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Myotendinous Junction Components of Different Skeletal Muscles Present Morphological Changes in Obese Rats

Published online by Cambridge University Press:  21 April 2021

Bruna Aléxia Cristofoletti Grillo
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
Lara C. Rocha*
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
Giovana Z. Martinez
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
Jurandyr Pimentel Neto
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
Carolina dos Santos Jacob
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
Ii-sei Watanabe
Affiliation:
Department of Anatomy, Institute of Biomedical Sciences -ICB III, University of São Paulo (USP), São Paulo, SP05508-900, Brazil
Adriano P. Ciena
Affiliation:
Laboratory of Morphology and Physical Activity (LAMAF), Institute of Biosciences (IB), São Paulo State University (UNESP), Rio Claro, SP13506-900, Brazil
*
*Author for correspondence: Lara C. Rocha, E-mail: [email protected]
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Abstract

Obesity is characterized by excess adipose tissue and chronic inflammation and promotes extensive changes that can compromise skeletal muscles’ structural and functional integrity. Obesity can seriously impact the force transmission region between the muscle and the tendon, the myotendinous junction (MTJ). The present study aimed to investigate the plasticity of muscle fibers and MTJ regions in high-fat diet-induced obesity in rat tibialis anterior (TA) and soleus (SO) muscles. Wistar rats were divided into control and obese groups (induced by a high-fat diet). The samples of TA and SO muscles were prepared for histochemical and ultrastructural analysis (sarcomeres and MTJ projection). In the muscle fiber, similar adaptations were observed between the muscles of the smaller fiber (types I and IIa) in the obesity results. The MTJ region demonstrated different adaptations between the analyzed muscles. The TA–MTJ region has shorter ultrastructures, while in the SO–MTJ region, the ultrastructures were larger. We conclude that obesity induced by a high-fat diet promotes similar adaptation in the muscle fibers; however, in the MTJ region, the sarcoplasmatic projections and adjacent sarcomere demonstrate different adaptations according to distinct muscle phenotypes.

Type
Biological Applications
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Acevedo, LM, Raya, AI, Ríos, R, Aguilera-Tejero, E & Rivero, JL (2017). Obesity-induced discrepancy between contractile and metabolic phenotypes slow-and fast-twitch skeletal muscles of female obese zucker rats. J Appl Physiol 123(1), 249259.10.1152/japplphysiol.00282.2017CrossRefGoogle ScholarPubMed
Allen, DG (2004). Skeletal muscle function: Role of ionic changes in fatigue, damage and disease. Clin Exp Pharmacol Physiol 31(8), 485493.10.1111/j.1440-1681.2004.04032.xCrossRefGoogle ScholarPubMed
Charvet, B, Ruggiero, F & Le Guellec, D (2012). The development of the myotendinous junction. A review. Muscles, Ligaments Tendons J 2(2), 5363.Google ScholarPubMed
Choi, SJ (2014). Cellular mechanism of eccentric-induced muscle injury and its relationship with sarcomere heterogeneity. J Exerc Rehabil 10(4), 200204.10.12965/jer.140139CrossRefGoogle ScholarPubMed
Ciena, AP, Almeida, SRY, Dias, FJ, Bolina, CS, Issa, JPM, Iyomasa, MM, Ogawa, K & Watanabe, I (2012). Fine structure of myotendinous junction between the anterior belly of the digastric muscle and intermediate tendon in adults rats. Micron 43(2–3), 258262.10.1016/j.micron.2011.08.009CrossRefGoogle ScholarPubMed
