Determination of local expressions of IGF-1, LC3B and NF-kB in white muscle disease in lambs by immunohistochemical method
Year 2024,
, 79 - 86, 22.08.2024
Gökhan Akçakavak
,
Özhan Karataş
,
Ayşenur Tural
,
Osman Dağar
,
Osman Doğan
,
Mehmet Tuzcu
Abstract
White muscle disease (WMD) is also known as Stiff Lamb Disease or Nutritional Muscular Dystrophy. Selenium and/or Vitamin E deficiency constitutes the etiology of the disease. This study aimed to immunohistochemically evaluate local protein expressions of Nuclear factor kappa B (NF-kB), Insulin-like growth factor-1 (IGF-1) and Microtubule-related protein 1A/1B-light chain 3 beta (LC3B) in WMD. The material of the study consisted of 15 WMD, and 6 healthy lamb heart samples. The heart tissues of the autopsied lambs were subjected to routine tissue processing and paraffin blocks were obtained. Then, it was stained with Hematoxylin-Eosin and immunohistochemical methods. Control group lambs had normal macroscopic appearance. Macroscopically, hyaline degeneration and zenker’s necrosis, calcification areas were observed in WMD tissues. Microscopically, degenerative and necrotic muscle fibers, calcification areas, fibrosis, mononuclear cell infiltrates and macrophage infiltrates were detected in WMD heart tissues. Immunohistochemically, significant increases were detected in IGF-1 (p<0.001), LC3B (p<0.001) and NF-kB (p<0.05) in the WMD group compared to the control group. Immunoreactivity in the relevant primers was detected commonly in degenerative and necrotic muscle fibers. In addition, occasional immunoreactivity was observed in the relevant primers in inflammatory cell infiltrates. In conclusion, NF-kB, IGF-1 and LC3B protein expressions were evaluated immunohistochemically for the first time in lambs with WMD. Our findings show that IGF-1 and LC3B proteins are highly expressed in heart tissue in WMD. Additionally, it is possible to say that IGF-1 and LC3B can be used in the diagnosis of WMD disease.
References
- Akcakavak G., Kazak F., & Deveci M.Z.Y. (2023). Eucalyptol protects against cisplatin-induced liver injury in rats. Biology Bulletin , 50, 987-994. https://10.1134/s106235902360085x
- Abutarbush, S.M., & Radostits, O.M. (2003). Congenital nutritional muscular dystrophy in a beef calf. The Canadian Veterinary Journal, 44(9), 738-739.
- Al‐Shanti, N., & Stewart, C.E. (2012). Inhibitory effects of IL‐6 on IGF‐1 activity in skeletal myoblasts could be mediated by the activation of SOCS‐3. Journal of Cellular Biochemistry, 113(3), 923-933. https://doi.org/10.1002/jcb.23420
- Ataollahi, F., Mohri, M., Seifi, H.A., Pingguan-Murphy, B., Wan Abas, W.A.B., & Osman, N. A.A. (2013). Evaluation of copper concentration in subclinical cases of white muscle disease and its relationship with cardiac troponin I. PloS One, 8(2), e56163. https://doi.org/10.1371/journal.pone.0056163
- Bailes, J., & Soloviev, M. (2021). Insulin-like growth factor-1 (IGF-1) and its monitoring in medical diagnostic and in sports. Biomolecules, 11(2), 217. https://doi.org/10.3390/biom11020217
- Biswas, R., & Bagchi, A. (2016). NFkB pathway and inhibition: an overview. Computational Molecular Biology, 6(1). https://doi.org/10.5376/cmb.2016.06.0001
- Cuevas, M.J., Almar, M., García-Glez, J.C., García-López, D., De Paz, J.A., Alvear-Órdenes, I., & González-Gallego, J. (2005). Changes in oxidative stress markers and NF-κB activation induced by sprint exercise. Free Radical Research, 39(4), 431-439. https://doi.org/10.1080/10715760500072149
- Dabak, M., Karataş, F., Gül, Y., & Kizil, Ö. (2002). Investigation of selenium and vitamin e deficiency in beef cattle. Turkish Journal of Veterinary & Animal Sciences, 26(4), 741-746.
