Maternal Overnutrition in Beef Cattle: Effects on Fetal Programming, Metabolic Health, and Postnatal Outcomes
Simple Summary
Abstract
1. Introduction
2. Fetal Development Under MO
2.1. Critical Windows in Fetal Development
2.2. Importance of Placental Development
2.3. Nutritional Programming and Muscle Development
2.4. Developmental Programming and Long-Term Growth
3. Effect of Maternal Feed Supplementation on Maternal Physiology
3.1. Impact on Body Weight, Body Condition, and Energy Balance
3.2. Effects on Reproductive Function and Metabolic Parameters
3.3. Long-Term Economic and Production Benefits
4. Epigenetics and Nutritional Interventions
4.1. Epigenetic Mechanisms and Metabolic Imprinting
4.1.1. DNA Methylation
4.1.2. Histone Modifications
4.1.3. Non-Coding RNAs (miRNAs and lncRNAs)
4.2. Transgenerational and Multigenerational Epigenetic Effects
5. Impact of MO on Fetal Gene Expression
5.1. Impacts on Muscle Development
5.2. Regulation of Adipogenesis and Fat Deposition
5.3. Fibrogenesis and Connective Tissue Formation
5.4. Energy Metabolism
5.5. Long-Term Consequences of MO-Induced Fetal Gene Expression
Gene(s) | Function | Nutritional Status | Stage | Expression Change | Impact | References |
---|---|---|---|---|---|---|
LOC107131843 | Insulin receptor signaling (Akt3-mTOR pathway) | Prot. Sup. | Postnatal | ↑ | Promotes muscle hypertrophy | [111] |
KRT8, KRT18, KRT19 | Apoptosis regulation and muscle fiber structure | ↑ | Balances protein synthesis and degradation, promoting muscle development | |||
CLSTN3 | Cell adhesion | ↑ | Enhances muscle integrity | |||
ANGPTL4 | Lipid metabolism | ↑ | Supports lipid metabolism and energy regulation | |||
KCNH3 | Potassium ion transport | ↑ | Enhances muscle function | |||
ENSBTAG00000055143 | Mitochondrial energy metabolism | ↑ | Improves energy efficiency and muscle development | |||
AK9 | Nucleobase metabolism | ↓ | Reduces metabolic activity in muscle | |||
LOC510904 | AA transport | ↓ | Limits nutrient transport | |||
CEACAM19, ENSBTAG00000032057 | ATP synthesis and energy production | ↓ | Alters mitochondrial function | |||
ALKBH1 | DNA methylation (N6-methyladenine regulation) | ↑ | Promotes muscle proliferation while reducing differentiation | |||
MYF5 | Myogenic regulatory factor (muscle fiber formation) | Energy + Prot. Sup. PUFA/MPN | Postnatal | ↓ | Reduces muscle fiber differentiation. 2- PUFA supplementation may preserve muscle development by maintaining MYF5 expression | [94,115] |
MYH7 | Muscle fiber development | PUFA | Postnatal | ↑ | Increased muscle development from birth to weaning | [117] |
Zfp423 | Regulates early preadipocyte commitment | MO, PUFA, RUP | Fetal and postnatal | ↑↓ | Promotes adipogenesis and fat deposition via PPARγ activation | [13,54,117] |
PPARG | Adipogenesis and lipid metabolism | MO, MPN, PUFA, RUP | Fetal and postnatal | ↑- | Increases fat accumulation, marbling, and adipogenic programming no significant difference (PUFA) | [13,54,94,117,120,124,140] |
AGRP | Appetite regulation (appetite-stimulating) | A high-protein or nutrient-rich diet | Postnatal | ↑ | Increases appetite and DMI | [141] |
C/EBPα | Adipocyte differentiation and fat deposition | MO, MPN, PUFA, RUP, low-energy diet | Fetal and postnatal | ↑ | 1. Increases adipogenesis and fat accumulation in muscle through interaction with PPARγ (MO). 2. Enhances adipogenic programming and fat deposition during fetal development (MPN). | [13,54,94,117,120,124,129] |
PSPH, PSAT1, PHGDH | Enzymes in serine biosynthesis pathway | Met Sup. | Postnatal | ↓ | Reduced serine synthesis and AA metabolism | [115] |
SLC7A1, SLC7A5, SLC3A2 | AA transporters | ↓ | Limited AA transport and reduced mTOR signaling | |||
