Effects of Dietary Protein Levels on Muscle Tissue Characteristics, Protein Turnover and Muscle Growth-Related Genes Expressions in Triploid Rainbow Trout

LI Xiaohua; TIAN Haining; LI Changzhong; MA Rui; MENG Yuqiong

doi:10.3969/j.issn.1006-267x.2022.05.046

2022 , Vol. 34 >Issue 5: 3194 - 3207

DOI: https://doi.org/10.3969/j.issn.1006-267x.2022.05.046

RESEARCH PAPER

Effects of Dietary Protein Levels on Muscle Tissue Characteristics, Protein Turnover and Muscle Growth-Related Genes Expressions in Triploid Rainbow Trout

LI Xiaohua ,
TIAN Haining ,
LI Changzhong ,
MA Rui ,
MENG Yuqiong

Expand

1. Provincial and Ministry Jointly Build the State Key Laboratory of Sanjiangyuan Ecology and Plateau Agriculture, Qinghai University, Xining 810016, China;
2. College of Ecological Environmental Engineering, Qinghai University, Xining 810016, China

Received date: 2021-09-27

Online published: 2022-05-14

Fold

Abstract

The study was aimed to explore the effects of dietary protein levels on muscle tissue characteristics, protein turnover and muscle growth-related genes expressions in triploid rainbow trout. Three isolipid and isoenergetic diets were formulated to contain 35.4% (low protein group), 45.8% (medium protein group) and 52.4% (high protein group) protein levels. A total of 1 200 triploid rainbow trout with an initial body weight of (232.8±0.1) g were randomly divided into 3 groups with 4 replicates per group and 100 fish per replicate. The experiment lasted for 80 days. The results showed as follows:1) compared to the medium and high-protein groups, the muscle fiber density and number were significantly increased in the low protein group (P<0.05). No difference was observed in the proportion of muscle fibers with a muscle fiber diameter (D) ≤ 20 μm among all groups (P>0.05). The proportion of muscle fibers with 120 μm 160 μm was the lowest in the low protein group (P<0.05). 2) With the increase of dietary protein levels, the growth hormone receptor (GHR), insulin-like growth factor Ⅰ (IGFⅠ) and insulin-like growth factor receptor Ⅰ (IGFRⅠ) gene relative expression levels increased and decreased thereafter, there were significantly different among groups (P<0.05), and reached the maximum in medium protein group. The myogenic differentiation antigen (Myod), myogenic regulatory factor 4 (Mrf4), myodifferentiation factor 5 (Myf5) and myogenin (Myog) gene relative expression levels of muscle increased with the increase of dietary protein levels (P<0.05). 3) In the protein synthesis pathway, the ratio of phosphorylated to total protein (p-AKT/AKT) of protein kinase B (AKT) in medium and high protein groups was significantly higher than that in low protein group (P<0.05). With the dietary protein levels increasing, the ratio of phosphorylated to total protein (p-TOR/TOR and p-4Ebp1/4Ebp1) of target rapamycin (TOR) and eukaryotic translation initiation factor 4E-binding protein 1 (4Ebp1) increased firstly and then decreased, there were significantly difference among groups (P<0.05), and reached the maximum in medium protein group. For the protein degradation pathway, with the dietary protein levels increasing, the autophagy related protein 12l (Atg12l) gene relative expression levels of muscle increased with the increase of dietary protein levels (P<0.05). The calpains 2 (Capn2) gene relative expression level in the high protein group was significantly higher than that in the low and medium protein groups (P<0.05); at the same time, the short isoforms of calpastatin (Cast-s) and long isoforms of calpastatin (Cast-l) gene relative expression levels of muscle increased then decreased thereafter with the increase of dietary protein levels (P<0.05). The muscle atrophy F-box protein 25 (Fbx25) gene relative expression level was firstly decreased and then increased, and medium protein group was significantly lower than low protein group (P<0.05). In summary, when the dietary protein level increase to 45.8%, it can promote the increase of muscle fiber, but has no effect on the proliferation of muscle fiber. Dietary protein level regulates muscle fiber enlargement by regulating myogenic regulatory factor and growth hormone-insulin-like growth factor pathways. When dietary protein level increases to 45.8%, muscle protein metabolism can be promoted. The decomposing pathways of muscle protein are different in different dietary protein level groups.

