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Intermittent leucine pulses during continuous feeding alters novel components involved in skeletal muscle growth of neonatal pigs

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Abstract

When neonatal pigs continuously fed formula are supplemented with leucine pulses, muscle protein synthesis and body weight gain are enhanced. To identify the responsible mechanisms, we combined plasma metabolomic analysis with transcriptome expression of the transcriptome and protein catabolic pathways in skeletal muscle. Piglets (n = 23, 7-day-old) were fed continuously a milk replacement formula via orogastric tube for 21 days with an additional parenteral infusion (800 μmol kg−1 h−1) of either leucine (LEU) or alanine (CON) for 1 h every 4 h. Plasma metabolites were measured by liquid chromatography-mass spectrometry. Gene and protein expression analyses of longissimus dorsi muscle were performed by RNA-seq and Western blot, respectively. Compared with CON, LEU pigs had increased plasma levels of leucine-derived metabolites, including 4-methyl-2-oxopentanoate, beta-hydroxyisovalerate, β-hydroxyisovalerylcarnitine, and 3-methylglutaconate (P ≤ 0.05). Leucine pulses downregulated transcripts enriched in the Kyoto Encyclopedia of Genes and Genomes terms “spliceosome,” “GAP junction,” “endocytosis,” “ECM-receptor interaction,” and “DNA replication”. Significant correlations were identified between metabolites derived from leucine catabolism and muscle genes involved in protein degradation, transcription and translation, and muscle maintenance and development (P ≤ 0.05). Further, leucine pulses decreased protein expression of autophagic markers and serine/threonine kinase 4, involved in muscle atrophy (P ≤ 0.01). In conclusion, results from our studies support the notion that leucine pulses during continuous enteral feeding enhance muscle mass gain in neonatal pigs by increasing protein synthetic activity and downregulating protein catabolic pathways through concerted responses in the transcriptome and metabolome.

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Abbreviations

AA:

Amino acids

ABLIM3:

Actin binding LIM protein family member 3

ALDH4A1:

Aldehyde dehydrogenase 4 family member A1

AMPKα:

AMP-activated protein kinase α

ANKH:

ANKH inorganic pyrophosphate transport regulator

ANKRD6:

Ankyrin repeat domain 6

AP4S1:

Adaptor related protein complex 4 sigma 1 subunit

ASF1B:

Anti-silencing function 1B histone chaperone

AU:

Arbitrary units

BCAA:

Branched-chain amino acids

BCL-XL:

B-cell lymphoma-extra large

BW:

Body weight

CCNJL:

Cyclin J like

CD9:

CD9 molecule

CDCA2:

Cell division cycle associated 2

CHRNA3:

Cholinergic receptor nicotinic alpha 3 subunit

CON:

Control group

DAVID:

Database for Annotation, Visualization, and Integrated Discovery

DEGs:

Differentially expressed genes

DSCC1:

DNA replication and sister chromatid cohesion 1

EAA:

Essential amino acids

ERLEC1:

Endoplasmic reticulum lectin 1

ESF1:

ESF1 nucleolar pre-rRNA processing protein, homolog

FN1:

Fibronectin 1

FOXO:

Forkhead box protein O

GNRHR2:

Gonadotropin-releasing hormone II receptor

GO:

Gene ontology

GPR37L1:

G protein-coupled receptor 37 like 1

GRM7:

Glutamate metabotropic receptor 7

HAUS1:

HAUS augmin like complex subunit 1

HMGCLL1:

3-Hydroxymethyl-3-methylglutaryl-CoA lyase like 1

INO80:

Chromatin-remodeling ATPase INO80

KEGG:

Kyoto encyclopedia of genes and genomes

KIC:

α-Ketoisocaproic acid

KLHDC3:

Kelch domain containing 3

LC3I/II:

Microtubule-associated protein 1A/1B light chain 3A

LD:

Longissimus dorsi

LEU:

Leucine supplemented group

LPXN:

Leupaxin

MAFbx:

Muscle Atrophy F-Box/Atrogin-1

MFAP3L:

Microfibrillar associated protein 3 like

MMP15:

Matrix metallopeptidase 15

mTORC1:

Mammalian target of rapamycin complex 1

MuRF-1:

Muscle RING-finger protein-1

NUAK2:

