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Beef Extract Supplementation Increases Leg Muscle Mass and Modifies Skeletal Muscle Fiber Types in Rats

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Beef Extract Supplementation Increases Leg Muscle Mass and Modifies Skeletal Muscle Fiber Types in Rats J Nutr Sci Vitaminol, 52, 183–193, 2006 Beef Extract Supplementation Increases Leg Muscle Mass and Modifies Skeletal Muscle Fiber Types in Rats Hiroyuki YOSHIHARA1, Jun-ichiro WAKAMATSU1, Fuminori KAWABATA1, Sunao MORI1, Atsushi HARUNO1, Toshiya HAYASHI2, Takeshi SEKIGUCHI3, Wataru MIZUNOYA1, Ryuichi TATSUMI1, Tatsumi ITO1 and Yoshihide IKEUCHI1,* 1Department of Bioscience and Biotechnology, Graduate School of Agriculture, Kyushu University, Fukuoka 812–8581, Japan 2Department of Applied Biological Chemistry, Faculty of Agriculture, Meijo University, Nagoya 468–8502, Japan 3Ito Life Sciences Inc., Ibaraki 302–0104, Japan (Received August 15, 2005) Summary The objective of this research was to investigate the effects of beef extract on fat metabolism, muscle mass and muscle fiber types in rats. We also investigated the synergetic effect of endurance exercise. Twenty-four male rats weighing about 270 g were assigned to two diets containing 0 or 6% beef extract (BE). Half the rats fed each diet were subjected to compulsory exercise (CE) for 30 min every other day. After 4 weeks feeding, the blood was collected and various organs were dissected. The muscle fiber type of the soleus and extensor digitorum longus (EDL) muscles were evaluated by histochemical and electrophoretical analyses. Rats supplemented with BE showed a decrease in fat content in liver and abdomen and an increase in the activity of carnitine palmitoyl transferase II in liver. BE as well as exercise increased the relative weights of both soleus and EDL. BE alone and BE plus CE did not affect the distribution of muscle fiber types in soleus. BE without exercise decreased in type IIb of EDL from 54% to 44% with compensatory increase in type IIa from 41% to 49% and type I from 5% to 7% compared with the nonsupplemented, nonexercised control group. No synergetic effect on a fast to slow fiber conversion due to the combination of BE and CE was detected. Thus, BE supplement increased muscle mass and slow type fiber in EDL. The effects of BE supplement on muscle characteristics were similar to those of exercise. Key Words beef extract, fat metabolism, muscle fiber type, muscle mass, L-carnitine A great deal of research has been done to elucidate ral stimulation. Concretely, endurance exercise re- the general nutritional value of beef on the growth of quiring the consumption of oxygen stimulates a shift to human subjects and the effects of protein quality and the slow twitch, oxidative muscle fibers (8). The fiber exercise on the growth and protein metabolism of ani- types of adult skeletal muscle are closely related to mals and human beings (1–3). However, existing infor- energy metabolic characteristics as described above. mation about the nutritional effects of beef extract on Nutrition-induced regulation in mRNA levels for a muscle metabolism is not sufficient. number of metabolic genes have been well reported (9– Skeletal muscle is composed of at least three fiber 11). Thus, one question concerns whether the transfor- types on the basis of their contractile and energy meta- mation of muscle fiber type can be induced nutrition- bolic properties; type I fibers exhibit an aerobic energy ally. If this would be possible, the diet containing the metabolism (slow-twitch fiber), type IIb fibers are pre- compositions promoting the aerobic metabolism would dominantly glycolytic (fast-twitch fiber) and type IIa be expected to induce fast-slow fiber transformation. fibers are the intermediate type exhibiting both oxida- Beef extract is rich in L-carnitine as well as carnosine, tive and glycolytic metabolisms. Lipids are easily accu- taurine and creatinine. With regard to the relationship mulated in type I fibers (4), while glycogen depletion between carnitine metabolism and muscle fiber type, occurs primarily in the type II (5). It is well known that Constantin-Teodosiu et al. (12) have recently demon- cross-reinnervation, electrical stimulation or exercise strated that accumulation of acetyl-L-carnitine in evokes the fiber type conversion, although the molecu- humans is greater in type I fibers, in which the greater lar mechanisms mediating the transformation are not mitochondria responsible for oxidative metabolism was clearly elucidated (6, 7). This means that skeletal mus- present, than in type II fibers after an exhaustive pro- cle cells possess a capacity to respond and adapt to met- longed one-legged exercise at ~75% VO2max for about abolic changes imposed by physical stimulation or neu- 220 min. However, their report did not describe the relationship between carnitine intake and the fiber type *To whom correspondence should be addressed. transformation. They only suggested the physiological E-mail: [email