Hostname: page-component-669899f699-rg895 Total loading time: 0 Render date: 2025-04-25T06:40:08.448Z Has data issue: false hasContentIssue false

(−)-Epicatechin treatment modify the expression of genes related to atrophy in gastrocnemius muscle of male rats obese by programing

Published online by Cambridge University Press:  07 October 2024

Ana Luisa Alvarez-Chávez
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, México Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Ciudad de México, México
Sergio De los Santos
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, México Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Ciudad de México, México
Ramón Mauricio Coral-Vázquez
Affiliation:
Sección de Estudios de Posgrado e Investigación, Escuela Superior de Medicina, Instituto Politécnico Nacional, Ciudad de México, México Subdirección de Enseñanza e Investigación, Centro Médico Nacional “20 de Noviembre”, Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Ciudad de México, México
Juan Pablo Méndez
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, México Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Ciudad de México, México
Carlos Palma Flores
Affiliation:
Sección de Estudios de Posgrado e Investigación, Escuela Superior de Medicina, Instituto Politécnico Nacional, Ciudad de México, México Subdirección de Enseñanza e Investigación, Centro Médico Nacional “20 de Noviembre”, Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Ciudad de México, México
Elena Zambrano
Affiliation:
Departamento de Biología de Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Ciudad de México, México Facultad de Química, Universidad Nacional Autónoma de México, Ciudad de México, México
Patricia Canto*
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, México Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán”, Ciudad de México, México
*
Corresponding author: Patricia Canto; Email: [email protected]

Abstract

The aim of this study is to determine if the offspring of mothers with obesity, present disorders in the expression of genes related to atrophy or protein synthesis in the muscle and if these disorders are modified with the (−)-epicatechin (Epi) treatment. Six male offspring per group were randomly assigned to the control groups [C and offspring of maternal obesity (MO)] or the Epi intervention groups, Epi treatment for 13 weeks (C + Epi long or MO + Epi long), or Epi administration for two weeks (C + Epi short or MO + Epi short). The effect of Epi in the gastrocnemius tissue was evaluated, analyzing mRNA and protein levels of Murf1, MAFbx, Foxo1, NFkB, and p70S6K-alpha. After the analysis by two-way ANOVA, we found an influence of the Epi long treatment over the model, by decreasing the Murf1 gene expression in both groups treated with the flavonoid (C + Epi long and MO + Epi long) (p = 0.036). Besides, Epi long treatment over the NFκB expression, by decreasing the fold increase in both groups treated with the flavonoid (C + Epi long and MO + Epi long) (p = 0.038). We not find any interaction between the variables or changes in the MAFbx, Foxo1 mRNA, neither in the phosphorylated/total protein ratio of NFκB, Foxo1, or p70S6K-alpha. In conclusions, treatment with a long protocol of Epi, reduces the mRNA of the muscle atrophy genes Murf 1 and NFkB, in the gastrocnemius muscle; however, these changes are not maintained at protein level.

