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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 64  |  Issue : 5  |  Page : 211-217

Mealworm (Tenebrio molitor)-derived protein supplementation attenuates skeletal muscle atrophy in hindlimb casting immobilized rats


1 Department of Physiology, College of Medicine, Soonchunhyang University, Cheonan, Korea
2 Department of Sports Science, Institute of Sports Health Science, Sunmoon University, Asan, South Korea

Date of Submission28-May-2021
Date of Decision25-Aug-2021
Date of Acceptance02-Oct-2021
Date of Web Publication27-Oct-2021

Correspondence Address:
Dr. Young-Ju Song
Institute of Sports Health Science, Sunmoon University, Asan 31460
South Korea
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/cjp.cjp_40_21

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  Abstract 


This study aimed to investigate the effect of mealworm (Tenebrio molitor) derived protein supplementation on skeletal muscle atrophy of hindlimb casted immobilized rats. Twenty-four six-week-old male Sprague-Dawley rats were randomly divided into three groups: control sedentary group (CD, n = 8), control diet casting group (CDC, n = 8), and the mealworm-derived protein supplemented casting group (MDC, n = 8). CD and CDC group was supplemented AIN-76G diet and mealworm-derived protein supplemented diet for MDC group was substituted as 5% casein protein to 5% mealworm protein for 5 weeks and left hindlimb casting immobilization using casting tape for CDC and MDC group was done 1 week before sacrifice. After 5 weeks of mealworm supplementation, the soleus muscle weight of the MDC group was significantly higher compared to the CDC group. In addition, the level of muscle protein synthesis factors p-Akt/Akt, p-4EBP1/4EBP1, and p-S6K/S6K significantly increased in the MDC group compared to the CDC group. On contrary, the level of muscle protein degradation factors (MuRF1 and atrogin-1) was significantly lower in the MDC group than that of the CDC group. These results suggest that mealworm-derived protein supplementation may have a significant role in the prevention of skeletal muscle atrophy via stimulation of muscle protein synthesis factors and inhibition of muscle protein degradation factors, and therefore a promising intervention in sarcopenia.

Keywords: Hindlimb casted immobilized rat, immobilization, mealworm, muscle atrophy, sarcopenia


How to cite this article:
Lee JB, Kwon DK, Jeon YJ, Song YJ. Mealworm (Tenebrio molitor)-derived protein supplementation attenuates skeletal muscle atrophy in hindlimb casting immobilized rats. Chin J Physiol 2021;64:211-7

How to cite this URL:
Lee JB, Kwon DK, Jeon YJ, Song YJ. Mealworm (Tenebrio molitor)-derived protein supplementation attenuates skeletal muscle atrophy in hindlimb casting immobilized rats. Chin J Physiol [serial online] 2021 [cited 2021 Nov 27];64:211-7. Available from: https://www.cjphysiology.org/text.asp?2021/64/5/211/329359




  Introduction Top


Sarcopenia is a syndrome characterized by a reduction of skeletal muscle volume and dysfunction of skeletal muscle,[1] and it is significantly associated with physical disability, poor quality of life, and mortality.[2],[3],[4]

While it is prevalent in the older population, factors that cause muscle atrophy have been reported as a predisposition to sarcopenia.[2],[3],[4] Muscle atrophy is known to be influenced by the balance between the rate of protein degradation and protein synthesis.

So far, there is no specific treatment for sarcopenia and management is mostly through non-pharmacological interventions. Regular resistant exercise in combination with adequate nutritional supplementation, in particular, creatine, protein, and leucine seem to have been reported as successful interventions in the improvement of muscle mass, muscle strength, and physical fitness.[5],[6]

Previous studies have suggested that maintaining adequate protein intake may help preserve muscle volume, and strength in both young adults, and the elderly.[7],[8] However, there are not enough studies on the specific types of proteins that prevent muscle atrophy. Recently, edible insects have been demonstrated as an alternative protein source worldwide, both as a delicacy and as emergency nutrition[9] and the consumption of edible insects has been supported by international organizations such as the Food and Agricultural Organization[10] and the European Commission.