CBS | Enzyme in the transsulfuration pathway | ↓ | Decreased transsulfuration pathway; potential methionine remethylation | |||
DNMT3a | DNA methyltransferase (de novo methylation) | Energy + Prot. Sup. | ↓ | Possible effects on epigenetic regulation and gene expression | ||
TGFBR2, SMAD2, SMAD4 | TGF-β signaling pathway | ↓ | Suppression of muscle growth, increased fibroblast activity | |||
Wnt-related (e.g., FZD7, APC) | Wnt/β-catenin pathway | ↓ | Reduced myogenesis, favoring adipogenesis | |||
MTHFD2, ALDH1L2, MTHFD1L | Mitochondrial folate metabolism | ↓ | Impacts one-carbon metabolism and methyl donor availability | |||
β-catenin | Suppresses adipogenesis (Wnt/β-catenin pathway) | MO/Met Sup. | Fetal and postnatal | ↓ | Favors adipocyte differentiation over myogenesis | [13,94,113] |
PCDH19 | Protocadherin; involved in immunity | Low maternal diet | Postnatal | ↑ | Regulates energy metabolism and growth, linked with feed efficiency and metabolic weight | [134] |
GSTM1/2 | Glutathione S-transferase; antioxidant activity | Prot. En. Sup. | ↑ | Regulates oxidative stress and detoxification | ||
CAST | Calpastatin; inhibits calpain enzymes | Prot. En. Sup | ↑ | Regulates muscle protein degradation, impacting meat quality | ||
μ-Calpain | Protein turnover and muscle fusion | HE diet | Fetal | ↑ | May indicate enhanced myoblast fusion and larger muscle fiber potential | [129] |
PAX3, GLI | Essential for skeletal myogenesis | Met Sup. | Postnatal | ↓ | Reduces myocyte development | [113] |
TGF-β | Regulates fibrogenesis and collagen deposition | MO, MPN, High-RUP diet | Fetal and postnatal | ↑ | Increases muscle fibrosis and collagen cross-linking | [13,54,94] |
COL3A1 | Collagen type III; fibrosis | MO | Fetal | ↑ | Promotes connective tissue formation and fibrosis | [13] |
FABP4 | Fatty acid metabolism | MPN | Postnatal | ↑ | Supports fat accumulation during fetal development | [117,124] |
FASN | Fatty acid synthesis | MPN, PUFA | Fetal and postnatal | ↑ | Increases marbling in muscle | [94,117,124,140] |
IGF2R | Insulin-like growth factor 2 receptor, regulates cell differentiation and apoptosis | HSD | Postnatal | ↑ | Facilitates IGF2 degradation to prevent fetal overgrowth | [95] |
MEG8 | Non-coding RNA associated with muscle growth | ↑ | Possibly involved in fetal programming and muscle development | |||
DNMT3a | DNA methyltransferase, involved in epigenetic regulation | ↑ | Modulates DNA methylation and epigenetic programming | |||
PDGFRα | Marker of fibro-adipogenic progenitor cells | High-RUP diet | Postnatal | ↑ | Enhances adipogenic and fibrogenic potential | [54] |
SCD | Stearoyl-CoA desaturase, regulates fat composition | MPN, PUFA | Postnatal | ↑↓ | Increases (MPN) and decreases (PUFA) marbling in muscle | [94,117,124] |
PPARGC1A | Mitochondrial biogenesis and energy metabolism | MO | Postnatal | ↓ | Reduces muscle oxidative capacity, suppresses energy metabolism | [116] |
miR-103, miR-107 | Regulate lipid metabolism (target CAV1) | MPN | Postnatal | ↑ | Modulate insulin sensitivity | [124] |
miR-27a/b, miR-130a | Suppress adipogenesis (target PPARG, C/EBPα) | ↓ | Facilitate fat accumulation | |||
miR-143 | Promotes adipocyte differentiation (target DLK1) | ↑ | Enhances adipogenesis | |||
ADCY6 | Converts ATP to cAMP | MO | Postnatal | ↑ | Adapts energy metabolism | [116] |
COL1A1, COL1A2 | Collagen organization and cross-linking | MO/Met Sup. | Postnatal | ↑ | Promotes fibrosis and connective tissue development | [113,135] |
HSPA6, HSPA1A | Cellular stress response | MO | Postnatal | ↑ | Protects cells from metabolic stress | [135] |
NME1, MAPK4 | Cell proliferation and differentiation | LPN | Postnatal | ↓ | Reduces muscle development | [94] |