protected] role of carnitine as a buffer agent neutralizing the 183 184 YOSHIHARA H et al. excess acetyl group occurring during prolonged exer- Table 1. The composition of two different diets, cise in type I fibers. To our knowledge, few studies have been so far conducted on the effect of nutrients such as Control diet Beef extract diet carnitine on muscle fiber type transformation, al- though undernutrition has been shown to induce an Casein 20 20 Beef extract concentration 0 6 increase in the proportion of slow type fiber (13–15). Olive oil 12 12 Thus, the present experiments were conducted to Sucrose 10 10 confirm the effect of beef extract on fats metabolism and Corn starch 50.9 44.9 anabolic action in rats, and then to examine whether or Cellulose powder 2 2 not the transformation from one type to another in the Mineral mixture 3.5 3.5 soleus and extensor digitorum longus (EDL) occurred in Vitamin mixture 1 1 response to the ingestion of beef extract as occurs with D,L-Methionine 0.3 0.3 exercise. Choline bitartrate 0.2 0.2 Cholesterol 0.1 0.1 MATERIALS AND METHODS Animals, diets and exercise. Wistar (7 wk old) male Total (g) 100 100 rats were purchased from a commercial supplier (Seac Yoshitomi Ltd., Fukuoka, Japan). They were individu- ally housed in stainless-steel wire-mesh cages in an ani- Table 2. The composiiton of beef extract concentration. mal room at 20˚C in 60% humidity under an artificial (%) lighting system of 12 h light and 12 h darkness in the animal raising facility of Biotron Institute of Kyushu Water 3.00 University. Rats were fed a commercial diet (Type MF of Proteins (including nitrogen compounds) 61.40 Lipids 0.00 Oriental Yeast Co. Ltd., Tokyo) and water for 1 wk in Carbohydrate 33.00 order to acclimate them to the environment. After pre- Ash 2.60 feeding, rats were divided into two groups. Twelve rats were assigned to the beef extract-supplemented diet and Total 100 the other twelve rats were given the nonsupplemented diet. Each dietary group was furthermore subdivided Carnitine 5.00 into aerobically exercised and nonexercised groups Anserine 0.45 (total 4 groups); Control: nonexercised, nonsupple- Carnosine 4.95 mented, BE: nonexercised, supplemented, CE: exercised, Taurine 2.82 nonsupplemented, BEϩCE: exercised, supplemented. Creatine 1.51 Exercised subjects engaged in compulsory exercise for Creatinine 7.29 Phosphoric acid 1.55 30 min every other day with a treadmill running tool Lactic acid 8.14 having 5% grade and 15 m/min speed and this protocol Sodium 0.70 was assumed as low intensity endurance exercise com- pared with previous reports (16). The body weight of each group at the beginning of the experiment (after pre-feeding) was adjusted to be as identical as possible and EDL muscles were harvested, weighed, individually [276.8Ϯ9.4 (SD) g in Control, 265.6Ϯ17.4 g in BE, quick frozen by placing them in a dry ice-isopenthane 275.1Ϯ10.8 g in CE, 265.2Ϯ13.7 g in BEϩCE]. Beef mixture, and then stored at Ϫ35˚C for histochemical extract (Ito Life Sciences Inc.) was added to the diets to analysis. achieve a concentration of 6%, which corresponded to All experimental procedures were performed accord- 0.3% L-carnitine. The composition of the two different ing to the guideline for Animal Experiment in the Fac- diets is given in Table 1. Table 2 shows the result of com- ulty of Agriculture and the Graduate Course of Kyushu ponential analysis of beef extract by Ito Life Sciences University and the law [No. 105] and notification [No. Inc. 1] of the Japanese Government. Rats were fed for 4 wk and were given free access to Measurement of fat content and fatty acid analysis. the diets and water supply. Food intake and body weight Lipids were extracted from serum, abdominal fat, liver of each rat were recorded every other day. After 4 weeks and muscle by the method of Folch et al. (17). Fat con- feeding, urine was collected for quantifying carnitine tent was quantified gravimetrically after evaporation of concentration. Food was removed 24 h before killing, the solvent (chloroform-methanol mixture) in the and the rats were killed after anesthetizing them with extracted lipids by freeze-drying. Fatty acid composition ethyl ether. The blood was collected by bleeding from of extracted fat was analyzed by gas chromatography the carotid artery. Sera were collected from the blood by (GC-14B, Gas Chromatograph, Shimazu Co. Ltd., Japan) centrifugation at 3,000 rpm for 10 min, and were kept according to the method described previously (18). at Ϫ80˚C until use for assays. Visible abdominal fat, Measurement of carnitine concentrations in serum and liver and other organs were carefully removed from car- urine. L-Carnitine in the serum and urine was deter- cass, weighed and frozen in liquid nitrogen. The soleus mined by the method of a combination of carnitine Beef Extract Diet and Muscle Fiber Type 185 acetyl transferase and acetyl CoA synthase method conditions. Type II fibers were further divided into type using Roche Kit No.
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