Edible insects have been known to various advantages to human health. As an alternative protein source, insect protein is currently gaining attention as human food in many countries, especially in Africa, Asia, and Latin America due to the high protein content.[11] In addition, edible insects have been shown to the effect of immunostimulatory and anti-cancer properties,[12] antidiabetic properties,[13] and antioxidant properties.[14]

Mealworm (Tenebrio molitor), an edible insect, has attracted particular interest as a potential candidate for protein supplement due to its high content of proteins and micro-nutrients.[15],[16] An in vitro experiment by Kim et al. reported that protein hydrolysate from mealworm is easily digested and absorbed, and has high myogenic potential.[17] In addition, we reported that mealworm-derived protein supplementation showed the anti-obesity effect on sarcopenic obese rats through skeletal muscle peroxisome proliferator-activated receptor-γ coactivator (PGC)-1α activation.[18] Mealworm has also been reported to have antimicrobial and antioxidant properties.[19],[20]

While accumulating evidence indicates that protein supplementation has possible anti-sarcopenic and anti-dynapenic effects studies on mealworm-derived protein benefits are limited. Herein, we investigated the effects of mealworm-derived protein supplementation on skeletal muscle signaling pathways involved in protein metabolism, in rats with hindlimb suspension-induced atrophy. We hypothesized that short-term “mealworm-derived protein” supplementation would attenuate the skeletal muscle mass loss by preventing the changes in protein metabolism signaling induced by short-term disuse in casting-induced hindlimb immobilized rats.


  Materials and Methods Top


Animals

All experimental protocols were approved by the animal study committee of Sunmoon University in Asan, Republic of Korea (SM-2018-01-02). Twenty-four five weeks old male Sprague-Dawley rats were purchased from Samtaco Bio Korea (Hwaseong, Korea). Following a one-week acclimation period, the rats were randomly divided into three groups: the CD, control sedentary group (n = 8); the CDC (control diet casting group: n = 8); and the MDC (mealworm-derived protein supplemented casting group: MDC, n = 8). The rats were housed in individual cages at controlled temperatures (23°C ± 1°C) and humidity (50 ± 5%) with a 12-h light-dark cycle. The food efficiency ratio was calculated as the total weight gain divided into total food intake for the experimental period.

Diets

The rats were provided free access to tap water and food for 5 weeks. The control diet was composed of 20% protein, 5% fat, 60% carbohydrates, 5% fiber, 3.5% minerals, and 1.0% vitamin mix based on the AIN-76G diet. Mealworm-derived protein supplemented diet was substituted as 5% casein protein to 5% mealworm protein. Mealworm larvae were purchased from local insect farmers (S-Worm, Chunan, Korea). Mealworm larvae were frozen with liquid nitrogen and stored at −22°C. Dried mealworm larvae were mixed with 1 L of extraction solvent (99.5% of ethanol) at solid-liquid ratio of 1:5 and defatted by ultra-sonicator at 70°C for 4 h. To use the deffated mealworm larvae as an animal feed, fat was removed using an environmentally friendly solvent, 99.5% of ethanol. After extraction, deffated mealworm larvae were left to settle down at 5000 × g for 30 min, pellet was obtained and it was dried at 60° C for 24 h. Then, protein analysis was done using the Kjeldahl method.

Casting-induced hindlimb immobilization

After feeding on the experimental diets for 4 weeks, unilateral hindlimb immobilization was performed on the left hindlimb as described previously.[21] Briefly, the rats were anesthetized lightly with diethyl ether to allow attachment of the casting material. The left hindlimb was fixed in a shortened position with complete plantar flexion of the ankle joint, using casting tape (Scotchcast Plus-J; 3M Health Care, St. Paul, MN, USA). The casting material was assessed for damage daily and repaired as required. The rats were immobilized for 7 days. After 5 weeks of the experimental procedure, rats were anesthetized with diethyl ether after an overnight fast. Blood was drawn from the left ventricle of the heart, and serum was collected by centrifugation of blood samples at 2000 g for 20 min at 4°C. Skeletal muscle and the other organs were dissected and immediately immersed in liquid nitrogen. The serum and tissues were stored at –70°C until the analysis.