Type
Original Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Shamah-Levy, T, Romero-Martínez, M, Barrientos-Gutiérrez, T, et al. Encuesta Nacional de Salud y Nutrición 2021 sobre Covid-19. Resultados nacionales, 2022. Instituto Nacional de Salud Pública, Cuernavaca, México.Google Scholar
Ahmed, A, Liang, M, Chi, L, et al. Maternal obesity persistently alters cardiac progenitor gene expression and programs adult-onset heart disease susceptibility. Mol Metab. 2021; 43, 101116.CrossRefGoogle ScholarPubMed
Schellong, K, Melchior, K, Ziska, T, Rancourt, RC, Henrich, W, Plagemann, A. Maternal but not paternal high-fat diet (HFD) exposure at conception predisposes for ‘Diabesity’ in offspring generations. Int J Environ Res Public Health. 2020; 17(12), 4229.CrossRefGoogle Scholar
De Los Santos, S, Reyes-Castro, LA, Coral-Vázquez, RM, Méndez, JP, Leal-García, M, Zambrano. E, etal, (-)-epicatechin reduces adiposity in male offspring of obese rats. J Dev Orig Health Dis. 2020; 11(1), 3743.CrossRefGoogle Scholar
Sishi, B, Loos, B, Ellis, B, Smith, W, Du Toit, EF, Engelbrecht, AM. Diet-induced obesity alters signalling pathways and induces atrophy and apoptosis in skeletal muscle in a prediabetic rat model. Exp Physiol. 2011; 96(2), 179193.CrossRefGoogle Scholar
Abrigo, J, Rivera, JC, Aravena, J, et al. High fat diet-induced skeletal muscle wasting is decreased by mesenchymal stem cells administration: implications on oxidative stress, ubiquitin proteasome pathway activation, and myonuclear apoptosis. Oxid Med Cell Longev. 2016; 9047821(1), 113.Google Scholar
Morales, PE, Monsalves-Álvarez, M, Tadinada, SM, et al. Skeletal muscle type-specific mitochondrial adaptation to high-fat diet relies on differential autophagy modulation. FASEB J. 2021; 35(10), e21933.CrossRefGoogle ScholarPubMed
Bayol, SA, Simbi, BH, Stickland, NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol. 2005; 567(3), 951961.CrossRefGoogle ScholarPubMed
De los Santos, S, Coral-Vázquez, RM, Menjivar, M, et al. (−)-Epicatechin modifies body composition of the male offspring of obese rats. J Funct Foods. 2019; 58, 367373.CrossRefGoogle Scholar
Mikovic, J, Brightwell, C, Lindsay, A, et al. An obesogenic maternal environment impairs mouse growth patterns, satellite cell activation, and markers of postnatal myogenesis. Am J Physiol Endocrinol Metab. 2020; 319(6), E1008E1018.CrossRefGoogle ScholarPubMed
Egerman, MA, Glass, DJ. Signaling pathways controlling skeletal muscle mass. Crit Rev Biochem Mol Biol. 2014; 49(1), 5968.CrossRefGoogle ScholarPubMed
Salto, R, Girón, MD, Manzano, M, et al. Programming skeletal muscle metabolic flexibility in offspring of male rats in response to maternal consumption of slow digesting carbohydrates during pregnancy. Nutrients. 2020; 12(2), 528.CrossRefGoogle ScholarPubMed
Cremonini, E, Iglesias, DE, Kang, J, et al. (-)-Epicatechin and the comorbidities of obesity. Arch Biochem Biophys. 2020; 690, 108505.CrossRefGoogle ScholarPubMed
Gutierrez-Salmean, G, Ciaraldi, TP, Nogueira, L, et al. Effects of (−)-epicatechin on molecular modulators of skeletal muscle growth and differentiation. J Nutr Biochem. 2014; 25(1), 9194.CrossRefGoogle ScholarPubMed
Lee, SJ, Leem, YE, Go, GY, et al. Epicatechin elicits MyoD-dependent myoblast differentiation and myogenic conversion of fibroblasts. Plos One. 2017; 12(4), e0175271.CrossRefGoogle ScholarPubMed
Munguia, L, Ramirez-Sanchez, I, Meaney, E, Villarreal, F, Ceballos, G, Najera, N. Flavonoids from dark chocolate and (-)-epicatechin ameliorate high-fat diet-induced decreases in mobility and muscle damage in aging mice. Food Biosci. 2020; 37, 100710.CrossRefGoogle ScholarPubMed
Rodríguez-González, GL, De Los Santos, S, Méndez-Sánchez, D, et al. High-fat diet consumption by male rat offspring of obese mothers exacerbates adipose tissue hypertrophy and metabolic alterations in adult life. Br J Nutr. 2023; 130(5), 783792.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH, Fahey, GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123(11), 19391951.CrossRefGoogle ScholarPubMed
Cheng, H, Xu, N, Zhao, W, et al. (-)-Epicatechin regulates blood lipids and attenuates hepatic steatosis in rats fed high-fat diet. Mol Nutr Food Res. 2017; 61, 1700303. DOI: 10.1002/mnfr.201700303.CrossRefGoogle ScholarPubMed
Ramirez-Sanchez, I, De los Santos, S, Gonzalez-Basurto, S, et al. (-)-Epicatechin improves mitochondrial-related protein levels and ameliorates oxidative stress in dystrophic δ-sarcoglycan null mouse striated muscle. FEBS J. 2014; 281(24), 55675580.CrossRefGoogle ScholarPubMed