- Grounds, M.D., Radley, H.G., Gebski, B.L., Bogoyevitch, M.A., & Shavlakadze, T. (2008). Implications of cross‐talk between tumour necrosis factor and insulin‐like growth factor‐1 signalling in skeletal muscle. Clinical and Experimental Pharmacology and Physiology, 35(7), 846-851. https://doi.org/10.1111/j.1440-1681.2007.04868.x
- Gusscott, S., Jenkins, C.E., Lam, S.H., Giambra, V., Pollak, M., & Weng, A.P. (2016). IGF1R derived PI3K/AKT signaling maintains growth in a subset of human T-cell acute lymphoblastic leukemias. PloS One, 11(8), e0161158. https://doi.org/10.1371/journal.pone.0161158
- Ichimiya, T., Yamakawa, T., Hirano, T., Yokoyama, Y., Hayashi, Y., Hirayama, D., Wagatsuma, K., Itoi, T., & Nakase, H. (2020). Autophagy and autophagy-related diseases: a review. International Journal of Molecular Sciences, 21(23), 8974. https://doi.org/10.1371/journal.pone.0161158
- Karakurt, E., Karataş, Ö., Dağ, S., Beytut, E., Mendil, A. S., Nuhoğlu, H., & Yildiz, A. (2021). Evaluation of 4-hydroxy-2-nonenal, dityrosine and 8-hydroxy-2-deoxyguanosine Expressions in Lambs with White Muscle Disease. Firat Universitesi Saglik Bilimleri Veteriner Dergisi, 35(2), 109-113.
- Karataş, Ö., & Akçakavak, G. (2024). Evaluation of local expressions of acute phase proteins in white muscle disease in lambs by the immunohistochemical method. Revista Cientifica-Facultad de Ciencias Veterinarias, 34(1), e34313. https://doi.org/10.52973/rcfcv-e34313
- Koshimizu, J.Y., Beltrame, F.L., de Pizzol, J.P., Cerri, P.S., Caneguim, B. H., & Sasso-Cerri, E. (2013). NF-kB overexpression and decreased immunoexpression of AR in the muscular layer is related to structural damages and apoptosis in cimetidine-treated rat vas deferens. Reproductive Biology and Endocrinology, 11(1), 1-10. https://doi:10.1186/1477-7827-11-29
- Kozat, S., Altug, N., Yuksek, N., & Ozkan, C. (2011). Evaluation of the levels of homocysteine, troponin I, and nitric oxide in lambs with subclinical white muscle disease. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 17(3), 441-444. https://doi.org/10.9775/kvfd.2010.3799
- Kozat, S., Gunduz, H., Deger, Y., Mert, N., Yoruk, I., & Sel, T. (2007). Studies on serum alpha-tocopherol, selenium levels and catalase activities in lambs with white muscle disease. Bulletin-Veterinary Institute in Pulawy, 51(2), 281.
- Luna, L. (1968) Routine staining procedures: Manual of histologic staining methods of the Armed Forces Institute of Pathology. USA: Blakiston Division McGraw-Hill
- Meng, Y.C., Lou, X.L., Yang, L.Y., Li, D., & Hou, Y.Q. (2020). Role of the autophagy-related marker LC3 expression in hepatocellular carcinoma: A meta-analysis. Journal of Cancer Research and Clinical Oncology, 146, 1103-1113. https://10.1007/s00432-020-03174-1
- Mizushima, N., & Yoshimori, T. (2007). How to interpret LC3 immunoblotting. Autophagy, 3(6), 542-545. https://10.4161/auto.4600
- Nascimento, T.L., Conte, T.C., Rissato, T., Luna, M.S., Soares, A.G., Moriscot, A.S., Yamanouye, N., & Miyabara, E.H. (2019). Radicicol enhances the regeneration of skeletal muscle injured by crotoxin via decrease of NF-kB activation. Toxicon, 167, 6-9. https://10.1016/j.toxicon.2019.06.011