Biochemical assay of serum components

Serum glucose, total cholesterol, triglyceride, and high-density lipoprotein cholesterol (HDLC) levels were analyzed using commercial enzymatic kits (Asan Pharmaceutical, Yongin, South Korea)

Western blotting assay

The total soleus muscle protein was extracted and prepared according to Baghirova et al.[22] The protein concentration was determined by the Bradford reagent (Bio-rad, Hercules, CA, USA). Briefly, proteins were transferred to polyvinylidene difluoride membranes (Millipore, Bedford, MA, USA) and blocked for 1 h at room temperature in 5% BSA using Tris-buffered saline in Tween-20 (TBST). Primary antibodies used included: p-Akts473 (Cell Signaling, Beverly, MA, USA), Akt (Cell Signaling, Beverly, MA, USA), FoxO1 (Cell Signaling, Beverly, MA, USA), MuRF1 (Abcam, Cambridge, MA, USA), or atrogin-1 (Abcam), 4EBP1 (Cell Signaling, Beverly, MA), p-4EBP1Thr37/46 (Cell Signaling), S6K (Cell Signaling, Beverly, MA), p-S6KThr389 (Cell Signaling). Primary antibody reactions were performed for 2 h at room temperature in 5% BSA, followed by incubation with a secondary antibody of either HRP-conjugated anti-goat IgG or anti-rabbit IgG (Santa Cruz, CA, USA) for 1 h. The target proteins were identified using an ECL kit (GE Healthcare, Buckinghamshire, UK). The obtained films were then scanned (Pixma E510 scanner, Canon Inc., Japan) and densitometric analysis of the bands was performed with the Quantity One program (Bio-rad, Hercules, CA, USA).

Statistical analysis

All data were analyzed using SPSS software version 15.0 for Windows (SPSS, Chicago, IL, USA). The data are expressed as the mean ± SE and the values were analyzed using one-way ANOVA, followed by the LSD (least significant difference) test. Significance was defined as α = 0.05.


  Results Top


Body weight and food intake

As shown in [Table 1], the final bodyweight of the CDC group was significantly lower compared to the CD group (P < 0.05), however, there was no significant difference between the final weight of the MDC group, and the CD and CDC group. There were no significant differences in food intake among the groups. However, for the food efficiency ratio, the value of the CD group was significantly higher than that of the CDC and MDC groups (P < 0.05).
Table 1: Effects of mealworm-derived protein supplementation on body weight, food intake, and food efficiency ratio

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Tissue weight

The results of tissue weight are shown in [Table 2]. There were no significant differences among the groups in the weight of fat pad and kidney. The cardiac muscle weight of the CD and MDC groups was significantly higher than that of the CDC group (P < 0.05). However, the liver weight of the CDC and MDC groups was significantly lower than that of the CD group (P < 0.05). For the soleus muscle weight, the value of the CD group was significantly higher than that of the CDC and MDC groups (P < 0.05), and the value of the MDC group was significantly higher than that of the CDC group (P < 0.05).
Table 2: Effects of mealworm-derived protein supplementation on tissue weights

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Serum components

As shown in [Table 3], the serum glucose level of the CDC group was significantly higher than that of the CD and MDC groups (P < 0.05). In addition, the HDLC levels of the CDC and MDC groups were significantly lower than that of the CD group (P < 0.05). However, there were no significant differences in serum triglyceride and TC levels among the groups.
Table 3: Effects of mealworm-derived protein supplementation on serum components

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Atrophy-related protein expression of skeletal muscle

Akt, p-Akt protein expression and p-Akt/Akt

The results of Akt, p-Akt protein expression, and p-Akt/Akt of soleus muscle are presented in [Figure 1]. For the Akt protein expression, there were no significant differences among the groups. However, the value of p-Akt protein expression in the CD group was significantly higher than that of the CDC and MDC groups (P < 0.01). In addition, the value of p-Akt protein expression in the MDC group was significantly higher than that of the CDC group (P < 0.05).
Figure 1: Effects of mealworm-derived protein supplementation on Akt, p-Akt protein expression, and Akt/p-Akt. CD: Control diet sedentary group, CDC: Control diet casting group, MDC: Mealworm diet casting group. Data values were expressed as the mean ± SE. At *P < 0.05 and **P < 0.01 for difference between groups.

