Dietary Protein Restriction Regulates Skeletal Muscle Fiber Metabolic Characteristics Associated with the FGF21-ERK1/2 Pathway

Overview

Journal iScience

Publisher Cell Press

Date 2024 Mar 7

PMID 38450157

Authors

Shuo Li

Haopeng Zhong

Zirui Wang

Jun Chen

Zhouyin Huang

Tiande Zou

Jinming You

Affiliations

Soon will be listed here.

Abstract

Under conditions of dietary amino acid balance, decreasing the dietary crude protein (CP) level in pigs has a beneficial effect on meat quality. To further elucidate the mechanism, we explored the alteration of muscle fiber characteristics and key regulators related to myogenesis in the skeletal muscle of pigs fed a protein restricted diet. Compared to pigs fed a normal protein diet, dietary protein restriction significantly increased the slow-twitch muscle fiber proportion in skeletal muscle, succinic dehydrogenase (SDH) activity, the concentrations of ascorbate, biotin, palmitoleic acid, and the ratio of s-adenosylhomocysteine (SAM) to s-adenosylhomocysteine (SAH), but the fast-twitch muscle fiber proportion, lactate dehydrogenase (LDH) activity, the concentrations of ATP, glucose-6-phosphate, SAM, and SAH in skeletal muscle, and the ratio of serum triiodothyronine (T3) to tetraiodothyronine (T4) were decreased. In conclusion, we demonstrated that dietary protein restriction induced skeletal muscle fiber remodeling association the regulation of FGF21-ERK1/2-mTORC1 signaling in weaned piglets.

References

Liu S, Xie J, Fan Z, Ma X, Yin Y . Effects of low protein diet with a balanced amino acid pattern on growth performance, meat quality and cecal microflora of finishing pigs. J Sci Food Agric. 2022; 103(2):957-967. DOI: 10.1002/jsfa.12245. View

Vankrunkelsven W, Thiessen S, Derde S, Vervoort E, Derese I, Pintelon I . Development of muscle weakness in a mouse model of critical illness: does fibroblast growth factor 21 play a role?. Skelet Muscle. 2023; 13(1):12. PMC: 10401744. DOI: 10.1186/s13395-023-00320-4. View

Lu T, Zhu Y, Guo J, Mo Z, Zhou Q, Hu C . MDFI regulates fast-to-slow muscle fiber type transformation via the calcium signaling pathway. Biochem Biophys Res Commun. 2023; 671:215-224. DOI: 10.1016/j.bbrc.2023.05.053. View

Pan Y, Chen L, Cheng J, Zhu X, Wu P, Bao L . Genome-wide DNA methylation profiles provide insight into epigenetic regulation of red and white muscle development in Chinese perch Siniperca chuatsi. Comp Biochem Physiol B Biochem Mol Biol. 2021; 256:110647. DOI: 10.1016/j.cbpb.2021.110647. View

Katashima C, de Oliveira Micheletti T, Braga R, Gaspar R, Goeminne L, Moura-Assis A . Evidence for a neuromuscular circuit involving hypothalamic interleukin-6 in the control of skeletal muscle metabolism. Sci Adv. 2022; 8(30):eabm7355. PMC: 9337767. DOI: 10.1126/sciadv.abm7355. View

Lautherbach N, Goncalves D, Silveira W, Paula-Gomes S, Valentim R, Zanon N . Urocortin 2 promotes hypertrophy and enhances skeletal muscle function through cAMP and insulin/IGF-1 signaling pathways. Mol Metab. 2022; 60:101492. PMC: 9035725. DOI: 10.1016/j.molmet.2022.101492. View

Warren C, OSullivan J, Friesen M, Becker C, Zhang X, Liu P . Induced Pluripotent Stem Cell Differentiation Enables Functional Validation of GWAS Variants in Metabolic Disease. Cell Stem Cell. 2017; 20(4):547-557.e7. DOI: 10.1016/j.stem.2017.01.010. View