Key words： protein; triploid rainbow trout; muscle tissue characteristics; protein turnover; muscle growth

Cite this article

LI Xiaohua , TIAN Haining , LI Changzhong , MA Rui , MENG Yuqiong . Effects of Dietary Protein Levels on Muscle Tissue Characteristics, Protein Turnover and Muscle Growth-Related Genes Expressions in Triploid Rainbow Trout[J]. Chinese Journal of Animal Nutrition, 2022 , 34(5) : 3194 -3207 . DOI: 10.3969/j.issn.1006-267x.2022.05.046

References

[1] 孙德文, 詹勇, 许梓荣.日粮营养素对水产动物免疫机能的影响[J].饲料研究, 2003(2):45-46. SUN D W, ZHAN Y, XU Z R.Effects of dietary nutrients on immune function of aquatic animals[J].Feed Research, 2003(2):45-46.(in Chinese)
[2] GAO Y J, LU S D, WU M J, et al.Effects of dietary protein levels on growth, feed utilization and expression of growth related genes of juvenile giant grouper (Epinephelus lanceolatus)[J].Aquaculture, 2019, 504:369-374.
[3] LIU G X, WANG L, YU H X, et al.Effects of dietary protein levels on growth performance, digestibility, anti-oxidative responses and expressions of growth-related genes in triploid rainbow trout Oncorhynchus mykiss farmed in seawater[J].Aquaculture Nutrition, 2021, 27(4):998-1008.

[4] 石军, 褚武英, 张建社.鱼类肌肉生长分化与基因表达调控[J].水生生物学报, 2013, 37(6):1145-1152. SHI J, CHU W Y, ZHANG J S.Muscle growth, differentiation and gene expression regulation in fish[J].Acta Hydrobiologica Sinica, 2013, 37(6):1145-1152.(in Chinese)
[5] KNUTSEN H R, OTTESEN O H, PALIHAWADANA A M, et al.Muscle growth and changes in chemical composition of spotted wolffish juveniles (Anarhichas minor) fed diets with and without microalgae (Scenedesmus obliquus)[J].Aquaculture Reports, 2019, 13:100175.
[6] CHOI Y M, KIM B C.Muscle fiber characteristics, myofibrillar protein isoforms, and meat quality[J].Livestock Science, 2009, 122(2/3):105-118.
[7] JOHNSTON I A, ALDERSON R, SANDHAM C, et al.Muscle fibre density in relation to the colour and texture of smoked Atlantic salmon (Salmo salar L.)[J].Aquaculture, 2000, 189(3/4):335-349.
[8] JIANG Q, YAN M Y, ZHAO Y, et al.Dietary isoleucine improved flesh quality, muscle antioxidant capacity, and muscle growth associated with AKT/TOR/S6K1 and AKT/FOXO3a signaling in hybrid bagrid catfish (Pelteobagrus vachelli♀×Leiocassis longirostris♂)[J].Journal of Animal Science and Biotechnology, 2021, 12(1):53.
[9] ZHAO Y, JIANG Q, ZHOU X Q, et al.Effect of dietary threonine on growth performance and muscle growth, protein synthesis and antioxidant-related signalling pathways of hybrid catfish Pelteobagrus vachelli♀×Leiocassis longirostris♂[J].British Journal of Nutrition, 2020, 123(2):121-134.

