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Effect of animal mixing as a stressor on biomarkers of autophagy and oxidative stress during pig muscle maturation

Published online by Cambridge University Press:  08 April 2015

A. Rubio-González
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
Y. Potes
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
D. Illán-Rodríguez
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
I. Vega-Naredo
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
V. Sierra
Affiliation:
Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Apdo. 13, 33300 Villaviciosa, Principado de Asturias, Spain
B. Caballero
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
E. Fàbrega
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Veïnat de Sies, s/n, 17121 Monells, Girona, Spain
A. Velarde
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Veïnat de Sies, s/n, 17121 Monells, Girona, Spain
A. Dalmau
Affiliation:
Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Veïnat de Sies, s/n, 17121 Monells, Girona, Spain
M. Oliván
Affiliation:
Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Apdo. 13, 33300 Villaviciosa, Principado de Asturias, Spain
A. Coto-Montes*
Affiliation:
Department of Morphology and Cellular Biology, Faculty of Medicine, University of Oviedo, Julián Clavería s/n, 33006 Oviedo, Principado de Asturias, Spain
*
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Abstract

The objective of this work was to study the postmortem evolution of potential biomarkers of autophagy (Beclin 1, LC3-II/LC3-I ratio) and oxidative stress (total antioxidant activity, TAA; superoxide dismutase activity, SOD and catalase activity, CAT) in the Longissimus dorsi muscle of entire male ((Large White×Landrace)×Duroc) pigs subjected to different management treatments that may promote stress, such as mixing unfamiliar animals at the farm and/or during transport and lairage before slaughter. During the rearing period at the farm, five animals were never mixed after the initial formation of the experimental groups (unmixed group at the farm, UF), whereas 10 animals were subjected to a common routine of being mixed with unfamiliar animals (mixed group at the farm, MF). Furthermore, two different treatments were used during the transport and lairage before slaughter: 10 pigs were not mixed (unmixed group during transport and lairage, UTL), whereas five pigs were mixed with unfamiliar animals on the lorry and during lairage (mixed group during transport and lairage, MTL). These mixing treatments were then combined into three pre-slaughter treatments – namely, UF-UTL, MF-UTL and MF-MTL. The results show that MF-UTL and MF-MTL increased significantly the muscle antioxidant defense (TAA, SOD and CAT) at short postmortem times (4 and 8 h; P<0.001), followed by an earlier depletion of the antioxidant activity at 24 h postmortem (P<0.05). We also found that mixing unfamiliar animals, both at the farm and during transport and lairage, triggers postmortem muscle autophagy, which showed an earlier activation (higher expression of Beclin 1 and LC3-II/LC3-I ratio at 4 h postmortem followed by a decreasing pattern of this ratio along first 24 h postmortem) in the muscle tissues of animals from the MF-UTL and MF-MTL groups, as an adaptive strategy of the muscle cells for counteracting induced stress. From these results, we propose that monitoring the evolution of the main biomarkers of autophagy (Beclin 1, LC3-II/LC3-I ratio) and muscle antioxidant defense (TAA, SOD, CAT) in the muscle tissue within the first 24 h postmortem may help the detection of animal stress and its potential effect on the postmortem muscle metabolism.