Meissner J, Freund R, Krone D, Umeda P, Chang K, Gros G . Extracellular signal-regulated kinase 1/2-mediated phosphorylation of p300 enhances myosin heavy chain I/beta gene expression via acetylation of nuclear factor of activated T cells c1. Nucleic Acids Res. 2011; 39(14):5907-25. PMC: 3152325. DOI: 10.1093/nar/gkr162. View

Choe J, Choi Y, Lee S, Shin H, Ryu Y, Hong K . The relation between glycogen, lactate content and muscle fiber type composition, and their influence on postmortem glycolytic rate and pork quality. Meat Sci. 2011; 80(2):355-62. DOI: 10.1016/j.meatsci.2007.12.019. View

10.

Brooke M, Kaiser K . Muscle fiber types: how many and what kind?. Arch Neurol. 1970; 23(4):369-79. DOI: 10.1001/archneur.1970.00480280083010. View

11.

Kim G, Yang H, Jeong J . Intramuscular variations of proteome and muscle fiber type distribution in semimembranosus and semitendinosus muscles associated with pork quality. Food Chem. 2017; 244:143-152. DOI: 10.1016/j.foodchem.2017.10.046. View

12.

Der Vartanian A, Quetin M, Michineau S, Aurade F, Hayashi S, Dubois C . PAX3 Confers Functional Heterogeneity in Skeletal Muscle Stem Cell Responses to Environmental Stress. Cell Stem Cell. 2019; 24(6):958-973.e9. PMC: 6628901. DOI: 10.1016/j.stem.2019.03.019. View

13.

Want E, Masson P, Michopoulos F, Wilson I, Theodoridis G, Plumb R . Global metabolic profiling of animal and human tissues via UPLC-MS. Nat Protoc. 2012; 8(1):17-32. DOI: 10.1038/nprot.2012.135. View

14.

Yuan W, Cui C, Li J, Xu Y, Fan C, Chen Y . Intracellular TMEM16A is necessary for myogenesis of skeletal muscle. iScience. 2022; 25(11):105446. PMC: 9647518. DOI: 10.1016/j.isci.2022.105446. View

15.

Cangelosi A, Puszynska A, Roberts J, Armani A, Nguyen T, Spinelli J . Zonated leucine sensing by Sestrin-mTORC1 in the liver controls the response to dietary leucine. Science. 2022; 377(6601):47-56. PMC: 10049859. DOI: 10.1126/science.abi9547. View

16.

Smith C, Want E, OMaille G, Abagyan R, Siuzdak G . XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem. 2006; 78(3):779-87. DOI: 10.1021/ac051437y. View

17.

Liu J, Wang L, Chen W, Li J, Shan T . CRTC3 Regulates the Lipid Metabolism and Adipogenic Differentiation of Porcine Intramuscular and Subcutaneous Adipocytes by Activating the Calcium Pathway. J Agric Food Chem. 2021; 69(25):7243-7255. DOI: 10.1021/acs.jafc.1c02021. View

18.

Ehlers M, Celona B, Black B . NFATc1 controls skeletal muscle fiber type and is a negative regulator of MyoD activity. Cell Rep. 2014; 8(6):1639-1648. PMC: 4180018. DOI: 10.1016/j.celrep.2014.08.035. View

19.

Burtscher J, Soltany A, Visavadiya N, Burtscher M, Millet G, Khoramipour K . Mitochondrial stress and mitokines in aging. Aging Cell. 2023; 22(2):e13770. PMC: 9924952. DOI: 10.1111/acel.13770. View

20.

Thevenot E, Roux A, Xu Y, Ezan E, Junot C . Analysis of the Human Adult Urinary Metabolome Variations with Age, Body Mass Index, and Gender by Implementing a Comprehensive Workflow for Univariate and OPLS Statistical Analyses. J Proteome Res. 2015; 14(8):3322-35. DOI: 10.1021/acs.jproteome.5b00354. View