Ciena, AP, Luques, IU, Dias, FJ, Almeida, SRY, Iyomasa, MM & Watanabe, I (2010). Ultrastructure of the myotendinous junction of the medial pterygoid muscle of adult and aged wistar rats. Micron 41(8), 10111014.CrossRefGoogle ScholarPubMed
Collins, KH, Hart, DA, Smith, IC, Issler, AM, Reimer, RA, Seerattan, RA, Rios, JL & Herzog, W (2017). Acute and chronic changes in rat soleus muscle after high-fat high-sucrose diet. Physiol Rep 5(10), e13270.CrossRefGoogle ScholarPubMed
Couturier, A, Ringseis, R, Mooren, F, Krüger, K, Most, E & Eder, K (2013). Carnitine supplementation to obese zucker rats prevents obesity-induced type I to type II muscle fiber transition and favors an oxidative phenotype of skeletal muscle. Nutr Metab 10(1), 111.CrossRefGoogle ScholarPubMed
Curzi, D, Lattanzi, D, Burattini, S, Tidball, JG & Falcieri, E (2013). Morphological changes of myotendínous junction generated by muscle disuse atrophy. Microscopie 19(1), 4652.Google Scholar
Curzi, D, Sartini, S, Guescini, M, Lattanzi, D, Di Palma, M, Ambrogini, P, Savelli, D, Stocchi, V, Cuppini, R & Falcieri, E (2016). Effect of different exercise intensities on the myotendinous junction plasticity. PLoS One 11(6), e015059.CrossRefGoogle ScholarPubMed
Gomes, SF, Silva, FC & Volp, ACP (2016). What is the role of inflammatory mediators on energy metabolism? Inflamm Cell Signal 3, e1189.Google Scholar
Guedes, JM, Pieri, BLS, Luciano, TF, Marques, SO, Guglielmo, LGA & Souza, CT (2020). Muscular resistance, hypertrophy and strength training equally reduce adiposity, inflammation and insulin resistance in mice with diet-induced obesity. Einstein 18, 19.Google ScholarPubMed
Gumina, S, Candela, V, Passaretti, D, Latino, G, Venditto, T, Mariani, L & Santilli, V (2014). The association between body fat and rotator cuff tear: The influence on rotator cuff tear sizes. J. Shoulder Elb Surg 23(11), 16691674.10.1016/j.jse.2014.03.016CrossRefGoogle ScholarPubMed
He, J, Watkins, S & Kelley, DE (2001). Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50(4), 817823.10.2337/diabetes.50.4.817CrossRefGoogle ScholarPubMed
Hyodo, M, Kawajita, S & Desaki, J (2001). Scanning electron microscopic study of the muscle fiber ends at the myotendinous junction in the posterior cricoarytenoid and cricothyroid muscle in rats. Acta Otolaryngol 121(8), 953956.10.1080/000164801317166853CrossRefGoogle Scholar
Izaola, O, Luis, D, Sajoux, I, Domingo, JC & Vidal, M (2015). Inflamácion y obesidad (lipo inflamácion). Nutr Hosp 31(6), 23522358.Google Scholar
Jacob, CdS, Rocha, LC, Pimentel Neto, J, Watanabe, I & Ciena, AP (2019). Effects of physical training on sarcomere lengths and muscle-tendon interface of the cervical region in an experimental model of menopause. Eur J Histochem 63(3038), 131135.CrossRefGoogle Scholar
Jacobson, KR, Lipp, S, Acuna, A, Leng, Y, Bu, Y & Calve, S (2020). Comparative analysis of the extracellular matrix proteome across the myotendinous junction. J Proteome Res 19(10), 39553967.10.1021/acs.jproteome.0c00248CrossRefGoogle ScholarPubMed
Kostrominova, TY, Calve, S, Arruda, EM & Larkin, LM (2009). Ultrastructure of myotendinous junctions in tendon-skeletal muscle constructs engineered in vitro. Histol Histopathol 24(5), 541550.Google ScholarPubMed
Krause Neto, W, Silva, WA, Ciena, AP, Anaruma, CA & Gama, EF (2017). Divergent effects of resistance training and anabolic steroid on the postsynaptic region of different skeletal muscles of aged rats. Exp Gerontol 98, 8090.10.1016/j.exger.2017.08.018CrossRefGoogle ScholarPubMed
Lee, CH, Shin, SH, Kang, GM, Kim, S, Kim, J, Yu, R & Kim, M (2019). Cellular source of hypothalamic macrophage accumulation in diet-induced obesity. J Neuroinflammation 16(1), 110.CrossRefGoogle ScholarPubMed