SCUBE1, CARD14 | Immune signaling and inflammation | ↑ | Induces inflammatory response | |||
PREF-1 | Inhibits adipocyte differentiation | HE maternal diet | Fetal | ↑ | Delays adipogenesis | [129] |
IGF-II | Promotes muscle growth | Tendency ↑ | Promotes fetal muscle development, though without observable fiber differences | |||
AGR | Appetite stimulation | Periconception (HPeri/LPost) | Postnatal | ↑ | Increases feed intake | [141] |
FGF2, PPARα | Regulate muscle hypertrophy and metabolism | Mid-gestation supplementation | Postnatal | ↑ | Enhances muscle growth and energy metabolism | [120] |
MYF3, MYF6, MYH1, MYH3 | Muscle structure and contraction | Se Sup. (TR1/TR3) | Postnatal | ↓ (TR1)/↑ (TR3) | Affects muscle development depending on trimester | [121] |
MYOG | Myogenin; regulates muscle differentiation | Maternal PS/Se Sup., Low-energy diet | Fetal and postnatal | ↑ | Promotes muscle fiber differentiation and regulates hypertrophy and atrophy | [121,129,134] |
ABCA6, ABCB11, SLC27A6, SLC2A2, SLC2A4 | Nutrient transport and metabolism | Vit/Min Sup. | Fetal | ↑ | Enhances metabolic activity | [140] |
MT1A, MT1E, MT2A | Metallothioneins involved in metal ion binding | ↑ | Enhances metal ion homeostasis | |||
PPARD | Regulates fatty acid oxidation | ↓ | Reduces fat oxidation | |||
FADS2, LPL | Lipid synthesis and metabolism | ↓ | Reduces fat storage |
6. Effect of Maternal Nutrition During Pregnancy on Postnatal Outcomes and Production Traits
6.1. Growth Performance and Development
6.2. Immune Function and Health
6.3. Reproductive Development
6.4. Carcass Traits and Meat Quality
6.5. Metabolic and Physiological Development
6.6. Influence of Fetal Sex on MO Outcomes
6.7. Impact of Maternal Nutrition on Offspring Rumen Microbiome and Gut Flora
6.8. Controversies and Breed-Specific Responses
7. OMICs Integration Reveals Metabolic Programming Under MO
8. Nutritional Strategies and Recommendations
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AA | Amino acid |
AAC | Organic-complexed trace minerals |
ADCY6 | Adenylyl cyclase 6 |
ADG | Average daily gain |
AGR | Agouti-related peptide |
AMPK | AMP-activated protein kinase |
APC | Adenomatous polyposis coli (Wnt co-factor) |
BAT | Brown adipose tissue |
BCS | Body-condition score |
BRD | Bovine respiratory disease |
BW | Body weight |
CBS | Cystathionine β-synthase |
CP | Crude protein |
CPT2 | Carnitine-palmitoyl-transferase 2 |
DMI | Dry-matter intake |
ECM | Extracellular matrix |
FASN | Fatty-acid synthase |
FCR | Feed-conversion ratio |
FGF2 | Fibroblast growth factor 2 |
FN1 | Fibronectin 1 |
FOXO1/3 | Forkhead box O1/O3 |
HCW | Hot-carcass weight |
HE | High-energy (diet) |
HFAT | High-fat bakery-waste diet |
HPN | High plane of nutrition |
HSD | High-starch diet |
IgG | Immunoglobulin G |
IUGR | Intrauterine growth retardation |
JAK-STAT | Janus-kinase/signal-transducer-and-activator-of-transcription pathway |
lncRNA | Long non-coding RNA |
LFAT | Low-fat bakery-waste diet |
LOX | Lysyl oxidase |
LPN | Low plane of nutrition |
ME | Metabolizable energy |
miRNA | Micro-RNA |
MO | Maternal overnutrition |
mTOR | Mechanistic target of rapamycin |
MPN | Medium plane of nutrition |
NRC | National Research Council |
OCM | One-carbon metabolites |
PUFA | Poly-unsaturated fatty acid |
RFI | Residual feed intake |
RPF | Rumen-protected fat |
RPM | Rumen-protected methionine |
RUP | Rumen-undegradable protein |
SCFA | Short-chain fatty acid |
Se | Selenium |
TDN | Total digestible nutrients |
VTM | Vitamin–mineral supplement |
WAT | White adipose tissue |
WGCNA | Weighted gene-co-expression network analysis |
ZFP423 | Zinc-finger protein 423 |
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Topic | Positive (Benefit Reported) | Neutral/Negative (no Benefit or Opposite) | Possible Reason(s) | Breed(s) Concerned |