[10] 马骏, 柳阳, 李勇, 等.脂肪和蛋白质营养对工业化养殖大西洋鲑相关代谢酶和生长基因表达的影响[J].中国水产科学, 2017, 24(4):669-680. MA J, LIU Y, LI Y, et al.Effects of dietary fat and protein nutrition on fat metabolic enzymes and growth-associated gene expression of Atlantic salmon (Salmo salar) in the recirculating aquaculture system[J].Journal of Fishery Sciences of China, 2017, 24(4):669-680.(in Chinese)
[11] ALAMI-DURANTE H, CLUZEAUD M, BAZIN D, et al.Muscle growth mechanisms in response to isoenergetic changes in dietary non-protein energy source at low and high protein levels in juvenile rainbow trout[J].Comparative Biochemistry and Physiology.Part A, Molecular & Integrative Physiology, 2019, 230:91-99.
[12] MA R, LIU X H, MENG Y Q, et al.Protein nutrition on sub-adult triploid rainbow trout (1):dietary requirement and effect on anti-oxidative capacity, protein digestion and absorption[J].Aquaculture, 2019, 507:428-434.
[13] CLEVELAND B M, WEBER G M.Effects of insulin-like growth factor-Ⅰ, insulin, and leucine on protein turnover and ubiquitin ligase expression in rainbow trout primary myocytes[J].American Journal of Physiology:Regulatory, Integrative and Comparative Physiology, 2010, 298(2):R341-R350.
[14] MANJARÍN R, COLUMBUS D A, SURYAWAN A, et al.Leucine supplementation of a chronically restricted protein and energy diet enhances mTOR pathway activation but not muscle protein synthesis in neonatal pigs[J].Amino Acids, 2016, 48(1):257-267.

[15] DUAN P, HU C H, QUAN C, et al.4-nonylphenol induces autophagy and attenuates mTOR-p70S6K/4EBP1 signaling by modulating AMPK activation in Sertoli cells[J].Toxicology Letters, 2017, 267:21-31.
[16] MA S L, LI X X, SUN L, et al.Effects of dietary protein levels on growth performance, serum indexes, PI3K/AKT/mTOR/S6K signalling and intestinal microbiota of abalone Haliotis discus hannai[J].Aquaculture Nutrition, 2021, 27(4):941-952.

[17] NEMOVA N N, LYSENKO L A, KANTSEROVA N P.Degradation of skeletal muscle protein during growth and development of salmonid fish[J].Russian Journal of Developmental Biology, 2016, 47(4):161-172.

[18] SEILIEZ I, PANSERAT S, LANSARD M, et al.Dietary carbohydrate-to-protein ratio affects TOR signaling and metabolism-related gene expression in the liver and muscle of rainbow trout after a single meal[J].American Journal of Physiology.Regulatory, Integrative and Comparative Physiology, 2011, 300(3):R733-R743.
[19] SEILIEZ I, GABILLARD J C, RIFLADE M, et al.Amino acids downregulate the expression of several autophagy-related genes in rainbow trout myoblasts[J].Autophagy, 2012, 8(3):364-375.

