Mitochondrial Bioenergetics of Extramammary Tissues in Lactating Dairy Cattle.

Victoria Favorit,Hailey A Parry,Patricia Villamediana,Amy L Skibiel,Andreas N Kavazis,Wendy R Hood,Kang Nian Yap

doi:10.3390/ani11092647

Victoria Favorit, Hailey A Parry + Show 5 more

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https://doi.org/10.3390/ani11092647

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Abstract

Simple SummaryThe nutrient and energy requirements of lactation are among the greatest required by any physiological process in the female mammal. The mammary gland and extramammary tissues undergo metabolic adaptations that coordinate changes in energy availability and nutrient partitioning that enable milk synthesis. Mitochondria are largely responsible for energy production in cells and their importance in milk synthesis has long been appreciated. However, mitochondrial adaptations across lactation are understudied, particularly for extramammary tissues with supporting roles in milk synthesis. Tracking mitochondrial function in dairy cattle across lactation, we found that the efficiency of energy production in the liver was elevated in the presence of fat-based substrates as the milk yield was increasing. In skeletal muscle, mitochondrial function showed little change across lactation and was not associated with milk production, suggesting that energy efficiency in this tissue is consistent regardless of the metabolic demands of lactation. A better understanding of mitochondrial bioenergetics during lactation may provide insight into the etiology of metabolic diseases during the transition period and low milk supply.Lactation is physiologically demanding, requiring increased nutrient and energy use. Mammary and extramammary tissues undergo metabolic changes for lactation. Although it has long been recognized that mitochondria play a critical role in lactation, the mitochondrial adaptations for milk synthesis in supporting tissues, such as liver and skeletal muscle are relatively understudied. In this study, we assessed the mitochondrial function in these tissues across lactation in dairy cattle. Tissue biopsies were taken at 8 ± 2 d (early, n = 11), 75 ± 4 d (peak, n = 11) and 199 ± 6 d (late, n = 11) in milk. Early lactation biopsies were harvested from one group of cows and the peak and late biopsies from a second cohort. Milk yield (MY) was recorded at each milking and milk samples were collected for composition analysis. Mitochondrial efficiency was quantified as the respiratory control ratio (RCR), comparing maximal to resting respiration rates. Liver complex II RCR was positively associated with MY. Liver ROS emission increased across lactation whereas liver antioxidant activity was similar across lactation. No change was detected in skeletal muscle RCR or ROS emission, but muscle GPx activity decreased across lactation and muscle SOD was negatively associated with MY. Muscle oxidative damage was elevated at early and late lactation. Across lactation, genes involved in mitochondrial biogenesis were upregulated in the liver. Our results indicate that during lactation, liver mitochondrial biogenesis and efficiency are increased, which is associated with greater milk yield. In contrast, the mitochondrial efficiency in skeletal muscle remains consistent across lactation, but undergoes oxidative damage, which is associated with reduced antioxidant activity.

Highlights

Lactation is a highly energetically demanding process that requires metabolic adaptations in the mammary gland and extramammary tissues [1]
We hypothesized that mitochondria in the liver and skeletal muscle would undergo functional changes in that mitochondria in the liver and skeletal muscle would undergo functional changes in respiratory capacity and oxidative status across lactation that may allow for coordinated respiratory capacity and oxidative status across lactation that may allow for coordinated metabolic changes to support shifting energy demand associated with milk synthesis
While oxidant emission increased across lactation, there was no evidence of liver oxidative damage, suggesting sufficient antioxidant activity to scavenge reactive oxygen species (ROS)

Summary

Introduction

Lactation is a highly energetically demanding process that requires metabolic adaptations in the mammary gland and extramammary tissues [1]. At the onset of lactation, dairy cattle enter a state of negative energy balance (NEB) where feed intake and nutrient availability are outpaced by the requirements of lactation and maintenance [4] This causes several physiological changes, such as mobilization of adipose tissue [5], increased hepatic glycogen mobilization and gluconeogenesis [1,6], and increased skeletal muscle proteolysis and reduced protein synthesis [7,8]. These metabolic adjustments allow tissues to shuttle nutrients to the mammary gland for milk synthesis [6,9]. Insufficient metabolic adjustment leads to health issues and metabolic disease that may disrupt milk production across the whole lactation [10]

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