Effects provoked by chronic undernourishment on the fibre type composition and contractility of fast muscles in male and female developing ratsby J. Pereyra-Venegas, B. Segura-Alegría, J. C. Guadarrama-Olmos, S. Mariscal-Tovar, S. Quiróz-González, I. Jiménez-Estrada

J Anim Physiol Anim Nutr

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Year
2014
DOI
10.1111/jpn.12274
Subject
Food Animals / Animal Science and Zoology

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ORIGINAL ARTICLE

Effects provoked by chronic undernourishment on the fibre type composition and contractility of fast muscles in male and female developing rats

J. Pereyra-Venegas1,2, B. Segura-Alegrıa1, J. C. Guadarrama-Olmos3, S. Mariscal-Tovar3, S. Quiroz-Gonzalez4 and I. Jimenez-Estrada3 1 Departamento de Biologıa, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autonoma de Mexico Tlalnepantla de Baz, Estado de

Mexico, Mexico 2 Instituto de Fisiologıa Celular, Universidad Nacional Autonoma de Mexico Mexico City, Mexico 3 Departamento de Fisiologıa, Biofısica y Neurociencias, Centro de Investigacion y Estudios Avanzados del Instituto Politecnico Nacional, San Pedro

Zacatenco, Del. Gustavo A. Madero., Mexico City, Mexico, and 4 Departamento de Acupuntura y Rehabilitacion, Universidad Estatal del Valle de Ecatepec, Valle de Anahuac, Ecatepec, Estado de Mexico, Mexico

Summary

In this study, we compare the effects of pre- and post-natal food deprivation on the relative proportion of fibre types and contractile responses in the extensor digitorum longus (EDL) muscle of female and male rats at different post-natal ages. EDL muscles from undernourished male (UM) rats showed a higher proportion of Type IIB than IIA fibres and larger normalized twitch responses (with respect to muscle weight) than those of controls (CM). In contrast, EDL muscles from control (CF) and undernourished female rats (UF) showed no significant differences in their fibre type composition and normalized twitch forces at most of the ages analysed. Our data are indicative that the EDL muscles from undernourished males are more susceptible to the effects exerted by low food income than the EDL muscles from female rats. It is proposed that changes in the reactive oxygen species (ROS) concentration and hormonal factors, due to undernutrition, are involved in the alterations observed in the fibre type composition and force production of EDL muscles in undernourished male rats and that estrogens may have an antioxidant protective role on the undernourished EDL muscles in female rats.

Keywords contractility, muscle fibres, gender, undernutrition, development

Correspondence I. Jimenez-Estrada, Departamento de Fisiologıa, Biofısica y Neurociencias, Centro de Investigacion y Estudios Avanzados del

Instituto Politecnico Nacional. Av. Instituto Politecnico Nacional 2508 Col. San Pedro Zacatenco, CP 07360, Mexico. Tel: 52 (55) 57473363;

Fax: 52 (55) 57473754; E-mail: ijimenez@fisio.cinvestav.mx

Abbreviations CM, control male; UM, undernourished male; CF, control female; UF, undernourished female; EDL, extensor digitorum longus; AT, total transversal area occupied by all fibres; AI, muscle transversal area occupied by Type I fibres; PN, post-natal age; MLC, Myosin light chains; MHC,

Myosin heavy chains; ROS, reactive oxygen species.

All authors contributed equally to the study.

Received: 18 November 2013; accepted: 27 October 2014

Introduction

Inadequate food consumption of mothers during critical stages of development (primarily pregnancy and lactation) leads to considerable alterations in the morphological, biochemical and functional properties of skeletal muscles in the offspring (Lennmarken et al., 1984; Young et al., 1990). Previous studies have shown that muscles that are mostly composed of fast fibres, such as the extensor digitorum longus (EDL) muscle (Soukup et al., 2002), are more affected by low food intake than muscles primarily composed of slow fibres (e.g. the soleus muscle) (Wareham et al., 1982; Dwyer et al., 1994). Such alterations include reduced muscle weight (Goldspink and Ward, 1979;

Bedi, 1994) and changes in the fibre type composition (White et al., 2000; Toscano et al., 2008). Furthermore, dietary restrictions produce significant changes in the mechanical properties of fast muscles, primarily force generation (Wareham et al., 1982; Bissonette

Journal of Animal Physiology and Animal Nutrition © 2014 Blackwell Verlag GmbH 1

DOI: 10.1111/jpn.12274 et al., 1997) and fatigability (Sieck et al., 1989; Prakash et al., 1993).

It is well known that the hypothalamic–pituitary– gonadal axis is negatively influenced by undernutrition during the rat perinatal development (Rhind et al., 2001). Such alteration leads to a reduction in estradiol and testosterone serum concentrations (Teixeira et al., 2007) and induce changes in the relative proportion of fibre types in muscles of male rats (Rajikin, 1984; D’Albis and Butler-Browne, 1993).

On the other side, estrogens exert a protective antioxidant effect in muscles (Zhang et al., 2007; Tiidus, 2011). According to the later, it is expected that preand post-natal food restriction affect most the structure and function of male muscles than those of female muscles. Because most of the studies about the effect of undernutrition on muscles have been conducted in male rats in consequence, there is a lack of experimental evidence regarding the effect of food deprivation on the muscles of female rats. In this study, we analyse the effects of pre- and postnatal food restriction on the histoenzymatic and functional characteristics of the EDL muscle in male and female rats at several post-natal ages. It was observed that a severe chronic food restriction produce larger changes on the fibre type composition and contractile properties of male muscles than in female muscles.

Materials and methods

Animals

All of the experiments were performed in accordance with the guidelines contained in the Guide for the

Care and Use of Laboratory (National Research Council, 2010; National Institutes of Health, Bethesda, MD,

USA; Animal Welfare Assurance #A5036-01), and the animal protocols were approved by the Institutional

Bioethical Committee for the Care and Handling of

Laboratory Animals (UPEAL-Protocol 013-02, CINVESTAV).

Two groups of female Wistar rats (mean body weight: 257.4  16.3 g) were subjected to the following feeding conditions: (i) Control group (C): Adult female rats (n = 16) and their offspring had free access to commercial food (Formulab 5008, Lab diet, Framingham, MA, USA). (ii) Chronic undernourished rats (U): Adult female rats (n = 18) were fed with approximately half of the mean food intake of the control animals, starting 2 weeks before mating and continuing during pregnancy and lactation (QuirozGonzalez et al., 2013). At the second post-partum