of age, about 2.6 kg body weight) raised at Jiujin farm (Suqian, Jiangsu, China) were used. Twelve unaffected (no detectable hardness of the breast area) and twelve WB-affected (diffuse remarkable hardness in the breast muscle) birds were selected from the commercial broiler farm according to the criteria proposed by previous studies. Results: The results indicated that WB showed histological lesions characterized by fiber degeneration and fibrosis, along with an increase of muscle fiber diameter (p<0.05). Moreover, higher pH value, lightness, yellowness, drip loss and cooking loss were observed in the WB group (p<0.05). Compared with the normal breast (NOR) group, the WB group showed higher formation of reactive oxygen species (p<0.05), increased level of oxidation products and antioxidant activities (p<0.05), accompanied with mitochondrial damages and lower mitochondrial membrane potential (p<0.05). Meanwhile, the relative mRNA expressions of Nrf2 and its downstream antioxidant genes including heme oxygenase-1, NAD(P)H qui none dehydrogenase 1, glutathione peroxidase, superoxide dismutase, and glutamate-cysteine ligase were higher than those of the NOR group (p<0.05). Conclusion: In conclusion, WB myopathy impairs meat quality by causing oxidative damages and mitochondrial dysfunction in broilers, even though the activated Nrf2/antioxidant response element pathway provides protection for the birds.

