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Tissue-specific profiling reveals modulation of cellular and mitochondrial oxidative stress in normal- and low-birthweight piglets throughout the peri-weaning period

  • A. K. Novais (a1) (a2), Y. Martel-Kennes (a1) (a3), C. Roy (a1), K. Deschêne (a1), S. Beaulieu (a1), N. Bergeron (a1), J-P. Laforest (a3), M. Lessard (a1), J. J. Matte (a1) and J. Lapointe (a1)...

Abstract

Weaning is known to induce important nutritional and energetic stress in piglets. Low-birthweight (LBW) piglets, now frequently observed in swine production, are more likely to be affected. The weaning period is also associated with dysfunctional immune responses, uncontrolled inflammation and oxidative stress conditions that are recognized risk factors for infections and diseases. Mounting evidence indicates that mitochondria, the main cellular sources of energy in the form of adenosine 5′ triphosphate (ATP) and primary sites of reactive oxygen species production, are related to immunity, inflammation and bacterial pathogenesis. However, no information is currently available regarding the link between mitochondrial energy production and oxidative stress in weaned piglets. The objective of this study was to characterize markers of cellular and mitochondrial energy metabolism and oxidative status in both normal-birthweight (NBW) and LBW piglets throughout the peri-weaning period. To conduct the study, 30 multiparous sows were inseminated and litters were standardized to 12 piglets. All the piglets were weighted at day 1 and 120 piglets were selected and assigned to 1 of 2 experimental groups: NBW (n = 60, mean weight of 1.73 ± 0.01 kg) and LBW piglets weighing less than 1.2 kg (n = 60, 1.01 ± 0.01 kg). Then, 10 piglets from each group were selected at 14, 21 (weaning), 23, 25, 29 and 35 days of age to collect plasma and organ (liver, intestine and kidney) samples. Analysis revealed that ATP concentrations were lower in liver of piglets after weaning than during lactation (P < 0.05) thus suggesting a significant impact of weaning stress on mitochondrial energy production. Oxidative damage to DNA (8-hydroxy-2′-deoxyguanosine, 8-OHdG) and proteins (carbonyls) measured in plasma increased after weaning and this coincides with a rise in enzymatic antioxidant activity of glutathione peroxidase (GPx) and superoxide dismutase (SOD) (P < 0.05). Mitochondrial activities of both GPx and SOD are also significantly higher (P < 0.05) in kidney of piglets after weaning. Additionally, oxidative damage to macromolecules is more important in LBW piglets as measured concentrations of 8-OHdG and protein carbonyls are significantly higher (P < 0.05) in plasma and liver samples, respectively, than for NBW piglets. These results provide novel information about the nature, intensity and duration of weaning stress by revealing that weaning induces mitochondrial dysfunction and cellular oxidative stress conditions which last for at least 2 weeks and more severely impact smaller piglets.