NUAK family SNF1-like kinase 2

OFD1:

Oral-facial-digital syndrome 1 protein

OPHN1:

Oligophrenin 1

OPTN:

Optineurin

P/T:

Phosphorylated/total protein

PARP8:

Protein mono-ADP-ribosyltransferase

PC:

Principal component analysis

PDE10A:

Phosphodiesterase 10A

PKB/Akt:

Protein kinase B

POPDC3:

Popeye domain containing 3

REPS2:

RalBP1-associated Eps domain-containing 2

RGS3:

Regulator of G-protein signaling 3

RNA-seq:

High-throughput RNA sequencing

RNF17:

Ring finger protein 17

ROMO1:

Reactive oxygen species modulator 1

RPKM:

Reads per kilobase per million mapped reads

SERBP1:

Plasminogen activator inhibitor 1 RNA-binding protein

SF3B4:

Splicing factor 3b subunit 4

SIRT-1:

Sirtuin 1

SNX32:

Sorting nexin 32

STK4:

Serine/threonine kinase 4

TAS2R40:

Taste 2 receptor member 40

TBX21:

T-box 21

TMEM117:

Transmembrane protein 117

UBL4A:

Ubiquitin like 4A

VNN2:

Vanin 2

ZBTB32:

Zinc finger and BTB domain containing 32

ZNF207:

Zinc finger protein 207

ZNF385D:

Zinc finger protein 385D

ZNF652:

Zinc finger protein 652

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Authors and Affiliations

  1. Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, U.S. Department of Agriculture/Agricultural Research Service, Houston, TX, 77030, USA

    Rodrigo Manjarín, Claire Boutry-Regard, Agus Suryawan, Hanh V. Nguyen, Marta L. Fiorotto & Teresa A. Davis

  2. Animal Science Department, California Polytechnic State University, 1 Grand Ave, San Luis Obispo, CA, 93407-0255, USA

    Rodrigo Manjarín & Mohammed Abo-Ismail

  3. Ontario Agricultural College, University of Guelph, Guelph, Canada

    Angela Canovas

  4. Arkansas Children’s Nutrition Center, U.S. Department of Agriculture/Agricultural Research Service, Little Rock, AR, 72202, USA

    Brian D. Piccolo

  5. Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR, 72202, USA

    Brian D. Piccolo

  6. Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Magdalena Maj

Authors
  1. Rodrigo Manjarín
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  4. Angela Canovas
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  9. Marta L. Fiorotto
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  10. Teresa A. Davis
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Contributions

Conceptualization—CBR, MF and TD. Data curation—CBR, AS and HN. Formal analysis—RM, BP, AC, MM, and MI. Funding acquisition—MF and TD. Investigation—CBR, AS, HN, MF and TD. Methodology—CBR, AS and TD. Project administration—MF and TD. Resources—MF and TD. Supervision—MF and TD. Validation—MF and TD. Visualization—RM, BP, AC, MM, and MI. Writing—original draft—RM, BP, AC, MM, and MI. Writing—review and editing—all authors.

Corresponding author

Correspondence to Rodrigo Manjarín.

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The authors declare that they have no conflict of interest.

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Experiments were carried out in accordance with the Institutional Animal Care and Use Committee of Baylor College of Medicine and conducted in accordance with the National Research Council’s Guide for the Care and Use of Laboratory Animals (2011).

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726_2020_2894_MOESM1_ESM.xlsx

Online Resource 1 Metabolomic analysis results in plasma from neonatal pigs fed continuously with an orogastric tube for 21 days and supplemented with either leucine or alanine pulses parenterally at 4-h intervals (XLSX 180 kb)

726_2020_2894_MOESM2_ESM.xlsx

Online Resource 2 Differentially expressed genes (P ≤ 0.05) in skeletal muscle tissue from neonatal pigs fed continuously with an orogastric tube for 21 days and supplemented with either leucine or alanine pulses parenterally at 4-h intervals (XLSX 113 kb)

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Manjarín, R., Boutry-Regard, C., Suryawan, A. et al. Intermittent leucine pulses during continuous feeding alters novel components involved in skeletal muscle growth of neonatal pigs. Amino Acids 52, 1319–1335 (2020). https://doi.org/10.1007/s00726-020-02894-5

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