Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T10:49:45.138Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  25 November 2019

A. K. Novais ,
Y. Martel-Kennes ,
C. Roy ,
K. Deschêne ,
S. Beaulieu ,
N. Bergeron ,
J-P. Laforest ,
M. Lessard ,
J. J. Matte  and
J. Lapointe Open the ORCID record for J. Lapointe [Opens in a new window]
A. K. Novais
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada Department of Animal Science, Universidade Estadual de Londrina, Londrina, Paraná 86057-970, Brazil
Y. Martel-Kennes
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada Département des Sciences Animales, Université Laval, Ville de Québec, Québec G1V 0A6, Canada
C. Roy
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
K. Deschêne
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
S. Beaulieu
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
N. Bergeron
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
J-P. Laforest
Affiliation:
Département des Sciences Animales, Université Laval, Ville de Québec, Québec G1V 0A6, Canada
M. Lessard
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
J. J. Matte
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
J. Lapointe*
Affiliation:
Agriculture and Agri-Food Canada, Sherbrooke Research and Development Centre, 2000 College St., Sherbrooke, Quebec J1M 0C8, Canada
*
†E-mail: [email protected]
Get access

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.

Keywords

mitochondriaenergymetabolismswineantioxidants
Type
Research Article
Information
animal , Volume 14 , Issue 5 , May 2020 , pp. 1014 - 1024
Copyright
© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.Google Scholar
Barton, MD 2014. Impact of antibiotic use in the swine industry. Current Opinion in Microbiology 19, 9–15.10.1016/j.mib.2014.05.017CrossRefGoogle ScholarPubMed
Brigelius-Flohé, R and Maiorino, M 2013. Glutathione peroxidases. Biochimica et Biophysica Acta (BBA) - General Subjects 1830, 3289–3303.CrossRefGoogle ScholarPubMed
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, 301–308.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Campbell, JM, Crenshaw, JD and Polo, J 2013. The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19.CrossRefGoogle ScholarPubMed
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, 1073–1083.CrossRefGoogle ScholarPubMed
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, 604–610.CrossRefGoogle ScholarPubMed
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, 609–619.CrossRefGoogle ScholarPubMed
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, 105–110.CrossRefGoogle ScholarPubMed
Ferraris, RP and Carey, HV 2000. Intestinal transport during fasting and malnutrition. Annual Review of Nutrition 20, 195–219.CrossRefGoogle ScholarPubMed
Friis, C 1980. Postnatal development of the pig kidney: ultrastructure of the glomerulus and the proximal tubule. Journal of Anatomy 130, 513–526.Google ScholarPubMed
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, 2131–2136.CrossRefGoogle ScholarPubMed
Green, DE and Tzagoloff, A 1966. The mitochondrial electron transfer chain. Archives of Biochemistry and Biophysics 116, 293–304.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 478–488.CrossRefGoogle ScholarPubMed
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, 809–821.CrossRefGoogle ScholarPubMed
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, 25–34.CrossRefGoogle ScholarPubMed
López-Armada, MJ, Riveiro-Naveira, RR, Vaamonde-García, C and Valcárcel-Ares, MN 2013. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13, 106–118.CrossRefGoogle ScholarPubMed
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, 1–10.Google ScholarPubMed
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 49, 69–74.Google Scholar
Moeser, AJ, Pohl, CS and Rajput, M 2017. Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Animal Nutrition 3, 313–321.CrossRefGoogle ScholarPubMed
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, 911–919.CrossRefGoogle ScholarPubMed
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, 2149–2157.CrossRefGoogle ScholarPubMed
Sander, LE and Garaude, J 2018. The mitochondrial respiratory chain: a metabolic rheostat of innate immune cell-mediated antibacterial responses. Mitochondrion 41, 28–36.CrossRefGoogle ScholarPubMed
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, 339–347.CrossRefGoogle ScholarPubMed
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, 1520–1527.CrossRefGoogle ScholarPubMed
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, 808–815.CrossRefGoogle ScholarPubMed
Weinberg, SE, Sena, LA and Chandel, NS 2015. Mitochondria in the regulation of innate and adaptive immunity. Immunity 42, 406–417.CrossRefGoogle ScholarPubMed
Weydert, CJ and Cullen, JJ 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nature Protocols 5, 51–66.CrossRefGoogle Scholar
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, 967–981.CrossRefGoogle ScholarPubMed
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, 612–619.CrossRefGoogle ScholarPubMed
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, 337–349.CrossRefGoogle Scholar
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, 1521–1530.CrossRefGoogle ScholarPubMed
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, 1–12.CrossRefGoogle ScholarPubMed
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, 2581–2589.CrossRefGoogle Scholar
Supplementary material: File

Novais et al. supplementary material

Tables S1-S3

Download Novais et al. supplementary material(File)
File 26.7 KB