- Nichenko, A.S., Southern, W.M., Atuan, M., Luan, J., Peissig, K.B., Foltz, S.J., Beedle, A.M., Warren, G.L., & Call, J.A. (2016). Mitochondrial maintenance via autophagy contributes to functional skeletal muscle regeneration and remodeling. American Journal of Physiology-Cell Physiology, 311(2), C190-C200. https://10.1152/ajpcell.00066.2016
- O’Neill, B.T., Lauritzen, H.P., Hirshman, M.F., Smyth, G., Goodyear, L.J., & Kahn, C.R. (2015). Differential role of insulin/IGF-1 receptor signaling in muscle growth and glucose homeostasis. Cell Reports, 11(8), 1220-1235. https://10.1016/j.celrep.2015.04.037
- Paolini, A., Omairi, S., Mitchell, R., Vaughan, D., Matsakas, A., Vaiyapuri, S., Ricketts, T., Rubinsztein, D. C., & Patel, K. (2018). Attenuation of autophagy impacts on muscle fibre development, starvation induced stress and fibre regeneration following acute injury. Scientific Reports, 8(1), 9062. https://10.1038/s41598-018-27429-7
- Pelosi, L., Giacinti, C., Nardis, C., Borsellino, G., Rizzuto, E., Nicoletti, C., Wannenes, F., Battistini, L., Rosenthal, N., & Molinaro, M. (2007). Local expression of IGF‐1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. The FASEB Journal, 21(7), 1393-1402. https://10.1096/fj.06-7690com
- Schreck, R., Albermann, K., & Baeuerle, P. A. (1992). Nuclear factor kB: An oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radical research communications, 17(4), 221-237. https://10.3109/10715769209079515
- Sobiech, P., & Żarczyńska, K. (2020). The influence of selenium deficiency on chosen biochemical parameters and histopathological changes in muscles of goat kids. Polish Journal of Veterinary Sciences, 23(2), 267-279. https://10.24425/pjvs.2020.133642
- Sukhanov, S., Higashi, Y., Shai, S.Y., Vaughn, C., Mohler, J., Li, Y., Song, Y.H., Titterington, J., & Delafontaine, P. (2007). IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(12), 2684-2690. https://10.1161/ATVBAHA.107.156257
- Tidball, J. G., & Welc, S. S. (2015). Macrophage-derived IGF-1 is a potent coordinator of myogenesis and inflammation in regenerating muscle. Molecular Therapy, 23(7), 1134-1135. https://doi.org/10.1038/mt.2015.97
- Tonkin, J., Temmerman, L., Sampson, R. D., Gallego-Colon, E., Barberi, L., Bilbao, D., Schneider, M. D., Musarò, A., & Rosenthal, N. (2015). Monocyte/macrophage-derived IGF-1 orchestrates murine skeletal muscle regeneration and modulates autocrine polarization. Molecular Therapy, 23(7), 1189-1200. https://doi.org/10.1038/mt.2015.66
- Tunca, R., Erdoğan, H.M., Sözmen, M., Çitil, M., Devrim, A.K., Erginsoy, S., & Uzlu, E. (2009). Evaluation of cardiac troponin I and inducible nitric oxide synthase expressions in lambs with white muscle disease. Turkish Journal of Veterinary & Animal Sciences, 33(1), 53-59.
- Wang, M., Zeng, L., Su, P., Ma, L., Zhang, M., & Zhang, Y.Z. (2022). Autophagy: A multifaceted player in the fate of sperm. Human Reproduction Update, 28(2), 200-231. https://doi.org/10.1093/humupd/dmab043
- Wang, Y., Sun, Y., Yang, C., Han, B., & Wang, S. (2023). Sodium salicylate ameliorates exercise-induced muscle damage in mice by inhibiting NF-kB signaling. Journal of Orthopaedic Surgery and Research, 18(1), 967. https://10.1186/s13018-023-04433-w
- Yavuz, O. (2017). The pathological investigations on nutritional myopathy causing lamb deaths in neonatal period. Bahri Dağdaş Hayvancılık Araştırma Dergisi, 6(2), 1-8.
