Prepartal dietary energy level affects peripartal bovine blood neutrophil metabolic, antioxidant, and inflammatory gene expression

Z. Zhou, D. P. Bu, M. Vailati Riboni, M. J. Khan, D. E. Graugnard, J. Luo, Felipe Cardoso, Juan J Loor

Research output: Contribution to journalArticle

Abstract

During the dry period, cows can easily overconsume higher-grain diets, a scenario that could impair immune function during the peripartal period. Objectives were to investigate the effects of energy overfeeding on expression profile of genes associated with inflammation, lipid metabolism, and neutrophil function, in 12 multiparous Holstein cows (n = 6/dietary group) fed control [CON, 1.34 Mcal/kg of dry matter (DM)] or higher-energy (HE, 1.62 Mcal/kg of DM) diets during the last 45 d of pregnancy. Blood was collected to evaluate 43 genes in polymorphonuclear neutrophil leukocytes (PMNL) isolated at -14, 7, and 14 d relative to parturition. We detected greater expression of inflammatory-related cytokines (IL1B, STAT3, NFKB1) and eicosanoid synthesis (ALOX5AP and PLA2G4A) in HE cows than in CON cows. Around parturition, all cows had a close balance in mRNA expression of the pro-inflammatory IL1B and the anti-inflammatory IL10, with greater expression of both in cows fed HE than CON. The expression of CCL2, LEPR, TLR4, IL6, and LTC4S was undetectable. Cows in the HE group had greater expression of genes involved in PMNL adhesion, motility, migration, and phagocytosis, which was similar to expression of genes related to the pro-inflammatory cytokine. This response suggests that HE cows experienced a chronic state of inflammation. The greater expression of G6PD in HE cows could have been associated with the greater plasma insulin, which would have diverted glucose to other tissues. Cows fed the HE diet also had greater expression of transcription factors involved in metabolism of long-chain fatty acids (PPARD, RXRA), suggesting that immune cells might be predisposed to use endogenous ligands such as nonesterified fatty acids available in the circulation when glucose is in high demand for milk synthesis. The lower overall expression of SLC2A1 postpartum than prepartum supports this suggestion. Targeting interleukin-1β signaling might be of value in terms of controlling the inflammatory response around calving. The present study revealed that overfeeding cows during late pregnancy results in activation, ahead of parturition, of PMNL responses associated with stress and inflammation. These adaptations observed in PMNL did not seem to be detrimental for production.

Original languageEnglish (US)
Pages (from-to)5492-5505
Number of pages14
JournalJournal of Dairy Science
Volume98
Issue number8
DOIs
StatePublished - Aug 1 2015

Fingerprint

neutrophils
Neutrophils
Antioxidants
Gene Expression
antioxidants
cows
gene expression
cattle
blood
energy
leukocytes
inflammation
Parturition
overfeeding
Diet
Inflammation
parturition
Cytokines
cytokines
Glucose

Keywords

  • Dietary energy
  • Gene expression
  • Polymorphonuclear neutrophil

ASJC Scopus subject areas

  • Food Science
  • Animal Science and Zoology
  • Genetics

Cite this

Prepartal dietary energy level affects peripartal bovine blood neutrophil metabolic, antioxidant, and inflammatory gene expression. / Zhou, Z.; Bu, D. P.; Vailati Riboni, M.; Khan, M. J.; Graugnard, D. E.; Luo, J.; Cardoso, Felipe; Loor, Juan J.

In: Journal of Dairy Science, Vol. 98, No. 8, 01.08.2015, p. 5492-5505.

