Differential hepatic mitochondrial function and gluconeogenic gene expression in 2 Holstein strains in a pasture-based system

Abstract

The objective of this study was to assess hepatic ATP synthesis in Holstein cows of North American and New Zealand origins and the gluconeogenic pathway, one of the pathways with the highest ATP demands in the ruminant liver. Autumn-calving Holstein cows of New Zealand and North American origins were managed in a pasture-based system with supplementation of concentrate that represented approximately 33% of the predicted dry matter intake during 2017, 2018, and 2019, and hepatic biopsies were taken during mid-lactation at 174 ± 23 days in milk. Cows of both strains produced similar levels of solids-corrected milk, and no differences in body condition score were found. Plasma glucose concentrations were higher for cows of New Zealand versus North American origin. Hepatic mitochondrial function evaluated measuring oxygen consumption rates showed that mitochondrial parameters related to ATP synthesis and maximum respiratory rate were increased for cows of New Zealand compared with North American origin. However, hepatic gene expression of pyruvate carboxylase, phosphoenolpyruvate carboxykinase, and pyruvate dehydrogenase kinase was increased in North American compared with New Zealand cows. These results altogether suggest an increased activity of the tricarboxylic cycle in New Zealand cows, leading to increased ATP synthesis, whereas North American cows pull tricarboxylic cycle intermediates toward gluconeogenesis. The fact that this occurs during mid-lactation could account for the increased persistency of North American cows, especially in a pasture-based system. In addition, we observed an augmented mitochondrial density in New Zealand cows, which could be related to feed efficiency mechanisms. In sum, our results contribute to the elucidation of hepatic molecular mechanisms in dairy cows in production systems with higher inclusion of pastures.

Hepatic metabolism of grazing cows of two Holstein strains under two feeding strategies with different levels of pasture inclusion

“…The distinct adaptability to pasture-based systems in cows of the NAH and NZH strains has been widely reported, as authors have shown that cows of the NAH fail to maintain BCS and BW in pasture-based systems [ 5 , 16 ]. Previous reports have suggested that NAH cows have a higher maintenance requirement [ 14 ], greater uncoupling of the somatotropic axis which accounts for a greater proportion of nutrients partitioning toward milk yield at the expense of body reserves [ 17 ] and increased gluconeogenesis in detriment of TCA cycling [ 18 ]. Indeed, mitochondria are at the crossroads of energy metabolism as they convert energy from nutrients to utilizable energy for cellular functions [ 10 ] and the liver in particular is a highly metabolic organ involved in service functions and represents an important proportion of basal energy expenditure [ 51 ].…”

“…It has been well established that the hepatocyte increases its size to meet physiological demands [ 52 ], in fact when comparing NAH vs . NZH cows in the MaxP feeding strategy during late mid-lactation, NZH cows showed increased hepatic mitochondrial density [ 18 ]. This evidence suggests that although NZH and NAH cows have similar levels of NEB markers, their hepatic intermediary metabolism adapts differently.…”

“…Indeed, the NZH strain has shown to be more suitable for grazing systems than the NAH strain since it maintains higher average body condition score, body weight and energy and feeding efficiency [ 5 , 15 , 16 ].Alongside, from a metabolic standpoint, the NAH strain presents uncoupling of the somatotropic axis during early lactation while the NZH strain maintains homeostatic levels of plasma growth hormone and insulin like growth factor-I [ 17 ]. Also, a recent publication from our group showed that cows of the NZH strain had increased mitochondrial function when compared to cows of the NAH strain in a pasture-based system during late mid-lactation and this was explained by an upregulation of the gluconeogenic pathway in cows of the NAH strain, since several metabolites are pulled toward gluconeogenesis instead of being oxidized to CO 2 [ 18 ]. Herein, we hypothesize that NZH cows will present improved mitochondrial function, lower levels of mitochondrial acetylation and oxidative metabolism in liver than NAH cows only in the feeding strategy with higher proportions of grazed pasture.…”