[20] 朱龙, 袁聪, 朱成科, 等.二倍体和三倍体虹鳟肌肉营养成分比较及分析[J].营养学报, 2018, 40(2):206-208. ZHU L, YUAN C, ZHU C K, et al.Comparison of nutritional compositions in muscles of diploid and triploid rainbow trouts (Oncorhynchus mykiss)[J].Acta Nutrimenta Sinica, 2018, 40(2):206-208.(in Chinese)
[21] SALIMIAN S, KEYVANSHOKOOH S, SALATI A P, et al.Effects of triploidy induction on physiological and immunological characteristics of rainbow trout (Oncorhynchus mykiss) at early developmental stages (fertilized eggs, eyed eggs and fry)[J].Animal Reproduction Science, 2016, 165:31-37.
[22] 王雪薇, 谢意军, 薛淑群, 等.二、三倍体虹鳟肌肉组织结构及营养成分的比较[J].水产科学, 2017, 36(5):569-576. WANG X W, XIE Y J, XUE S Q, et al.Comparison of microstructure and nutrient in muscles between diploid and triploid rainbow trout Oncorhynchus mykiss[J].Fisheries Science, 2017, 36(5):569-576.(in Chinese)
[23] MATOS E, GONÇALVES A, BANDARRA N, et al.Plant proteins and vegetable oil do not have detrimental effects on post-mortem muscle instrumental texture, sensory properties and nutritional value of gilthead seabream[J].Aquaculture, 2012, 358/359:205-212.
[24] 李本相, 卫育良, 梁萌青, 等.水解鱼蛋白对大菱鲆生长、体组成及肌纤维组织形态结构的影响[J].渔业科学进展, 2019, 40(5):155-165. LI B X, WEI Y L, LIANG M Q, et al.The effects of fish protein hydrolysate on the growth, body composition and morphological structure of muscle fiber of turbot (Scophthalmus maximus L.)[J].Progress in Fishery Sciences, 2019, 40(5):155-165.(in Chinese)
[25] 王巍, 甘佳, 付茂忠, 等.日粮能量和蛋白质水平对蜀宣花牛肉品质的影响[J].黑龙江畜牧兽医, 2020(7):54-57. WANG W, GAN J, FU M Z, et al.Effects of dietary energy and protein levels on the meat quality of Shuxuan cattle[J].Heilongjiang Animal Science and Veterinary Medicine, 2020(7):54-57.(in Chinese)
[26] 王丹, 唐金虎.饲粮蛋白水平对肥育猪不同部位肌纤维发育增生的影响[J].饲料工业, 2008, 29(21):16-19. WANG D, TANG J H.Effect of diet protein level on muscle fiber hypertrophy of different part in the finishing pigs[J].Feed Industry, 2008, 29(21):16-19.(in Chinese)
[27] 程贵兰, 梁诲弈, AWUDZA A H, 等.饲粮的不同蛋白质水平对12周龄麒麟鸡肌肉品质和肌肉营养成分的影响[J].饲料工业, 2019, 40(13):29-33. CHENG G L, LIANG H Y, AWUDZA A H, et al.Effects of dietary protein levels on muscle quality and nutritional composition of muscle of 12-week-old Frizzle chicken[J].Feed Industry, 2019, 40(13):29-33.(in Chinese)
[28] SAAVEDRA M, PEREIRA T G, CANDEIAS-MENDES A, et al.Effect of increased dietary protein level in meagre (Argyrosomus regius) juvenile growth and muscle cellularity[J].Aquaculture Nutrition, 2018, 24(3):1153-1159.

[29] 尹丽卿, 苏琳, 靳烨.肌纤维特性与鱼肉品质的关系及其调控技术的研究进展[J].食品工业, 2015, 36(2):231-234. YIN L Q, SU L, JIN Y.Relationship between fish muscle fiber characteristics and meat quality and its regulation technology[J].The Food Industry, 2015, 36(2):231-234.(in Chinese)
[30] DE ALMEIDA F L A, CARVALHO R F, PINHAL D, et al.Differential expression of myogenic regulatory factor MyoD in pacu skeletal muscle (Piaractus mesopotamicus Holmberg 1887:Serrasalminae, Characidae, Teleostei) during juvenile and adult growth phases[J].Micron, 2008, 39(8):1306-1311.

[31] ROWLERSON A, VEGGETTI A.5-cellular mechanisms of post-embryonic muscle growth in aquaculture species[J].Fish Physiology, 2001, 18:103-140.
[32] FERNANDEZ D A, CALVO J, FRANKLIN C E, et al.Muscle fibre types and size distribution in sub-antarctic notothenioid fishes[J].Journal of Fish Biology, 2000, 56(6):1295-1311.

[33] ALAMI-DURANTE H, WRUTNIAK-CABELLO C, KAUSHIK S J, et al.Skeletal muscle cellularity and expression of myogenic regulatory factors and myosin heavy chains in rainbow trout (Oncorhynchus mykiss):effects of changes in dietary plant protein sources and amino acid profiles[J].Comparative Biochemistry and Physiology.Part A:Molecular & Integrative Physiology, 2010, 156(4):561-568.