Research output: Contribution to journalArticle

Zhou, Z. ; Bu, D. P. ; Vailati Riboni, M. ; Khan, M. J. ; Graugnard, D. E. ; Luo, J. ; Cardoso, Felipe ; Loor, Juan J. / Prepartal dietary energy level affects peripartal bovine blood neutrophil metabolic, antioxidant, and inflammatory gene expression. In: Journal of Dairy Science. 2015 ; Vol. 98, No. 8. pp. 5492-5505.
@article{5cb013a085c945f2886429e4bbf08ae6,
title = "Prepartal dietary energy level affects peripartal bovine blood neutrophil metabolic, antioxidant, and inflammatory gene expression",
abstract = "During the dry period, cows can easily overconsume higher-grain diets, a scenario that could impair immune function during the peripartal period. Objectives were to investigate the effects of energy overfeeding on expression profile of genes associated with inflammation, lipid metabolism, and neutrophil function, in 12 multiparous Holstein cows (n = 6/dietary group) fed control [CON, 1.34 Mcal/kg of dry matter (DM)] or higher-energy (HE, 1.62 Mcal/kg of DM) diets during the last 45 d of pregnancy. Blood was collected to evaluate 43 genes in polymorphonuclear neutrophil leukocytes (PMNL) isolated at -14, 7, and 14 d relative to parturition. We detected greater expression of inflammatory-related cytokines (IL1B, STAT3, NFKB1) and eicosanoid synthesis (ALOX5AP and PLA2G4A) in HE cows than in CON cows. Around parturition, all cows had a close balance in mRNA expression of the pro-inflammatory IL1B and the anti-inflammatory IL10, with greater expression of both in cows fed HE than CON. The expression of CCL2, LEPR, TLR4, IL6, and LTC4S was undetectable. Cows in the HE group had greater expression of genes involved in PMNL adhesion, motility, migration, and phagocytosis, which was similar to expression of genes related to the pro-inflammatory cytokine. This response suggests that HE cows experienced a chronic state of inflammation. The greater expression of G6PD in HE cows could have been associated with the greater plasma insulin, which would have diverted glucose to other tissues. Cows fed the HE diet also had greater expression of transcription factors involved in metabolism of long-chain fatty acids (PPARD, RXRA), suggesting that immune cells might be predisposed to use endogenous ligands such as nonesterified fatty acids available in the circulation when glucose is in high demand for milk synthesis. The lower overall expression of SLC2A1 postpartum than prepartum supports this suggestion. Targeting interleukin-1β signaling might be of value in terms of controlling the inflammatory response around calving. The present study revealed that overfeeding cows during late pregnancy results in activation, ahead of parturition, of PMNL responses associated with stress and inflammation. These adaptations observed in PMNL did not seem to be detrimental for production.",
keywords = "Dietary energy, Gene expression, Polymorphonuclear neutrophil",
author = "Z. Zhou and Bu, {D. P.} and {Vailati Riboni}, M. and Khan, {M. J.} and Graugnard, {D. E.} and J. Luo and Felipe Cardoso and Loor, {Juan J}",
year = "2015",
month = "8",
day = "1",
doi = "10.3168/jds.2014-8811",
language = "English (US)",
volume = "98",
pages = "5492--5505",
journal = "Journal of Dairy Science",
issn = "0022-0302",
publisher = "Elsevier Limited",
number = "8",

}

TY - JOUR

T1 - Prepartal dietary energy level affects peripartal bovine blood neutrophil metabolic, antioxidant, and inflammatory gene expression

AU - Zhou, Z.

AU - Bu, D. P.

AU - Vailati Riboni, M.

AU - Khan, M. J.

AU - Graugnard, D. E.

AU - Luo, J.