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FoxO1 protein expression

As shown in [Figure 2], the value of FoxO1 protein expression in the CDC group was significantly higher compared to that of the CD and MDC groups (P < 0.05, P < 0.01, respectively). The value of FoxO1 protein expression in the MDC group was significantly lower compared to the value of the CD group (P < 0.05).
Figure 2: Effects of mealworm-derived protein supplementation on FoxO1 protein expression. CD: Control diet sedentary group, CDC: Control diet casting group, MDC: Mealworm diet casting group. Data values were expressed as the mean ± SE. At *P < 0.05 and **P < 0.01 for difference between groups.

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MuRF1 and atrogin-1 protein expression

The results of MuRF1 and atrogin-1 protein expression are shown in [Figure 3]. The value of MuRF1 protein expression in the CDC group was significantly higher compared to that of the CD and MDC groups (P < 0.01, P < 0.05, respectively) and the value of MuRF1 protein expression in the MDC group were significantly higher compared to that of the CD group (P < 0.01). The value of atrogin-1 protein expression in the CDC group was also significantly higher compared to that of the CD and MDC groups (P < 0.01).
Figure 3: Effects of mealworm-derived protein supplementation on MuRF1 and atrogin-1 protein expression. CD: Control diet sedentary group, CDC: Control diet casting group, MDC: Mealworm diet casting group. Data values were expressed as the mean ± SE. At *P < 0.05 and **P < 0.01 for difference between groups.

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4EBP1, p-4EBP1 protein expressions, and p-4EBP1/4EBP1

The results of 4EBP1, p-4EBP1 protein expressions, and p-4EBP1/4EBP1 are shown in [Figure 4]. The value of 4EBP1 protein expression in the MDC group was significantly higher compared to the CD and CDC groups (P < 0.01).
Figure 4: Effects of mealworm-derived protein supplementation on 4EBP1, p-4EBP1 protein expressions and p-4EBP1/4EBP1. CD: Control diet sedentary group, CDC: Control diet casting group, MDC: Mealworm diet casting group. Data values were expressed as the mean ± SE. At *P < 0.05 and **P < 0.01 for difference between groups.

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The value of p-4EBP1 protein expression in the CD group was significantly higher compared to the value of the CDC and MDC groups (P < 0.01). In addition, the value of p-4EBP1 protein expression in the MDC group was significantly higher compared to that of the CDC (P < 0.05). For p-4EBP1/4EBP1, the value of the CDC group was significantly lower compared to the value of CD and MDC groups (P < 0.01). Furthermore, the value of p-4EBP1/4EBP1 in the MDC group was significantly higher compared to that of the CDC group (P < 0.01) and significantly lower compared to that of the CD group (P < 0.05).

S6K, p-S6K protein expressions, and p-S6K/S6K

The results of s6K, p-S6K protein expressions, and p-S6K/S6K are shown in [Figure 5]. For the S6K protein expression, there were no significant differences among the groups. The value of p-S6K protein expression in the CDC group was significantly lower compared to the CD and MDC groups (P < 0.01). For p-S6K/S6K, the value of the CDC group was significantly lower compared to the value of CD and MDC groups (P < 0.01). Furthermore, the value of p-S6K/S6K in the MDC group was significantly lower compared to that of the CD group (P < 0.01).
Figure 5: Effects of mealworm-derived protein supplementation on S6K, p-S6K protein expressions, and p-S6K/S6K. CD: Control diet sedentary group, CDC: Control diet casting group, MDC: Mealworm diet casting group. Data values were expressed as the mean ± SE. At **P < 0.01 for difference between groups.

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  Discussion Top


In the present study, we demonstrated the effect of mealworm-derived protein supplementation on muscle atrophy in casting-induced hindlimb immobilized rats. Our findings suggested that mealworm-derived protein supplementation may have a significant role in the prevention of skeletal muscle atrophy via stimulation of muscle protein synthesis factors and inhibition of muscle protein degradation factors, in the hindlimb casting immobilized rat.