[34] JOHNSTON I A, LEE H T, MACQUEEN D J, et al.Embryonic temperature affects muscle fibre recruitment in adult zebrafish:genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes[J].The Journal of Experimental Biology, 2009, 212(Pt 12):1781-1793.
[35] AGUIAR A F, VECHETTI-JÚNIOR I J, ALVES DE SOUZA R W, et al.Myogenin, MyoD and IGF-Ⅰ regulate muscle mass but not fiber-type conversion during resistance training in rats[J].International Journal of Sports Medicine, 2013, 34(4):293-301.
[36] AZIZI S, NEMATOLLAHI M A, MOJAZI AMIRI B, et al.IGF-Ⅰ and IGF-Ⅱ effects on local IGF system and signaling pathways in gilthead sea bream (Sparus aurata) cultured myocytes[J].General and Comparative Endocrinology, 2016, 232:7-16.
[37] CODINA M, MONTSERRAT N, GARCÍA DE LA SERRANA D, et al.Role of insulin and IGFs in fish muscle development and quality[J].Archives Animal Breeding, 2006, 49(Special Issue):33-38.
[38] FUENTES E N, BJÖRNSSON B T, VALDÉS J A, et al.IGF-Ⅰ/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder[J].American Journal of Physiology.Regulatory, Integrative and Comparative Physiology, 2011, 300(6):R1532-R1542.
[39] VÉLEZ E J, LUTFI E, JIMÉNEZ-AMILBURU V, et al.IGF-Ⅰ and amino acids effects through TOR signaling on proliferation and differentiation of gilthead sea bream cultured myocytes[J].General and Comparative Endocrinology, 2014, 205:296-304.
[40] YANG S Y, LIU Z, YAN Z Z, et al.Improvement of skeletal muscle growth by GH/IGF growth-axis contributes to growth performance in commercial fleshy sturgeon[J].Aquaculture, 2021, 543:736929.
[41] 苗田田, 赵金良.外源生长激素注射对尼罗罗非鱼GH-IGFs生长轴通路因子及MyoD基因表达的影响[J].水产科技情报, 2018, 45(4):186-191. MIAO T T, ZHAO J L.Effects of growth hormone injection on expression of the GH/IGF-axis growth-related genes and MyoD genes in Nile tilapia, Oreochromis niloticus[J].Fisheries Science & Technology Information, 2018, 45(4):186-191.(in Chinese)
[42] STERLE J A, CANTLEY T C, LAMBERSON W R, et al.Effects of recombinant porcine somatotropin on placental size, fetal growth, and IGF-Ⅰ and IGF-Ⅱ concentrations in pigs[J].Journal of Animal Science, 1995, 73(10):2980-2985.

[43] ALAMI-DURANTE H, MÉDALE F, CLUZEAUD M, et al.Skeletal muscle growth dynamics and expression of related genes in white and red muscles of rainbow trout fed diets with graded levels of a mixture of plant protein sources as substitutes for fishmeal[J].Aquaculture, 2010, 303(1/2/3/4):50-58.
[44] ALAMI-DURANTE H, BAZIN D, CLUZEAUD M, et al.Effect of dietary methionine level on muscle growth mechanisms in juvenile rainbow trout (Oncorhynchus mykiss)[J].Aquaculture, 2018, 483:273-285.
[45] VÉLEZ E J, LUTFI E, AZIZI S, et al.Understanding fish muscle growth regulation to optimize aquaculture production[J].Aquaculture, 2017, 467:28-40.
[46] SAXTON R A, SABATINI D M.mTOR signaling in growth, metabolism, and disease[J].Cell, 2017, 168(6):960-976.