Lieber, RL & Ward, SR (2011). Skeletal muscle design to meet functional demands. Phil Trans R Soc B 366(1570), 14661476.10.1098/rstb.2010.0316CrossRefGoogle ScholarPubMed
MacIntosh, BR (2017). Recent developments in understanding the length dependence of contractile response of skeletal muscle. Eur J Appl Physiol 117(6), 10591071.CrossRefGoogle ScholarPubMed
Moura, LP, Dalia, RA, Araújo, MB, Sponton, AdS, Pauli, JR, Moura, RF & Mello, MAR (2012). Alterações bioquímicas e hepáticas em ratos submetidos à uma dieta. Rev Nutr 25(6), 685693.CrossRefGoogle Scholar
Palma, LD, Marinelli, M, Pavan, M & Bertoni-Freddari, C (2011). Involvement of the muscle-tendon junction in skeletal muscle atrophy: An ultrastructural study. Rom J Morphol Embryol 52(1), 105109.Google Scholar
Pellegrinelli, V, Rouault, C, Rodriguez-Cuenca, S, Albert, V, Edom-Vovard, F, Vidal-Puig, A, Clément, K, Butler-Browne, GS & Lacasa, D (2015). Human adipocytes induce inflammation and atrophy in muscle cells during obesity. Diabetes 74(9), 31213134.CrossRefGoogle Scholar
Picchi, MG, Mattos, AM, Barbosa, MR, Duarte, CP, Gandini, MA, Portari, GV & Jordão, AA (2011). A high-fat diet as a model of fatty liver disease in rats. Acta Cir Bras 26, 2530.10.1590/S0102-86502011000800006CrossRefGoogle ScholarPubMed
Pimentel Neto, J, Rocha, LC, Klein, GB, Jacob, CdS, Krause Neto, W, Watanabe, I & Ciena, AP (2020). Myotendinous junction adaptations to ladder-based resistance training: Identification of a new telocyte niche. Sci Rep 10(1), 18.CrossRefGoogle ScholarPubMed
Pincu, Y, Linden, MA, Zou, K, Baynard, T & Boppart, MD (2015). The effects of high fat diet and moderate exercise on TGFβ1 and collagen deposition in mouse skeletal muscle. Cytokine 73(1), 2329.10.1016/j.cyto.2015.01.013CrossRefGoogle ScholarPubMed
Rassier, DE (2017). Sarcomere mechanics in striated muscles: From molecules to sarcomeres to cells. Am J Physiol Cell Physiol 313(2), C134C145.CrossRefGoogle ScholarPubMed
Ringseis, R, Mooren, F & Krüger, K (2015). Metabolic signals and innate immune activation in obesity and exercise. Exerc Immunol Rev 21, 5868.Google ScholarPubMed
Rocha, LC, Pimentel Neto, J, De Sant'Ana, JS, Jacob, CdS, Klein, GB, Krause Neto, W, Watanabe, I & Ciena, AP (2020). Repercussions on sarcomeres of the myotendinous junction and the myofibrillar type adaptations in response to different training on vertical ladder. Microsc Res Tech 83(10), 11901197.Google ScholarPubMed
Sierra, LR, Fávaro, G, Cerri, BR, Rocha, LC, Yokomizo de Almeida, SR, Watanabe, I & Ciena, AP (2018). Myotendinous junction plasticity in aged ovariectomized rats submitted to aquatic training. Microsc Res Tech 81(8), 816822.CrossRefGoogle Scholar
Tallis, J, James, RS & Seebacher, F (2018). The effects of obesity on skeletal muscle contractile function. J Exp Biol 221(13), 114.CrossRefGoogle ScholarPubMed
Tomlinson, DJ, Erskine, RM, Morse, DI, Winwood, K & Onambélé-Pearson, G (2016). The impact of obesity on skeletal muscle strength and structure through adolescence to old age. Biogerontology 17(3), 467483.CrossRefGoogle ScholarPubMed
Valeria, A, Cardile, A, Cozzi, V, Bracale, R, Tedesco, L, Pisconti, A, Palomba, L, Cantoni, O, Clementi, E, Moncada, S, Carruba, MO & Nisoli, E (2006). TNF-α downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116(10), 27912798.CrossRefGoogle Scholar
Wang, X, Zhao, D, Cui, Y, Lu, S, Gao, D & Liu, J (2019). Proinflammatory macrophages impair skeletal muscle differentiation in obesity through secretion of tumor necrosis factor-α via sustained activation of p38 mitogen-activated protein kinase. J Cell Physiol 234(3), 25662580.CrossRefGoogle ScholarPubMed