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Agriculture and Agri-Food Canada 1993. Recommended code of practice for the care and handling of farm animals – pigs. Publ. No. 1898E. Agriculture and Agri-Food Canada, Ottawa, ON, Canada.
Barton, MD 2014. Impact of antibiotic use in the swine industry. Current Opinion in Microbiology 19, 915.
Brigelius-Flohé, R and Maiorino, M 2013. Glutathione peroxidases. Biochimica et Biophysica Acta (BBA) - General Subjects 1830, 32893303.
Bruininx, EM, van der Peet-Schwering, CM, Schrama, JW, Vereijken, PF, Vesseur, PC, Everts, H, den Hartog, LA and Beynen, AC 2001. Individually measured feed intake characteristics and growth performance of group-housed weanling pigs: effects of sex, initial body weight, and body weight distribution within groups. Journal of Animal Science 79, 301308.
Buchet, A, Belloc, C, Leblanc-Maridor, MM and Merlot, E 2017. Effects of age and weaning conditions on blood indicators of oxidative status in pigs. PLoS ONE 12, e0178487.
Campbell, JM, Crenshaw, JD and Polo, J 2013. The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19.
Cao, ST, Wang, CC, Wu, H, Zhang, QH, Jiao, LF and Hu, CH 2018. Weaning disrupts intestinal antioxidant status, impairs intestinal barrier and mitochondrial function, and triggers mitophagy in piglets. Journal of Animal Science 96, 10731083.
Damgaard, LH, Rydhmer, L, Lovendahl, P and Grandinson, K 2003. Genetic parameters for within-litter variation in piglet birth weight and change in within-litter variation during suckling. Journal of Animal Science 81, 604610.
De Vos, M, Che, L, Huygelen, V, Willemen, S, Michiels, J, Van Cruchten, S and Van Ginneken, C 2014. Nutritional interventions to prevent and rear low-birthweight piglets. Journal of Animal Physiology and Animal Nutrition (Berlin) 98, 609619.
Domenicali, M, Caraceni, P, Vendemiale, G, Grattagliano, I, Nardo, B, Dall’Agata, M, Santoni, B, Trevisani, F, Cavallari, A, Altomare, E and Bernardi, M 2001. Food deprivation exacerbates mitochondrial oxidative stress in rat liver exposed to ischemia-reperfusion injury. Journal of Nutrition 131, 105110.
Ferraris, RP and Carey, HV 2000. Intestinal transport during fasting and malnutrition. Annual Review of Nutrition 20, 195219.
Friis, C 1980. Postnatal development of the pig kidney: ultrastructure of the glomerulus and the proximal tubule. Journal of Anatomy 130, 513526.
Grattagliano, I, Vendemiale, G, Caraceni, P, Domenicali, M, Nardo, B, Cavallari, A, Trevisani, F, Bernardi, M and Altomare, E 2000. Starvation impairs antioxidant defense in fatty livers of rats fed a choline-deficient diet. Journal of Nutrition 130, 21312136.
Green, DE and Tzagoloff, A 1966. The mitochondrial electron transfer chain. Archives of Biochemistry and Biophysics 116, 293304.
Kétilim-Novais, A, Roy, C, Beaulieu, S, Martel-Kennes, Y, Lessard, M, Matte, JJ and Lapointe, J. 2018. Evidences of mitochondrial dysfunction and oxidative stress in newly weaned piglets. Journal of Animal Science 96, 491.
Lallès, JP and David, JC 2011. Fasting and refeeding modulate the expression of stress proteins along the gastrointestinal tract of weaned pigs. Journal of Animal Physiology and Animal Nutrition 95, 478488.
Lapointe, J 2014. Mitochondria as promising targets for nutritional interventions aiming to improve performance and longevity of sows. Journal of Animal Physiology and Animal Nutrition (Berlin) 98, 809821.
Lessard, M, Blais, M, Beaudoin, F, Deschene, K, Verso, LL, Bissonnette, N, Lauzon, K and Guay, F 2018. Piglet weight gain during the first two weeks of lactation influences the immune system development. Veterinary Immunology and Immunopathology 206, 2534.
López-Armada, MJ, Riveiro-Naveira, RR, Vaamonde-García, C and Valcárcel-Ares, MN 2013. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13, 106118.
Luo, Z, Zhu, W, Guo, Q, Luo, W, Zhang, J, Xu, W and Xu, J 2016. Weaning induced hepatic oxidative stress, apoptosis, and aminotransferases through MAPK signaling pathways in piglets. Oxidative Medicine and Cellular Longevity 2016, 110.
Matte, JJ, Audet, I, Ouattara, B, Bissonnette, N, Talbot, G, Lapointe, J, Guay, F, Lo Verso,  and Lessard, M 2017. Effets des sources et voies d’administration du cuivre et des vitamines A et D sur le statut postnatal de ces micronutriments chez les porcelets sous la mère. Journées Recherche Porcine, France 496974.
Moeser, AJ, Pohl, CS and Rajput, M 2017. Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Animal Nutrition 3, 313321.
Roy, C, Lavoie, M, Richard, G, Archambault, A and Lapointe, J 2016. Evidence that oxidative stress is higher in replacement gilts than in multiparous sows. Journal of Animal Physiology and Animal Nutrition (Berlin) 100, 911919.
Salin, K, Villasevil, EM, Anderson, GJ, Auer, SK, Selman, C, Hartley, RC, Mullen, W, Chinopoulos, C and Metcalfe, NB 2018. Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost. Functional Ecology 32, 21492157.
Sander, LE and Garaude, J 2018. The mitochondrial respiratory chain: a metabolic rheostat of innate immune cell-mediated antibacterial responses. Mitochondrion 41, 2836.
Sorensen, M, Sanz, A, Gómez, J, Pamplona, R, Portero-Otín, M, Gredilla, R and Barja, G 2006. Effects of fasting on oxidative stress in rat liver mitochondria. Free Radical Research 40, 339347.
Spreeuwenberg, MAM, Verdonk, JMAJ, Gaskins, HR and Verstegen, MWA 2001. Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. Journal of Nutrition 131, 15201527.
Vendemiale, G, Grattagliano, I, Caraceni, P, Caraccio, G, Domenicali, M, Dall’Agata, M, Trevisani, F, Guerrieri, F, Bernardi, M and Altomare, E 2001. Mitochondrial oxidative injury energy metabolism alteration in rat fatty liver: Effect of the nutritional status. Hepatology 33, 808815.
Weinberg, SE, Sena, LA and Chandel, NS 2015. Mitochondria in the regulation of innate and adaptive immunity. Immunity 42, 406417.
Weydert, CJ and Cullen, JJ 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nature Protocols 5, 5166.
Wijtten, PJ, van der Meulen, J and Verstegen, MW 2011. Intestinal barrier function and absorption in pigs after weaning: a review. British Journal of Nutrition 105, 967981.
Yin, J, Wu, MM, Xiao, H, Ren, WK, Duan, JL, Yang, G, Li, TJ and Yin, YL 2014. Development of an antioxidant system after early weaning in piglets. Journal of Animal Science 92, 612619.
Zelko, IN, Mariani, TJ and Folz, RJ 2002. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radical Biology and Medicine 33, 337349.
Zhang, H, Li, Y, Hou, X, Zhang, L and Wang, T 2016. Medium-chain TAG improve energy metabolism and mitochondrial biogenesis in the liver of intra-uterine growth-retarded and normal-birth-weight weanling piglets. British Journal of Nutrition 115, 15211530.
Zhang, H, Li, Y, Su, W, Ying, Z, Zhou, L, Zhang, L and Wang, T 2017. Resveratrol attenuates mitochondrial dysfunction in the liver of intrauterine growth retarded suckling piglets by improving mitochondrial biogenesis and redox status. Molecular Nutrition and Food Research 61, 112.
Zhu, LH, Zhao, KL, Chen, XL and Xu, JX 2012. Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs. Journal of Animal Science 90, 25812589.

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Tissue-specific profiling reveals modulation of cellular and mitochondrial oxidative stress in normal- and low-birthweight piglets throughout the peri-weaning period

  • A. K. Novais (a1) (a2), Y. Martel-Kennes (a1) (a3), C. Roy (a1), K. Deschêne (a1), S. Beaulieu (a1), N. Bergeron (a1), J-P. Laforest (a3), M. Lessard (a1), J. J. Matte (a1) and J. Lapointe (a1)...

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