[47] LI H D, TIAN X L, ZHAO K, et al.Effect of Clostridium butyricum in different forms on growth performance, disease resistance, expression of genes involved in immune responses and mTOR signaling pathway of Litopenaeus vannamai[J].Fish & Shellfish Immunology, 2019, 87:13-21.
[48] TADASHI Y, PATRICE D.Mechanisms of IGF-1-mediated regulation of skeletal muscle hypertrophy and atrophy[J].Cells, 2020, 9(9):2-25.
[49] 张静静, 郑旭, 李玥, 等.低蛋白质饲粮添加蛋白酶对肉仔鸡生长性能、肝脏生长基因及雷帕霉素靶蛋白信号通路基因表达的影响[J].动物营养学报, 2021, 33(9):5332-5344. ZHANG J J, ZHENG X, LI Y, et al.Effects of protease supplementation in low protein diet on growth performance, liver growth gene and target of rapamycin signaling pathway gene expression of broilers[J].Chinese Journal of Animal Nutrition, 2021, 33(9):5332-5344.(in Chinese)
[50] LI Y H, LI F N, WU L, et al.Effects of dietary protein restriction on muscle fiber characteristics and mTORC1 pathway in the skeletal muscle of growing-finishing pigs[J].Journal of Animal Science and Biotechnology, 2016, 7(1):47.
[51] BALMORI-CEDEÑO J, LIU J T, MISK E, et al.Autophagy-related genes in rainbow trout Oncorhynchus mykiss (Walbaum) gill epithelial cells and their role in nutrient restriction[J].Journal of Fish Diseases, 2019, 42(4):549-558.

[52] SEILIEZ I, GUTIERREZ J, SALMERÓN C, et al.An in vivo and in vitro assessment of autophagy-related gene expression in muscle of rainbow trout (Oncorhynchus mykiss)[J].Comparative Biochemistry and Physiology.Part B:Biochemistry and Molecular Biology, 2010, 157(3):258-266.

[53] 潘红梅.牦牛CAPN3基因克隆、多态性及胴体和肉质性状关联分析[D].硕士学位论文.兰州:甘肃农业大学, 2013. PAN H M.Cloning and polymorphisms analysis of CAPN3 gene and their associations with carcass and meat quality traits in yak[D].Master's Thesis.Lanzhou:Gansu Agricultural University, 2013.(in Chinese)
[54] 王耀梅, 田孟芳, 孙家乐, 等.不同蛋白质水平精料对色瓦绵羊生产性能及生长速度、肉品质相关基因表达的影响[J].黑龙江畜牧兽医, 2021(16):92-98. WANG Y M, TIAN M F FSUN J L, et al.Effects of different protein levels level concentrate on production performance, growth speed and meat quality related gene expression of Sewa sheep[J].Heilongjiang Animal Science and Veterinary Medicine, 2021(16):92-98.(in Chinese)
[55] 马丽娜, 王锦, 赵正伟, 等.滩羊肌肉组织钙蛋白酶系统基因表达及其与嫩度的相关分析[J].上海畜牧兽医通讯, 2020(3):2-4. MA L N, WANG J, ZHAO Z W, et al.Gene expression of calprotease system in muscle tissue of Tan sheep and its correlation with tenderness[J].Shanghai Journal of Animal Husbandry and Veterinary Medicine, 2020(3):2-4.(in Chinese)
[56] 董慧琳, 聂红明, 梅昭荷, 等.泛素蛋白酶体途径的应用研究进展[J].中国医药导报, 2019, 16(29):25-30. DONG H L, NIE H M, MEI Z H, et al.Research progress of the application of ubiquitin proteasome pathway[J].China Medical Herald, 2019, 16(29):25-30.(in Chinese)
[57] BAPTISTA I L, SILVA W J, ARTIOLI G G, et al.Leucine and HMB differentially modulate proteasome system in skeletal muscle under different sarcopenic conditions[J].PLoS One, 2013, 8(10):e76752.

Options

Outlines

模态框（Modal）标题

Abstract

Cite this article

References