In the present study, the final body weight of the CDC group was significantly lower compared to the CD group and a similar trend was also observed in the MDC group. These results are due to the food efficiency ratio, as shown in [Table 1]. It is also assumed that the reduction in heart and liver weights in the casting groups is due to reduced body weight with decreased food efficiency ratio. In addition, in the present study, serum glucose level was increased and serum HDLC level was decreased in the CDC group compared to the CD group. Similar to our study, Pan et al.[23] reported that increased serum glucose level and decreased serum HDLC level in immobilization-stressed rats. These results are assumed that consistent with the reduced weight gain and lower food intake in addition to increased serum corticosterone level by immobilization in the casting group.

In previous studies, Jones et al.[24] reported that soleus muscle has more active PI3K/Akt/mTOR pathway, greater inhibition of GSK3β, increased in β-catenin levels compared to fast-twitch muscle type and result in more active hypertrophic response. Therefore, we evaluated hypertrophic response in response to mealworm-derived protein supplementation in soleus muscle.

Similar to the previous studies, in our present study, the weight of the soleus muscle was reduced by casting immobilization.[25],[26] However, in the present study, 1 week after immobilization, dietary mealworm-derived protein intake significantly increased the weight of soleus muscles as compared with casein intake in immobilized rats. This suggests that the mealworm-derived protein supplementation on skeletal muscle would be more effective than casein supplementation in the recovery of atrophy. Our result also suggests that mealworm-derived protein supplementation may exert stimulatory effects on skeletal muscle weights. Therefore, dietary mealworm-derived protein supplementation may be an alternative approach to stimulate muscle recovery for sarcopenia patients.

The mealworm nutrition is composed of 47%–55% protein, 27%–38% lipid, and 5%–15% carbohydrate making it an excellent future alternative source of protein.[27] Better still, defatted mealworms have a very high content of protein, and the protein extract obtained is an essential amino acids-rich ingredient suitable for various food applications.[28] In addition, previous studies reported excellent ileal digestibility and growth performance in mealworm supplementation; up to 6% dried mealworm in weaning pigs' diet improves growth performance and nutrient digestibility without any detrimental effect on immune responses.[29],[30]

Muscle atrophy interferes with the intramuscular muscle protein synthesis and degradation pathway. In the present study, mealworm supplemented rats increased p-Akt protein expression, p-Akt/Akt and p-4EBP1 protein expression, p-4EBP1/4EBP1 and p-S6K protein expression, p-S6K/S6K, and decreased FoxO1 protein expression contrary to the casted rats. In addition, MuRF1 and atrogin-1 protein expression of mealworm supplemented rats were significantly decreased compared to casted rats. These results suggest that mealworm-derived protein stimulates skeletal muscle protein synthesis and inhibits skeletal muscle protein degradation. Similar to our findings, Kim et al.[17] reported that mealworm larvae protein hydrolysate had a high capacity of myogenesis and decreased proinflammatory cytokines such as interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-α), and IL-1β, which increase proteolysis and muscle atrophy in vitro. In addition, another study also reported that defatted mealworm fermentation extract enhanced the antioxidant defense system by elevating the level of glutathione and glutathione reductase activity, and at the same time attenuated the inflammatory response by downregulating proinflammatory cytokines such as a TNF-α and IL-6 in chronic alcohol-fed rats.[31]


  Conclusion Top


Mealworm-derived protein supplementation is a promising intervention for the prevention of skeletal muscle atrophy, in sarcopenia through stimulation of muscle protein synthesis factors and inhibition of muscle protein degradation factors.

However, in this study, only soleus muscle, slow-twitch fiber, was assessed on the effect of the supplementation of mealworm-derived protein on skeletal muscle atrophy. Therefore, more various muscle types should be studied to prevent skeletal muscle atrophy in future study.

In addition, in future research, various edible insects including sluggard, locusts, cricket should be assessed for the prevention of skeletal muscle atrophy as an alternative protein.

Acknowledgments

This work was supported by the Sun Moon University Research Grant of 2019.

Financial support and sponsorship

This work was supported by the Sun Moon University Research Grant of 2019.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

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