---|---|---|---|---|
Late-gestation protein + energy supplementation | ↑ birth and weaning BW, heavier carcasses (150% req.; [68,80]) | No change in pregnancy rate despite ↑ BCS [59,61,67] Similar calf BW and carcass traits vs. control [5,13,61,74,118] | Gestational timing, dam BCS, post-weaning management | Multiple Bos taurus breeds; Hanwoo shows no benefit |
Mid-gestation protein supplementation | ↑ birth and weaning BW, larger muscle fibers [64] | Costa et al. [142]: mid-gestation restriction ↓ muscle fibers even at 450 d; Lawson [69]: added protein/methionine late G → minimal early-life effects | Level (restriction vs. surplus); genetic line | Angus-cross, Nellore, Wagyu |
RUP | ↑ ADG and final BW of dams [54] | No definitive fertility gain [54] | Source of protein vs. energy balance | Angus × Hereford cows |
RPM (periconception) | ↑ calf BW, ↑ post-weaning ADG [66] | Did not improve pregnancy outcomes in dams | May target fetal metabolism more than dam fertility | Angus × Simmental |
HE late gestation diets | ↑ calf birth BW, ↑ neonatal immune/antioxidant markers [138] | HE diet may ↓ colostral IgG [174]; other HE trials → no long-term growth advantage [13,68] | Excess energy depresses IgG; breed tolerance | Bos taurus beef breeds |
PUFA supplementation (late gestation) | ↑ steers’ ADG and HCW [160] | No response in heifer contemporaries [160] | Sex-specific adipogenic programming | Angus/Angus-cross |
Trace-mineral (Zn, Cu, Mn) supplementation | Chelated form ↓ haptoglobin, ↑ colostrum yield and calf immunity [146,147] | No effect on marbling or REA regardless of mineral source [147] | Immune vs. carcass pathways distinct | Red Angus, Angus, Hereford mixes |
Breed-specific MO response | Angus, marbling ↑ with moderate MO, tenderness mostly retained [75] and greater intramuscular fat deposition [124] | Hanwoo and Wagyu—already high marbling; MO ↑ collagen genes (COL3A1, FN1) → ↓ tenderness [12,116] | Genetic propensity for fat vs. collagen synthesis | Hanwoo, Wagyu, Angus, Angus × Simmental |
Bos indicus vs. Bos taurus | Nellore bulls: full programming ↑ immune-related hepatic networks (PTPRC, SLC12A8) and ↑ papillae count in rumen [55,171] | Zebu multigenerational study: historic gestational environment explains up to 52.9% variance in repro traits [105] but growth responses less pronounced than in Bos taurus trials | Differences in placental efficiency, heat tolerance, fat partitioning | Nellore, Zebu |
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Shokrollahi, B.; Park, M.; Jang, G.-S.; Jin, S.; Moon, S.-J.; Um, K.-H.; Jang, S.-S.; Baek, Y.-C. Maternal Overnutrition in Beef Cattle: Effects on Fetal Programming, Metabolic Health, and Postnatal Outcomes. Biology 2025, 14, 645. https://doi.org/10.3390/biology14060645
Shokrollahi B, Park M, Jang G-S, Jin S, Moon S-J, Um K-H, Jang S-S, Baek Y-C. Maternal Overnutrition in Beef Cattle: Effects on Fetal Programming, Metabolic Health, and Postnatal Outcomes. Biology. 2025; 14(6):645. https://doi.org/10.3390/biology14060645
Chicago/Turabian StyleShokrollahi, Borhan, Myungsun Park, Gi-Suk Jang, Shil Jin, Sung-Jin Moon, Kyung-Hwan Um, Sun-Sik Jang, and Youl-Chang Baek. 2025. "Maternal Overnutrition in Beef Cattle: Effects on Fetal Programming, Metabolic Health, and Postnatal Outcomes" Biology 14, no. 6: 645. https://doi.org/10.3390/biology14060645
APA StyleShokrollahi, B., Park, M., Jang, G.-S., Jin, S., Moon, S.-J., Um, K.-H., Jang, S.-S., & Baek, Y.-C. (2025). Maternal Overnutrition in Beef Cattle: Effects on Fetal Programming, Metabolic Health, and Postnatal Outcomes. Biology, 14(6), 645. https://doi.org/10.3390/biology14060645