Type
Research Article
Copyright
© The Animal Consortium 2015 

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References

Azad, MB, Chen, Y and Gibson, SB 2009. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxidants & Redox Signaling 11, 777790.Google Scholar
Bensaad, K, Cheung, EC and Vousden, KH 2009. Modulation of intracellular ROS levels by TIGAR controls autophagy. The EMBO Journal 28, 30153026.Google Scholar
Burke, G, Fiehn, O and Moran, N 2010. Effects of facultative symbionts and heat stress on the metabolome of pea aphids. The ISME Journal 4, 242252.Google Scholar
Caballero, B and Coto-Montes, A 2012. An insight into the role of autophagy in cell responses in the aging and neurodegenerative brain. Histology and Histopathology 27, 263275.Google Scholar
Caballero, B, Sierra, V, Vega-Naredo, I, Tomás-Zapico, C, Rodríguez-Colunga, MJ, Tolivia, D, Hardeland, R, Oliván, M and Coto-Montes, A 2006. Enzimas antioxidantes en la maduración de carne de vacuno procedente de dos cabañas autóctonas asturianas. ITEA 102, 288303.Google Scholar
Caballero, B, Sierra, V, Oliván, M, Vega-Naredo, I, Tomás-Zapico, C, Álvarez-García, O, Tolivia, D, Hardeland, R, Rodríguez-Colunga, MJ and Coto-Montes, A 2007. Activity of cathepsins during beef aging related to mutations in the myostatin gene. Journal of the Science of Food and Agriculture 87, 192199.Google Scholar
Chen, Y, Azad, MB and Gibson, SB 2009. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death & Differentiation 16, 10401052.Google Scholar
Chen, Y, McMillan-Ward, E, Kong, J, Israels, SJ and Gibson, SB 2008. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death & Differentiation 15, 171182.Google Scholar
Coto-Montes, A, Boga, JA, Rosales-Corral, S, Fuentes-Broto, L, Tan, DX and Reiter, RJ 2012. Role of melatonin in the regulation of autophagy and mitophagy: a review. Molecular and Cellular Endocrinology 361, 1223.CrossRefGoogle ScholarPubMed
Coto-Montes, A, Caballero, B, Sierra, V, Vega-Naredo, I, Tomás-Zapico, C, Hardeland, R, Tolivia, D, Ureña, F and Rodríguez-Colunga, MJ 2004. Actividad de los principales enzimas antioxidantes durante el periodo de oreo de culones de la raza asturiana de los valles. ITEA 1, 4355.Google Scholar
de Gonzalo-Calvo, D, Neitzert, K, Fernández, M, Vega-Naredo, I, Caballero, B, García-Macia, M, Suárez, FM, Rodríguez-Colunga, MJ, Solano, JJ and Coto-Montes, A 2010. Differential inflammatory responses in aging and disease: TNF-alpha and IL-6 as possible biomarkers. Free Radical Biology & Medicine 49, 733737.Google Scholar
Fàbrega, E, Puigvert, X, Soler, J, Tibau, J and Dalmau, A 2013. Effect of on farm mixing and slaughter strategy on behaviour, welfare and productivity in Duroc finished entire male pigs. Applied Animal Behaviour Science 143, 3139.Google Scholar
García-Macia, M, Sierra, V, Palanca, A, Vega-Naredo, I, de Gonzalo-Calvo, D, Rodríguez-González, S, Oliván, M and Coto-Montes, A 2014. Autophagy during beef aging. Autophagy 10, 137143.Google Scholar
Gispert, M, Faucitano, L, Oliver, MA, Guardia, MD, Coll, C, Siggens, K, Harvey, K and Diestre, A 2000. A survey of pre-slaughter conditions, halothane gene frequency, and carcass and meat quality in five Spanish pig commercial abattoirs. Meat Science 55, 97106.Google Scholar
Hambrecht, E, Eissen, JJ, Newman, DJ, Smits, CH, Verstegen, MW and den Hartog, LA 2005. Preslaughter handling effects on pork quality and glycolytic potential in two muscles differing in fiber type composition. Journal of Animal Science 83, 900907.Google Scholar
Kang, R, Zeh, HJ, Lotze, MT and Tang, D 2011. The Beclin 1 network regulates autophagy and apoptosis. Cell Death & Differentiation 18, 571580.Google Scholar