De Los Santos, S, García-Pérez, V, Hernández-Reséndiz, S, et al. (-)-Epicatechin induces physiological cardiac growth by activation of the PI3K/Akt pathway in mice. Mol Nutr Food Res. 2017; 61, 1600343. DOI: 10.1002/mnfr.201600343.CrossRefGoogle ScholarPubMed
Blaauw, B, Schiaffino, S, Reggiani, C. Mechanisms modulating skeletal muscle phenotype. Compr Physiol. 2013; 3, 16451687.CrossRefGoogle ScholarPubMed
Roy, B, Curtis, ME, Fears, LS, Nahashon, SN, Fentress, HM. Molecular mechanisms of obesity-induced osteoporosis and muscle atrophy. front physiol. 2016;7, 439.CrossRefGoogle ScholarPubMed
Collins, KH, Herzog, W, MacDonald, GZ, et al. Metabolic syndrome, and musculoskeletal disease: common inflammatory pathways suggest a central role for loss of muscle integrity. Front Physiol. 2018; 9, 112.CrossRefGoogle ScholarPubMed
Tong, JF, Yan, X, Zhu, MJ, Ford, SP, Nathanielsz, PW, Du, M. Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle. Am J Physiol Endocrinol Metab. 2009; 296(4), E917E924.CrossRefGoogle ScholarPubMed
Pileggi, CA, Segovia, SA, Markworth, JF, et al. Maternal conjugated linoleic acid supplementation reverses high-fat diet-induced skeletal muscle atrophy and inflammation in adult male rat offspring. Am J Physiol Regul Integr Comp Physiol. 2016; 310(5), R432R439.CrossRefGoogle ScholarPubMed
Cui, J, Song, L, Wang, R, et al. Maternal metformin treatment during gestation and lactation improves skeletal muscle development in offspring of rat dams fed high-fat diet. Nutrients. 2021; 13(10), 3417.CrossRefGoogle ScholarPubMed
Taub, PR, Ramirez-Sanchez, I, Ciaraldi, TP, et al. Perturbations in skeletal muscle sarcomere structure in patients with heart failure and type 2 diabetes: restorative effects of (-)-epicatechin-rich cocoa. Clin Sci (Lond). 2013; 125(8), 383389.CrossRefGoogle ScholarPubMed
McDonald, CM, Ramirez-Sanchez, I, Oskarsson, B, et al. (-)-Epicatechin induces mitochondrial biogenesis and markers of muscle regeneration in adults with Becker muscular dystrophy. Muscle Nerve. 2021; 63(2), 239249.CrossRefGoogle ScholarPubMed
Ramírez-Ramírez, M, Fernández-Valverde, F, Reséndiz-García, A, et al. (-)-Epicatechin improves tibialis anterior muscle repair in CD1 mice with BaCl2-induced damage. J Nutr Biochem. 2022; 107, 109069.CrossRefGoogle Scholar
Granado, M, Martín, AI, Priego, T, López-Calderón, A, Villanúa, MA. Tumour necrosis factor blockade did not prevent the increase of muscular muscle RING finger-1 and muscle atrophy F-box in arthritic rats. J Endocrinol. 2006; 191(1), 319326.CrossRefGoogle Scholar
Ohanna, M, Sobering, AK, Lapointe, T, et al. Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol. 2005; 7(3), 286294.CrossRefGoogle ScholarPubMed
Sun, YN, Huang, JQ, Chen, ZZ, et al. Amyotrophy induced by a high-fat diet is closely related to inflammation and protein degradation determined by quantitative phosphoproteomic analysis in skeletal muscle of C57BL/6 J mice. J Nutr. 2020; 150(2), 294302.CrossRefGoogle ScholarPubMed
Cheng, TL, Lin, ZY, Liao, KY, et al. Magnesium lithospermate B attenuates high-fat diet-induced muscle atrophy in C57BL/6J mice. Nutrients. 2021; 14(1), 104.CrossRefGoogle ScholarPubMed
Schwanhäusser, B, Busse, D, Li, N, et al. Global quantification of mammalian gene expression control. Nature. 2011; 473(7347), 337342.CrossRefGoogle ScholarPubMed
Geiger, J, Burkhart, JM, Gambaryan, S, Walter, U, Sickmann, A, Zahedi, RP. Response: platelet transcriptome and proteome--relation rather than correlation. Blood. 2013; 121(26), 52575258.CrossRefGoogle ScholarPubMed
Lexell, J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci. 1995; 50, 1116.Google ScholarPubMed
Verdijk, LB, Koopman, R, Schaart, G, Meijer, K, Savelberg, HH, van Loon, LJ. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab. 2007; 292(1), E151E157.CrossRefGoogle ScholarPubMed
Schiaffino, S, Reggiani, C. Fiber types in mammalian skeletal muscles. Physiol Rev. 2011; 91(4), 14471531.CrossRefGoogle ScholarPubMed
Talbot, J, Maves, L. Skeletal muscle fiber type: using insights from muscle developmental biology to dissect targets for susceptibility and resistance to muscle disease. Wiley Interdiscip Rev Dev Biol. 2016; 5(4), 518534.CrossRefGoogle ScholarPubMed
Tanner, CJ, Barakat, HA, Lynis Dohm, G, et al. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab. 2002; 282(6), 11911196.CrossRefGoogle ScholarPubMed
Maltin, CA. Muscle development and obesity. Organogenesis. 2008; 4(3), 158169.CrossRefGoogle ScholarPubMed
Supplementary material: File

Alvarez-Chávez et al. supplementary material

Alvarez-Chávez et al. supplementary material
Download Alvarez-Chávez et al. supplementary material(File)
File 343.2 KB