- Ye, F., Mathur, S., Liu, M., Borst, S. E., Walter, G. A., Sweeney, H. L., & Vandenborne, K. (2013). Overexpression of insulin‐like growth factor‐1 attenuates skeletal muscle damage and accelerates muscle regeneration and functional recovery after disuse. Experimental physiology, 98(5), 1038-1052. https://10.1113/expphysiol.2012.070722
- Yildirim, S., Ozkan, C., Huyut, Z., & Çınar, A. (2019). Detection of Se, vit. E, vit. A, MDA, 8-OHdG, and CoQ10 levels and histopathological changes in heart tissue in sheep with white muscle disease. Biological Trace Element Research, 188, 419-423. https://10.1007/s12011-018-1434-7
- Yoshida, T., & Delafontaine, P. (2020). Mechanisms of IGF-1-mediated regulation of skeletal muscle hypertrophy and atrophy. Cells, 9(9), 1970. https://10.3390/cells9091970
- Yumusak, N., Yigin, A., Polat, P., Hitit, M., & Yilmaz, R. (2018). Expression of ADAMTS-7 in myocardial dystrophy associated with white muscle disease in lambs. Polish Journal of Veterinary Sciences, 21(1). https://10.24425/119029
- Yun, H.R., Jo, Y.H., Kim, J., Shin, Y., Kim, S.S., & Choi, T.G. (2020). Roles of autophagy in oxidative stress. International Journal of Molecular Sciences, 21(9), 3289. https://doi.org/10.3390/ijms21093289
- Zinatizadeh, M.R., Schock, B., Chalbatani, G.M., Zarandi, P.K., Jalali, S.A., & Miri, S.R. (2021). The Nuclear Factor Kappa B (NF-kB) signaling in cancer development and immune diseases. Genes & Diseases, 8(3), 287-297. https://doi.org/10.1016/j.gendis.2020.06.005
Year 2024,
, 79 - 86, 22.08.2024
Gökhan Akçakavak
,
Özhan Karataş
,
Ayşenur Tural
,
Osman Dağar
,
Osman Doğan
,
Mehmet Tuzcu
References
- Akcakavak G., Kazak F., & Deveci M.Z.Y. (2023). Eucalyptol protects against cisplatin-induced liver injury in rats. Biology Bulletin , 50, 987-994. https://10.1134/s106235902360085x
- Abutarbush, S.M., & Radostits, O.M. (2003). Congenital nutritional muscular dystrophy in a beef calf. The Canadian Veterinary Journal, 44(9), 738-739.
- Al‐Shanti, N., & Stewart, C.E. (2012). Inhibitory effects of IL‐6 on IGF‐1 activity in skeletal myoblasts could be mediated by the activation of SOCS‐3. Journal of Cellular Biochemistry, 113(3), 923-933. https://doi.org/10.1002/jcb.23420
- Ataollahi, F., Mohri, M., Seifi, H.A., Pingguan-Murphy, B., Wan Abas, W.A.B., & Osman, N. A.A. (2013). Evaluation of copper concentration in subclinical cases of white muscle disease and its relationship with cardiac troponin I. PloS One, 8(2), e56163. https://doi.org/10.1371/journal.pone.0056163
- Bailes, J., & Soloviev, M. (2021). Insulin-like growth factor-1 (IGF-1) and its monitoring in medical diagnostic and in sports. Biomolecules, 11(2), 217. https://doi.org/10.3390/biom11020217
- Biswas, R., & Bagchi, A. (2016). NFkB pathway and inhibition: an overview. Computational Molecular Biology, 6(1). https://doi.org/10.5376/cmb.2016.06.0001
- Cuevas, M.J., Almar, M., García-Glez, J.C., García-López, D., De Paz, J.A., Alvear-Órdenes, I., & González-Gallego, J. (2005). Changes in oxidative stress markers and NF-κB activation induced by sprint exercise. Free Radical Research, 39(4), 431-439. https://doi.org/10.1080/10715760500072149
- Dabak, M., Karataş, F., Gül, Y., & Kizil, Ö. (2002). Investigation of selenium and vitamin e deficiency in beef cattle. Turkish Journal of Veterinary & Animal Sciences, 26(4), 741-746.
- Grounds, M.D., Radley, H.G., Gebski, B.L., Bogoyevitch, M.A., & Shavlakadze, T. (2008). Implications of cross‐talk between tumour necrosis factor and insulin‐like growth factor‐1 signalling in skeletal muscle. Clinical and Experimental Pharmacology and Physiology, 35(7), 846-851. https://doi.org/10.1111/j.1440-1681.2007.04868.x
- Gusscott, S., Jenkins, C.E., Lam, S.H., Giambra, V., Pollak, M., & Weng, A.P. (2016). IGF1R derived PI3K/AKT signaling maintains growth in a subset of human T-cell acute lymphoblastic leukemias. PloS One, 11(8), e0161158. https://doi.org/10.1371/journal.pone.0161158
- Ichimiya, T., Yamakawa, T., Hirano, T., Yokoyama, Y., Hayashi, Y., Hirayama, D., Wagatsuma, K., Itoi, T., & Nakase, H. (2020). Autophagy and autophagy-related diseases: a review. International Journal of Molecular Sciences, 21(23), 8974. https://doi.org/10.1371/journal.pone.0161158
- Karakurt, E., Karataş, Ö., Dağ, S., Beytut, E., Mendil, A. S., Nuhoğlu, H., & Yildiz, A. (2021). Evaluation of 4-hydroxy-2-nonenal, dityrosine and 8-hydroxy-2-deoxyguanosine Expressions in Lambs with White Muscle Disease. Firat Universitesi Saglik Bilimleri Veteriner Dergisi, 35(2), 109-113.