Keywords

References

  1. Petracci M, Mudalal S, Soglia F, Cavani C. Meat quality in fast-growing broiler chickens. Worlds Poult Sci J 2015;71:363-74. https://doi.org/10.1017/S0043933915000367
  2. Velleman SG. Relationship of skeletal muscle development and growth to breast muscle myopathies: a review. Avian Dis 2015;59:525-31. https://doi.org/10.1637/11223-063015-Review.1
  3. Sihvo HK, Immonen K, Puolanne E. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol 2014;51:619-23. https://doi.org/10.1177/0300985813497488
  4. Soglia F, Mudalal S, Babini E, et al. Histology, composition, and quality traits of chicken Pectoralis major muscle affected by wooden breast abnormality. Poult Sci 2016;95:651-9. https://doi.org/10.3382/ps/pev353
  5. Soglia F, Laghi L, Canonico L, Cavani C, Petracci M. Functional property issues in broiler breast meat related to emerging muscle abnormalities. Food Res Int 2016;89:1071-6. https://doi.org/10.1016/j.foodres.2016.04.042
  6. Zambonelli P, Zappaterra M, Soglia F, et al. Detection of differentially expressed genes in broiler pectoralis major muscle affected by white striping - wooden breast myopathies. Poult Sci 2016;95:2771-85. https://doi.org/10.3382/ps/pew268
  7. Kuttappan VA, Bottje W, Ramnathan R, et al. Proteomic analysis reveals changes in carbohydrate and protein metabolism associated with broiler breast myopathy. Poult Sci 2017;96:2992-9. https://doi.org/10.3382/ps/pex069
  8. Abasht B, Mutryn MF, Michalek RD, Lee WR. Oxidative stress and metabolic perturbations in wooden breast disorder in chickens. PLoS One 2016;11:e0153750. https://doi.org/10.1371/journal.pone.0153750
  9. Mutryn MF, Brannick EM, Fu W, Lee WR, Abasht B. Characterization of a novel chicken muscle disorder through differential gene expression and pathway analysis using RNAsequencing. BMC Genomics 2015;16:399. https://doi.org/10.1186/s12864-015-1623-0
  10. Clark DL, Velleman SG. Spatial influence on breast muscle morphological structure, myofiber size, and gene expression associated with the wooden breast myopathy in broilers. Poult Sci 2016;95:2930-45. https://doi.org/10.3382/ps/pew243
  11. Reid MB. Free radicals and muscle fatigue: of ROS, canaries, and the IOC. Free Radic Biol Med 2008;44:169-79. https://doi.org/10.1016/j.freeradbiomed.2007.03.002
  12. Lu Z, He X, Ma B, et al. Chronic heat stress impairs the quality of breast-muscle meat in broilers by affecting redox status and energy-substance metabolism. J Agric Food Chem 2017; 65:11251-8. https://doi.org/10.1021/acs.jafc.7b04428
  13. Van Horssen J, Schreibelt G, Drexhage J, et al. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 2008;45:1729-37. https://doi.org/10.1016/j.freeradbiomed.2008.09.023
  14. Xu L, Zhang H, Yue H, et al. Low-current & high-frequency electrical stunning increased oxidative stress, lipid peroxidation, and gene transcription of the mitogen-activated protein kinase/nuclear factor-erythroid 2-related factor 2/antioxidant responsive element (MAPK/Nrf2/ARE) signaling pathway in breast muscle of broilers. Food Chem 2018;242:491-6. https://doi.org/10.1016/j.foodchem.2017.09.079
  15. Kay HY, Yang JW, Kim TH, et al. Ajoene, a stable garlic byproduct, has an antioxidant effect through Nrf2-mediated glutamate-cysteine ligase induction in HepG2 cells and primary hepatocytes. J Nutr 2010;140:1211-9. https://doi.org/10.3945/jn.110.121277
  16. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004;36:1199-207. https://doi.org/10.1016/j.freeradbiomed.2004.02.074
  17. Kawasaki T, Yoshida T, Watanabe T. Simple method for screening the affected birds with remarkably hardened pectoralis major muscles among broiler chickens. J Poult Sci 2016;53:291-7. https://doi.org/10.2141/jpsa.0160036
  18. Papah MB, Brannick EM, Schmidt CJ, Abasht B. Evidence and role of phlebitis and lipid infiltration in the onset and pathogenesis of wooden breast disease in modern broiler chickens. Avian Pathol 2017;46:623-43. https://doi.org/10.1080/03079457.2017.1339346
  19. Kawasaki T, Iwasaki T, Yamada M, Yoshida T, Watanabe T. Rapid growth rate results in remarkably hardened breast in broilers during the middle stage of rearing: a biochemical and histopathological study. PLoS One 2018;13:e0193307. https://doi.org/10.1371/journal.pone.0193307
  20. Brambila GS, Bowker BC, Chatterjee D, Zhuang H. Descriptive texture analyses of broiler breast fillets with the wooden breast condition stored at 4℃ and -20℃. Poult Sci 2018;97:1762-7. https://doi.org/10.3382/ps/pew327
  21. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  22. Dalle Zotte A, Tasoniero G, Puolanne E, et al. Effect of "wooden breast" appearance on poultry meat quality, histological traits, and lesions characterization. Czech J Anim Sci 2017;62:51-7. https://doi.org/10.17221/54/2016-CJAS
  23. Velleman SG. Recent developments in breast muscle myopathies associated with growth in poultry. Annu Rev Anim Biosci 2019;7:289-308. https://doi.org/10.1146/annurevanimal-020518-115311
  24. Meloche KJ, Dozier WA, Brandebourg TD, Starkey JD. Skeletal muscle growth characteristics and myogenic stem cell activity in broiler chickens affected by wooden breast. Poult Sci 2018;97:4401-14. https://doi.org/10.3382/ps/pey287
  25. Wilhelm AE, Maganhini MB, Hernandez-Blazquez FJ, Ida EI, Shimokomaki M. Protease activity and the ultrastructure of broiler chicken PSE (pale, soft, exudative) meat. Food Chem 2010;119:1201-4. https://doi.org/10.1016/j.foodchem.2009.08.034
  26. Maxwell AD, Bowker BC, Zhuang H, Chatterjee D, Adhikari K. Descriptive sensory analysis of marinated and non-marinated wooden breast fillet portions. Poult Sci 2018;97:2971-8. https://doi.org/10.3382/ps/pey145
  27. Dalgaard LB, Rasmussen MK, Bertram HC, et al. Classification of wooden breast myopathy in chicken pectoralis major by a standardised method and association with conventional quality assessments. Int J Food Sci Technol 2018;53:1744-52. https://doi.org/10.1111/ijfs.13759
  28. Salles GBC, Boiago MM, Silva AD, et al. Lipid peroxidation and protein oxidation in broiler breast fillets with white striping myopathy. J Food Biochem 2019;43:e12792. https://doi.org/10.1111/jfbc.12792
  29. Noeman SA, Hamooda HE, Baalash AA. Biochemical study of oxidative stress markers in the liver, kidney and heart of high fat diet induced obesity in rats. Diabetol Metab Syndr 2011;3:17. https://doi.org/10.1186/1758-5996-3-17
  30. Kristal BS, Park BK, Yu BP. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J Biol Chem 1996;271:6033-8. https://doi.org/10.1074/jbc.271.11.6033
  31. Martinaud A, Mercier Y, Marinova P, Tassy C, Gatellier P, Renerre M. Comparison of oxidative processes on myofibrillar proteins from beef during maturation and by different model oxidation systems. J Agric Food Chem 1997;45:2481-7. https://doi.org/10.1021/jf960977g
  32. Kanner J. Oxidative processes in meat and meat products: quality implications. Meat Sci 1994;36:169-89. https://doi.org/10.1016/0309-1740(94)90040-X
  33. Sohail MU, Rahman ZU, Ijaz A, et al. Single or combined effects of mannan-oligosaccharides and probiotic supplements on the total oxidants, total antioxidants, enzymatic antioxidants, liver enzymes, and serum trace minerals in cyclic heat-stressed broilers. Poult Sci 2011;90:2573-7. https://doi.org/10.3382/ps.2011-01502

Cited by

  1. Redox Homeostasis in Poultry: Regulatory Roles of NF-κB vol.10, pp.2, 2021, https://doi.org/10.3390/antiox10020186