Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes

Oleksandr Nychyk; Wiley Barton; Agata M. Rudolf; Serena Boscaini; Aaron Walsh; Thomaz F.S. Bastiaanssen; Linda Giblin; Paul Cormican; Liang Chen; Yolanda Piotrowicz; Davina Derous; Áine Fanning; Xiaofei Yin; Jim Grant; Silvia Melgar; Lorraine Brennan; Sharon E. Mitchell; John F. Cryan; Jun Wang; Paul D. Cotter; John R. Speakman; Kanishka N. Nilaweera

doi:10.1016/j.celrep.2021.109093

Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes

Oleksandr Nychyk, Wiley Barton, Agata M. Rudolf, Serena Boscaini, Aaron Walsh, Thomaz F.S. Bastiaanssen, Linda Giblin, Paul Cormican, Liang Chen, Yolanda Piotrowicz, Davina Derous, Áine Fanning, Xiaofei Yin, Jim Grant, Silvia Melgar, Lorraine Brennan, Sharon E. Mitchell, John F. Cryan, Jun Wang, Paul D. CotterJohn R. Speakman, Kanishka N. Nilaweera

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Abstract

We investigated how protein quantity (10%–30%) and quality (casein and whey) interact with dietary fat (20%–55%) to affect metabolic health in adult mice. Although dietary fat was the main driver of body weight gain and individual tissue weight, high (30%) casein intake accentuated and high whey intake reduced the negative metabolic aspects of high fat. Jejunum and liver transcriptomics revealed increased intestinal permeability, low-grade inflammation, altered lipid metabolism, and liver dysfunction in casein-fed but not whey-fed animals. These differential effects were accompanied by altered gut size and microbial functions related to amino acid degradation and lipid metabolism. Fecal microbiota transfer confirmed that the casein microbiota increases and the whey microbiota impedes weight gain. These data show that the effects of dietary fat on weight gain and tissue partitioning are further influenced by the quantity and quality of the associated protein, primarily via effects on the microbiota.

Original language	English
Article number	109093
Number of pages	34
Journal	Cell Reports
Volume	35
Issue number	6
Early online date	11 May 2021
DOIs	https://doi.org/10.1016/j.celrep.2021.109093
Publication status	Published - 11 May 2021

Bibliographical note

ACKNOWLEDGMENTS
This work was supported by a research grant from Science Foundation Ireland
(SFI) under grant SFI/16/BBSRC/3389, BBSRC under grant number BB/
P009875/1 (to K.N.N. and J.R.S.), and in part by SFI and the Department of
Agriculture, Food and Marine under grant 16/RC/3835 (to VistaMilk). We thank
Conall Strain, David Mannion, and John Leech for contributing to the metabolomics analysis. We thank Alina Kondrashina for help with the Milliplex
system.

Keywords

high fat intake
high protein intake
energy metabolism
gut microbiota
adiposity
whey protein
IGF1
inflammation
body weight and tissue correlation
gut permeability

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Nychyk_etal_CR_Protein_Quality_And_VoR
© 2021 The Authors. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
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Cite this

Nychyk, O., Barton, W., Rudolf, A. M., Boscaini, S., Walsh, A., Bastiaanssen, T. F. S., Giblin, L., Cormican, P., Chen, L., Piotrowicz, Y., Derous, D., Fanning, Á., Yin, X., Grant, J., Melgar, S., Brennan, L., Mitchell, S. E., Cryan, J. F., Wang, J., ... Nilaweera, K. N. (2021). Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes. Cell Reports, 35(6), Article 109093. https://doi.org/10.1016/j.celrep.2021.109093

Nychyk, O, Barton, W, Rudolf, AM, Boscaini, S, Walsh, A, Bastiaanssen, TFS, Giblin, L, Cormican, P, Chen, L, Piotrowicz, Y, Derous, D, Fanning, Á, Yin, X, Grant, J, Melgar, S, Brennan, L, Mitchell, SE, Cryan, JF, Wang, J, Cotter, PD, Speakman, JR & Nilaweera, KN 2021, 'Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes', Cell Reports, vol. 35, no. 6, 109093. https://doi.org/10.1016/j.celrep.2021.109093

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title = "Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes",

abstract = "We investigated how protein quantity (10%–30%) and quality (casein and whey) interact with dietary fat (20%–55%) to affect metabolic health in adult mice. Although dietary fat was the main driver of body weight gain and individual tissue weight, high (30%) casein intake accentuated and high whey intake reduced the negative metabolic aspects of high fat. Jejunum and liver transcriptomics revealed increased intestinal permeability, low-grade inflammation, altered lipid metabolism, and liver dysfunction in casein-fed but not whey-fed animals. These differential effects were accompanied by altered gut size and microbial functions related to amino acid degradation and lipid metabolism. Fecal microbiota transfer confirmed that the casein microbiota increases and the whey microbiota impedes weight gain. These data show that the effects of dietary fat on weight gain and tissue partitioning are further influenced by the quantity and quality of the associated protein, primarily via effects on the microbiota.",