- Karataş, Ö., & Akçakavak, G. (2024). Evaluation of local expressions of acute phase proteins in white muscle disease in lambs by the immunohistochemical method. Revista Cientifica-Facultad de Ciencias Veterinarias, 34(1), e34313. https://doi.org/10.52973/rcfcv-e34313
- Koshimizu, J.Y., Beltrame, F.L., de Pizzol, J.P., Cerri, P.S., Caneguim, B. H., & Sasso-Cerri, E. (2013). NF-kB overexpression and decreased immunoexpression of AR in the muscular layer is related to structural damages and apoptosis in cimetidine-treated rat vas deferens. Reproductive Biology and Endocrinology, 11(1), 1-10. https://doi:10.1186/1477-7827-11-29
- Kozat, S., Altug, N., Yuksek, N., & Ozkan, C. (2011). Evaluation of the levels of homocysteine, troponin I, and nitric oxide in lambs with subclinical white muscle disease. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 17(3), 441-444. https://doi.org/10.9775/kvfd.2010.3799
- Kozat, S., Gunduz, H., Deger, Y., Mert, N., Yoruk, I., & Sel, T. (2007). Studies on serum alpha-tocopherol, selenium levels and catalase activities in lambs with white muscle disease. Bulletin-Veterinary Institute in Pulawy, 51(2), 281.
- Luna, L. (1968) Routine staining procedures: Manual of histologic staining methods of the Armed Forces Institute of Pathology. USA: Blakiston Division McGraw-Hill
- Meng, Y.C., Lou, X.L., Yang, L.Y., Li, D., & Hou, Y.Q. (2020). Role of the autophagy-related marker LC3 expression in hepatocellular carcinoma: A meta-analysis. Journal of Cancer Research and Clinical Oncology, 146, 1103-1113. https://10.1007/s00432-020-03174-1
- Mizushima, N., & Yoshimori, T. (2007). How to interpret LC3 immunoblotting. Autophagy, 3(6), 542-545. https://10.4161/auto.4600
- Nascimento, T.L., Conte, T.C., Rissato, T., Luna, M.S., Soares, A.G., Moriscot, A.S., Yamanouye, N., & Miyabara, E.H. (2019). Radicicol enhances the regeneration of skeletal muscle injured by crotoxin via decrease of NF-kB activation. Toxicon, 167, 6-9. https://10.1016/j.toxicon.2019.06.011
- Nichenko, A.S., Southern, W.M., Atuan, M., Luan, J., Peissig, K.B., Foltz, S.J., Beedle, A.M., Warren, G.L., & Call, J.A. (2016). Mitochondrial maintenance via autophagy contributes to functional skeletal muscle regeneration and remodeling. American Journal of Physiology-Cell Physiology, 311(2), C190-C200. https://10.1152/ajpcell.00066.2016
- O’Neill, B.T., Lauritzen, H.P., Hirshman, M.F., Smyth, G., Goodyear, L.J., & Kahn, C.R. (2015). Differential role of insulin/IGF-1 receptor signaling in muscle growth and glucose homeostasis. Cell Reports, 11(8), 1220-1235. https://10.1016/j.celrep.2015.04.037
- Paolini, A., Omairi, S., Mitchell, R., Vaughan, D., Matsakas, A., Vaiyapuri, S., Ricketts, T., Rubinsztein, D. C., & Patel, K. (2018). Attenuation of autophagy impacts on muscle fibre development, starvation induced stress and fibre regeneration following acute injury. Scientific Reports, 8(1), 9062. https://10.1038/s41598-018-27429-7
- Pelosi, L., Giacinti, C., Nardis, C., Borsellino, G., Rizzuto, E., Nicoletti, C., Wannenes, F., Battistini, L., Rosenthal, N., & Molinaro, M. (2007). Local expression of IGF‐1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. The FASEB Journal, 21(7), 1393-1402. https://10.1096/fj.06-7690com
- Schreck, R., Albermann, K., & Baeuerle, P. A. (1992). Nuclear factor kB: An oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radical research communications, 17(4), 221-237. https://10.3109/10715769209079515
