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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

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: Jerome.lapointe@canada.ca
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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

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