keywords = "high fat intake, high protein intake, energy metabolism, gut microbiota, adiposity, whey protein, IGF1, inflammation, body weight and tissue correlation, gut permeability",

author = "Oleksandr Nychyk and Wiley Barton and Rudolf, {Agata M.} and Serena Boscaini and Aaron Walsh and Bastiaanssen, {Thomaz F.S.} and Linda Giblin and Paul Cormican and Liang Chen and Yolanda Piotrowicz and Davina Derous and {\'A}ine Fanning and Xiaofei Yin and Jim Grant and Silvia Melgar and Lorraine Brennan and Mitchell, {Sharon E.} and Cryan, {John F.} and Jun Wang and Cotter, {Paul D.} and Speakman, {John R.} and Nilaweera, {Kanishka N.}",

note = "ACKNOWLEDGMENTS This work was supported by a research grant from Science Foundation Ireland (SFI) under grant SFI/16/BBSRC/3389, BBSRC under grant number BB/ P009875/1 (to K.N.N. and J.R.S.), and in part by SFI and the Department of Agriculture, Food and Marine under grant 16/RC/3835 (to VistaMilk). We thank Conall Strain, David Mannion, and John Leech for contributing to the metabolomics analysis. We thank Alina Kondrashina for help with the Milliplex system.",

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AU - Nychyk, Oleksandr

AU - Barton, Wiley

AU - Rudolf, Agata M.

AU - Boscaini, Serena

AU - Walsh, Aaron

AU - Bastiaanssen, Thomaz F.S.

AU - Giblin, Linda

AU - Cormican, Paul

AU - Chen, Liang

AU - Piotrowicz, Yolanda

AU - Derous, Davina

AU - Fanning, Áine

AU - Yin, Xiaofei

AU - Grant, Jim

AU - Melgar, Silvia

AU - Brennan, Lorraine

AU - Mitchell, Sharon E.

AU - Cryan, John F.

AU - Wang, Jun

AU - Cotter, Paul D.

AU - Speakman, John R.

AU - Nilaweera, Kanishka N.

N1 - ACKNOWLEDGMENTS This work was supported by a research grant from Science Foundation Ireland (SFI) under grant SFI/16/BBSRC/3389, BBSRC under grant number BB/ P009875/1 (to K.N.N. and J.R.S.), and in part by SFI and the Department of Agriculture, Food and Marine under grant 16/RC/3835 (to VistaMilk). We thank Conall Strain, David Mannion, and John Leech for contributing to the metabolomics analysis. We thank Alina Kondrashina for help with the Milliplex system.

PY - 2021/5/11

Y1 - 2021/5/11

N2 - We investigated how protein quantity (10%–30%) and quality (casein and whey) interact with dietary fat (20%–55%) to affect metabolic health in adult mice. Although dietary fat was the main driver of body weight gain and individual tissue weight, high (30%) casein intake accentuated and high whey intake reduced the negative metabolic aspects of high fat. Jejunum and liver transcriptomics revealed increased intestinal permeability, low-grade inflammation, altered lipid metabolism, and liver dysfunction in casein-fed but not whey-fed animals. These differential effects were accompanied by altered gut size and microbial functions related to amino acid degradation and lipid metabolism. Fecal microbiota transfer confirmed that the casein microbiota increases and the whey microbiota impedes weight gain. These data show that the effects of dietary fat on weight gain and tissue partitioning are further influenced by the quantity and quality of the associated protein, primarily via effects on the microbiota.

AB - We investigated how protein quantity (10%–30%) and quality (casein and whey) interact with dietary fat (20%–55%) to affect metabolic health in adult mice. Although dietary fat was the main driver of body weight gain and individual tissue weight, high (30%) casein intake accentuated and high whey intake reduced the negative metabolic aspects of high fat. Jejunum and liver transcriptomics revealed increased intestinal permeability, low-grade inflammation, altered lipid metabolism, and liver dysfunction in casein-fed but not whey-fed animals. These differential effects were accompanied by altered gut size and microbial functions related to amino acid degradation and lipid metabolism. Fecal microbiota transfer confirmed that the casein microbiota increases and the whey microbiota impedes weight gain. These data show that the effects of dietary fat on weight gain and tissue partitioning are further influenced by the quantity and quality of the associated protein, primarily via effects on the microbiota.

KW - high fat intake

KW - high protein intake

KW - energy metabolism

KW - gut microbiota

KW - adiposity

KW - whey protein

KW - IGF1

KW - inflammation

KW - body weight and tissue correlation

KW - gut permeability

U2 - 10.1016/j.celrep.2021.109093

DO - 10.1016/j.celrep.2021.109093

M3 - Article

C2 - 33979605

SN - 2211-1247

VL - 35

JO - Cell Reports

JF - Cell Reports

IS - 6

M1 - 109093

ER -

Protein quality and quantity influence the effect of dietary fat on weight gain and tissue partitioning via host-microbiota changes

Abstract

Bibliographical note

Keywords

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