- Sobiech, P., & Żarczyńska, K. (2020). The influence of selenium deficiency on chosen biochemical parameters and histopathological changes in muscles of goat kids. Polish Journal of Veterinary Sciences, 23(2), 267-279. https://10.24425/pjvs.2020.133642
- Sukhanov, S., Higashi, Y., Shai, S.Y., Vaughn, C., Mohler, J., Li, Y., Song, Y.H., Titterington, J., & Delafontaine, P. (2007). IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(12), 2684-2690. https://10.1161/ATVBAHA.107.156257
- Tidball, J. G., & Welc, S. S. (2015). Macrophage-derived IGF-1 is a potent coordinator of myogenesis and inflammation in regenerating muscle. Molecular Therapy, 23(7), 1134-1135. https://doi.org/10.1038/mt.2015.97
- Tonkin, J., Temmerman, L., Sampson, R. D., Gallego-Colon, E., Barberi, L., Bilbao, D., Schneider, M. D., Musarò, A., & Rosenthal, N. (2015). Monocyte/macrophage-derived IGF-1 orchestrates murine skeletal muscle regeneration and modulates autocrine polarization. Molecular Therapy, 23(7), 1189-1200. https://doi.org/10.1038/mt.2015.66
- Tunca, R., Erdoğan, H.M., Sözmen, M., Çitil, M., Devrim, A.K., Erginsoy, S., & Uzlu, E. (2009). Evaluation of cardiac troponin I and inducible nitric oxide synthase expressions in lambs with white muscle disease. Turkish Journal of Veterinary & Animal Sciences, 33(1), 53-59.
- Wang, M., Zeng, L., Su, P., Ma, L., Zhang, M., & Zhang, Y.Z. (2022). Autophagy: A multifaceted player in the fate of sperm. Human Reproduction Update, 28(2), 200-231. https://doi.org/10.1093/humupd/dmab043
- Wang, Y., Sun, Y., Yang, C., Han, B., & Wang, S. (2023). Sodium salicylate ameliorates exercise-induced muscle damage in mice by inhibiting NF-kB signaling. Journal of Orthopaedic Surgery and Research, 18(1), 967. https://10.1186/s13018-023-04433-w
- Yavuz, O. (2017). The pathological investigations on nutritional myopathy causing lamb deaths in neonatal period. Bahri Dağdaş Hayvancılık Araştırma Dergisi, 6(2), 1-8.
- Ye, F., Mathur, S., Liu, M., Borst, S. E., Walter, G. A., Sweeney, H. L., & Vandenborne, K. (2013). Overexpression of insulin‐like growth factor‐1 attenuates skeletal muscle damage and accelerates muscle regeneration and functional recovery after disuse. Experimental physiology, 98(5), 1038-1052. https://10.1113/expphysiol.2012.070722
- Yildirim, S., Ozkan, C., Huyut, Z., & Çınar, A. (2019). Detection of Se, vit. E, vit. A, MDA, 8-OHdG, and CoQ10 levels and histopathological changes in heart tissue in sheep with white muscle disease. Biological Trace Element Research, 188, 419-423. https://10.1007/s12011-018-1434-7
- Yoshida, T., & Delafontaine, P. (2020). Mechanisms of IGF-1-mediated regulation of skeletal muscle hypertrophy and atrophy. Cells, 9(9), 1970. https://10.3390/cells9091970
- Yumusak, N., Yigin, A., Polat, P., Hitit, M., & Yilmaz, R. (2018). Expression of ADAMTS-7 in myocardial dystrophy associated with white muscle disease in lambs. Polish Journal of Veterinary Sciences, 21(1). https://10.24425/119029
- Yun, H.R., Jo, Y.H., Kim, J., Shin, Y., Kim, S.S., & Choi, T.G. (2020). Roles of autophagy in oxidative stress. International Journal of Molecular Sciences, 21(9), 3289. https://doi.org/10.3390/ijms21093289
- Zinatizadeh, M.R., Schock, B., Chalbatani, G.M., Zarandi, P.K., Jalali, S.A., & Miri, S.R. (2021). The Nuclear Factor Kappa B (NF-kB) signaling in cancer development and immune diseases. Genes & Diseases, 8(3), 287-297. https://doi.org/10.1016/j.gendis.2020.06.005