AU - Cardoso, Felipe

AU - Loor, Juan J

PY - 2015/8/1

Y1 - 2015/8/1

N2 - During the dry period, cows can easily overconsume higher-grain diets, a scenario that could impair immune function during the peripartal period. Objectives were to investigate the effects of energy overfeeding on expression profile of genes associated with inflammation, lipid metabolism, and neutrophil function, in 12 multiparous Holstein cows (n = 6/dietary group) fed control [CON, 1.34 Mcal/kg of dry matter (DM)] or higher-energy (HE, 1.62 Mcal/kg of DM) diets during the last 45 d of pregnancy. Blood was collected to evaluate 43 genes in polymorphonuclear neutrophil leukocytes (PMNL) isolated at -14, 7, and 14 d relative to parturition. We detected greater expression of inflammatory-related cytokines (IL1B, STAT3, NFKB1) and eicosanoid synthesis (ALOX5AP and PLA2G4A) in HE cows than in CON cows. Around parturition, all cows had a close balance in mRNA expression of the pro-inflammatory IL1B and the anti-inflammatory IL10, with greater expression of both in cows fed HE than CON. The expression of CCL2, LEPR, TLR4, IL6, and LTC4S was undetectable. Cows in the HE group had greater expression of genes involved in PMNL adhesion, motility, migration, and phagocytosis, which was similar to expression of genes related to the pro-inflammatory cytokine. This response suggests that HE cows experienced a chronic state of inflammation. The greater expression of G6PD in HE cows could have been associated with the greater plasma insulin, which would have diverted glucose to other tissues. Cows fed the HE diet also had greater expression of transcription factors involved in metabolism of long-chain fatty acids (PPARD, RXRA), suggesting that immune cells might be predisposed to use endogenous ligands such as nonesterified fatty acids available in the circulation when glucose is in high demand for milk synthesis. The lower overall expression of SLC2A1 postpartum than prepartum supports this suggestion. Targeting interleukin-1β signaling might be of value in terms of controlling the inflammatory response around calving. The present study revealed that overfeeding cows during late pregnancy results in activation, ahead of parturition, of PMNL responses associated with stress and inflammation. These adaptations observed in PMNL did not seem to be detrimental for production.

AB - During the dry period, cows can easily overconsume higher-grain diets, a scenario that could impair immune function during the peripartal period. Objectives were to investigate the effects of energy overfeeding on expression profile of genes associated with inflammation, lipid metabolism, and neutrophil function, in 12 multiparous Holstein cows (n = 6/dietary group) fed control [CON, 1.34 Mcal/kg of dry matter (DM)] or higher-energy (HE, 1.62 Mcal/kg of DM) diets during the last 45 d of pregnancy. Blood was collected to evaluate 43 genes in polymorphonuclear neutrophil leukocytes (PMNL) isolated at -14, 7, and 14 d relative to parturition. We detected greater expression of inflammatory-related cytokines (IL1B, STAT3, NFKB1) and eicosanoid synthesis (ALOX5AP and PLA2G4A) in HE cows than in CON cows. Around parturition, all cows had a close balance in mRNA expression of the pro-inflammatory IL1B and the anti-inflammatory IL10, with greater expression of both in cows fed HE than CON. The expression of CCL2, LEPR, TLR4, IL6, and LTC4S was undetectable. Cows in the HE group had greater expression of genes involved in PMNL adhesion, motility, migration, and phagocytosis, which was similar to expression of genes related to the pro-inflammatory cytokine. This response suggests that HE cows experienced a chronic state of inflammation. The greater expression of G6PD in HE cows could have been associated with the greater plasma insulin, which would have diverted glucose to other tissues. Cows fed the HE diet also had greater expression of transcription factors involved in metabolism of long-chain fatty acids (PPARD, RXRA), suggesting that immune cells might be predisposed to use endogenous ligands such as nonesterified fatty acids available in the circulation when glucose is in high demand for milk synthesis. The lower overall expression of SLC2A1 postpartum than prepartum supports this suggestion. Targeting interleukin-1β signaling might be of value in terms of controlling the inflammatory response around calving. The present study revealed that overfeeding cows during late pregnancy results in activation, ahead of parturition, of PMNL responses associated with stress and inflammation. These adaptations observed in PMNL did not seem to be detrimental for production.

KW - Dietary energy

KW - Gene expression

KW - Polymorphonuclear neutrophil

UR - http://www.scopus.com/inward/record.url?scp=84937520646&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84937520646&partnerID=8YFLogxK

U2 - 10.3168/jds.2014-8811

DO - 10.3168/jds.2014-8811

M3 - Article

C2 - 26026766

AN - SCOPUS:84937520646

VL - 98

SP - 5492

EP - 5505

JO - Journal of Dairy Science

JF - Journal of Dairy Science

SN - 0022-0302

IS - 8

ER -