A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle

<b>Objectives</b>: This study investigated the long-term effects of maternal undernutrition on overall muscle metabolism, growth performance, and muscle characteristics in postnatal offspring of Wagyu (Japanese Black) cattle. <b>Methods</b>: Wagyu cows were divided into nutri...

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Main Authors: Daichi Nishino, Taketo Haginouchi, Takeshi Shimogiri, Susumu Muroya, Kenji Kawabata, Saki Urasoko, Ichiro Oshima, Shinobu Yasuo, Takafumi Gotoh
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Language:English
Published: MDPI AG 2025-03-01
Series:Metabolites
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Online Access:https://www.mdpi.com/2218-1989/15/3/209
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author Daichi Nishino
Taketo Haginouchi
Takeshi Shimogiri
Susumu Muroya
Kenji Kawabata
Saki Urasoko
Ichiro Oshima
Shinobu Yasuo
Takafumi Gotoh
author_facet Daichi Nishino
Taketo Haginouchi
Takeshi Shimogiri
Susumu Muroya
Kenji Kawabata
Saki Urasoko
Ichiro Oshima
Shinobu Yasuo
Takafumi Gotoh
author_sort Daichi Nishino
collection DOAJ
description <b>Objectives</b>: This study investigated the long-term effects of maternal undernutrition on overall muscle metabolism, growth performance, and muscle characteristics in postnatal offspring of Wagyu (Japanese Black) cattle. <b>Methods</b>: Wagyu cows were divided into nutrient-adequate (control, CNT; <i>n</i> = 4, 120% of requirements) and nutrient-restricted groups (NR; <i>n</i> = 4; 60% of requirements), and treated from day 35 of gestation until parturition. Diets were delivered on the basis of crude protein requirements, meeting 100% and 80% of dry matter requirements in CNT and NR groups, respectively. All offspring were provided with the same diet from birth to 300 days of age (d). Longissimus thoracis muscle (LM) samples were collected from the postnatal offspring. <b>Results</b>: The NR offspring had lower birth body weight, but their body weight caught up before weaning. These offspring showed enhanced efficiency in nutrient utilization during the post-weaning growth period. Comprehensive analyses of metabolites and transcripts revealed the accumulation of proteinogenic amino acid, asparagine, in NR offspring LM at 300 d, while the abundance of nicotinamide adenine dinucleotide (NADH) and succinate were reduced. These changes were accompanied by decreased gene expression of nicotinamide phosphoribosyltransferase (<i>NAMPT</i>), NADH: ubiquinone oxidoreductase subunit A12 (<i>NDUFA12</i>), and NADH dehydrogenase subunit 5 (<i>ND5</i>), which are essential for mitochondrial energy production. Additionally, NR offspring LM exhibited decreased abundance of neurotransmitter, along with a higher proportion of slow-oxidative myofibers and a lower proportion of fast-oxidative myofibers at 300 d. <b>Conclusions</b>: Offspring from nutrient-restricted cows might suppress muscle energy production, primarily in the mitochondria, and conserve energy expenditure for muscle protein synthesis. These findings suggest that maternal undernutrition programs a thrifty metabolism in offspring muscle, with long-term effects.
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spelling doaj-art-1f293f3eece447b29aa9518b6f1875552025-08-20T03:43:27ZengMDPI AGMetabolites2218-19892025-03-0115320910.3390/metabo15030209A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef CattleDaichi Nishino0Taketo Haginouchi1Takeshi Shimogiri2Susumu Muroya3Kenji Kawabata4Saki Urasoko5Ichiro Oshima6Shinobu Yasuo7Takafumi Gotoh8Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, JapanField Science Center for Northern Biosphere, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo 060-0811, JapanThe United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-24 Korimoto, Kagoshima 890-8580, JapanThe United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-24 Korimoto, Kagoshima 890-8580, JapanLivestock Experiment Station, Kagoshima Prefectural Institute for Agricultural Development, 2440 Kokubuuenodan, Kirishima 899-4461, JapanLivestock Experiment Station, Kagoshima Prefectural Institute for Agricultural Development, 2440 Kokubuuenodan, Kirishima 899-4461, JapanThe United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-24 Korimoto, Kagoshima 890-8580, JapanGraduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, JapanGraduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, Japan<b>Objectives</b>: This study investigated the long-term effects of maternal undernutrition on overall muscle metabolism, growth performance, and muscle characteristics in postnatal offspring of Wagyu (Japanese Black) cattle. <b>Methods</b>: Wagyu cows were divided into nutrient-adequate (control, CNT; <i>n</i> = 4, 120% of requirements) and nutrient-restricted groups (NR; <i>n</i> = 4; 60% of requirements), and treated from day 35 of gestation until parturition. Diets were delivered on the basis of crude protein requirements, meeting 100% and 80% of dry matter requirements in CNT and NR groups, respectively. All offspring were provided with the same diet from birth to 300 days of age (d). Longissimus thoracis muscle (LM) samples were collected from the postnatal offspring. <b>Results</b>: The NR offspring had lower birth body weight, but their body weight caught up before weaning. These offspring showed enhanced efficiency in nutrient utilization during the post-weaning growth period. Comprehensive analyses of metabolites and transcripts revealed the accumulation of proteinogenic amino acid, asparagine, in NR offspring LM at 300 d, while the abundance of nicotinamide adenine dinucleotide (NADH) and succinate were reduced. These changes were accompanied by decreased gene expression of nicotinamide phosphoribosyltransferase (<i>NAMPT</i>), NADH: ubiquinone oxidoreductase subunit A12 (<i>NDUFA12</i>), and NADH dehydrogenase subunit 5 (<i>ND5</i>), which are essential for mitochondrial energy production. Additionally, NR offspring LM exhibited decreased abundance of neurotransmitter, along with a higher proportion of slow-oxidative myofibers and a lower proportion of fast-oxidative myofibers at 300 d. <b>Conclusions</b>: Offspring from nutrient-restricted cows might suppress muscle energy production, primarily in the mitochondria, and conserve energy expenditure for muscle protein synthesis. These findings suggest that maternal undernutrition programs a thrifty metabolism in offspring muscle, with long-term effects.https://www.mdpi.com/2218-1989/15/3/209Wagyu cattlebeef cattlematernal nutritionundernutritionfetal programmingenergy metabolism
spellingShingle Daichi Nishino
Taketo Haginouchi
Takeshi Shimogiri
Susumu Muroya
Kenji Kawabata
Saki Urasoko
Ichiro Oshima
Shinobu Yasuo
Takafumi Gotoh
A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
Metabolites
Wagyu cattle
beef cattle
maternal nutrition
undernutrition
fetal programming
energy metabolism
title A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
title_full A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
title_fullStr A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
title_full_unstemmed A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
title_short A Pilot Study: Maternal Undernutrition Programs Energy Metabolism and Alters Metabolic Profile and Morphological Characteristics of Skeletal Muscle in Postnatal Beef Cattle
title_sort pilot study maternal undernutrition programs energy metabolism and alters metabolic profile and morphological characteristics of skeletal muscle in postnatal beef cattle
topic Wagyu cattle
beef cattle
maternal nutrition
undernutrition
fetal programming
energy metabolism
url https://www.mdpi.com/2218-1989/15/3/209
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