Lardone, PJ, Álvarez-García, O, Carrillo-Vico, A, Vega-Naredo, I, Caballero, B, Guerrero, JM and Coto-Montes, A 2006. Inverse correlation between endogenous melatonin levels and oxidative damage in some tissues of SAM P8 mice. Journal of Pineal Research 40, 153157.Google Scholar
Li, Q, Zhang, M, Chen, YJ, Wang, YJ, Huang, F and Liu, J 2011. Oxidative damage and HSP70 expression in masseter muscle induced by psychological stress in rats. Physiology & Behavior 104, 365372.Google Scholar
Lubinsky, S and Bewley, GC 1979. Genetics of catalase in Drosophila melanogaster: rates of synthesis and degradation of the enzyme in flies aneuploid and euploid for the structural gene. Genetics 91, 723742.Google Scholar
Martin, JP Jr, Dailey, M and Sugarman, E 1987. Negative and positive assays of superoxide dismutase based on hematoxylin autoxidation. Archives of Biochemistry and Biophysics 255, 329336.Google Scholar
Pinho, RA, Andrades, ME, Oliveira, MR, Pirola, AC, Zago, MS, Silveira, PC, Dal-Pizzol, F and Moreira, JC 2006. Imbalance in SOD/CAT activities in rat skeletal muscles submitted to treadmill training exercise. Cell Biology International 30, 848853.Google Scholar
Rubinsztein, DC, Cuervo, AM, Ravikumar, B, Sarkar, S, Korolchuk, V, Kaushik, S and Klionsky, DJ 2009. In search of an “autophagomometer”. Autophagy 5, 585589.CrossRefGoogle ScholarPubMed
Scherz-Shouval, R and Elazar, Z 2011. Regulation of autophagy by ROS: physiology and pathology. Trends in Biochemical Sciences 36, 3038.Google Scholar
Schiavone, S, Jaquet, V, Trabace, L and Krause, KH 2013. Severe life stress and oxidative stress in the brain: from animal models to human pathology. Antioxidants & Redox Signaling 18, 14751490.Google Scholar
Sierra, V 2003. Estudio de catepsinas a lo largo del periodo de maduración en añojos culones y heterocigotos de la raza “Asturiana de los Valles”. Minor Thesis, Oviedo University, Oviedo, Spain.Google Scholar
Skop, V, Cahova, M, Papackova, Z, Palenickova, E, Dankova, H, Baranowski, M, Zabielski, P, Zdychova, J, Zidkova, J and Kazdova, L 2012. Autophagy-lysosomal pathway is involved in lipid degradation in rat liver. Physiological Research 61, 287297.Google Scholar
Tanida, I, Ueno, T and Kominami, E 2008. LC3 and autophagy. Methods in Molecular Biology 445, 7788.Google Scholar
Terlouw, C 2005. Stress reactions at slaughter and meat quality in pigs: genetic background and prior experience. A brief review of recent findings. Livestock Production Science 94, 125135.Google Scholar
Terlouw, EMC, Porcher, J and Fernandez, X 2005. Repeated handling of pigs during rearing. II. Effect of reactivity to humans on aggression during mixing and on meat quality. Journal of Animal Science 83, 16641672.Google Scholar
Trefan, L, Bunger, L, Bloom-Hansen, J, Rooke, JA, Salmi, B, Larzul, C, Terlouw, C and Doeschl-Wilson, A 2011. Meta-analysis of the effects of dietary vitamin E supplementation on alpha-tocopherol concentration and lipid oxidation in pork. Meat Science 87, 305314.Google Scholar
Warriss, PD, Brown, SN, Knowles, TG, Edwards, JE, Kettlewell, PJ and Guise, HJ 1998. The effect of stocking density in transit on the carcass quality and welfare of slaughter pigs: 2. Results from the analysis of blood and meat samples. Meat Science 50, 447456.Google Scholar
Warriss, PD, Brown, SN, Nute, GR, Knowles, TG, Edwards, JE, Perry, AM and Johnson, SP 1995. Potential interactions between the effects of preslaughter stress and post-mortem electrical stimulation of the carcasses on meat quality in pigs. Meat Science 41, 5568.Google Scholar