Scientia Agricultura Sinica ›› 2015, Vol. 48 ›› Issue (6): 1195-1204.doi: 10.3864/j.issn.0578-1752.2015.06.15

• ANIMAL SCIENCE·VETERINARY SCIENCERE·SOURCE INSECT • Previous Articles     Next Articles

Expression Profile of IGF-I-calcineurin-NFATc3-Dependent Pathway Genes in Skeletal Muscles and Their Associations with Myofiber Traits During Embryonic and Early Post-Hatching Development in Ducks

SHU Jing-ting1, SONG Chi1, XU Wen-juan1, ZHANG Ming1, SHAN Yan-ju1, CHEN Wen-feng2, SONG Wei-tao1, TAO Zhi-yun1, LI Hui-fang1   

  1. 1Jiangsu Institute of Poultry Science,Yangzhou 225125, Jiangsu
    2 Jiangsu Tengdayuan Agriculture and Livestock Co. Ltd, Jiangyan 225538, Jiangsu
  • Received:2014-05-06 Online:2015-03-16 Published:2015-03-16

Abstract: 【Objective】Insulin-like growth factor I (IGF-I)-calcineurin (CaN)-NFAT signal pathway have been implicated in the regulation of myocyte hypertrophy and fiber type specificity. In the present study, expression of CnAα, NFATc3 and IGF-I genes was firstly studied in Gaoyou and Jinding ducks differing in their muscle growth rates. 【Method】 Expression of IGF-I, CnAα and NFATc3 was quantified by RT-PCR in the breast muscle (BM) and leg muscle (LM) on days 13, 17, 21, 25 and, 27 of embryonic development, as well as at 7 days post-hatching (PH). Lateral gastrocnemius muscles collected from two duck breeds were cut at -20 using a cryotome and then stained with the method of myosin-ATPase in order to analyze muscle fiber type composition. SPSS 20.0 software was used to conduct the significant difference analysis, for investigating the possible regulation mechanism of IGF-I-CaN-NFAT pathway in myofiber type transition. 【Result】 Overall, the percentage of type I fibers increased and that of type IIb fibers decreased consistently. However, the percentage of type IIa fibers was almost constant as development proceeded in both duck breeds. The consistent expression patterns of CnAα, NFATc3 and IGF-I were found in the same anatomical location at different development stages in both duck breeds, showing extremely significant differences in age-specific fashion. However, the three genes were differentially expressed in different anatomical location (BM and LM). CnAα, NFATc3 and IGF-I mRNA could be detected as early as on E 13d, and the highest level was appeared at this stage in both BM and LM, significantly higher than those at the other five development stages, indicating that these three genes might have some effects on the ontogenesis of myofibers. The mRNA expression of duck CnAα in BM showed a tendency as the “V”, the lowest level appeared on E 21d, and then increased continuously up until 7 days PH in both duck breeds, while in LM, CnAα gene expression was variable throughout the course of this study and the lowest level appeared on E 27d. Expression of NFATc3 decreased significantly to a very low level from E 13d to E 17d and maintained this relative low level during late development stages in both BM and LM, the lowest level appeared on E 21d in BM while the expression level on E 21d in LM was significantly higher (P<0.05) than those on embryonic days 17, 25 and 27, and at 7 days PH. Expression of IGF-I declined to the lowest level just prior to hatch (E 27d), and then elevated a little on 1 week PH in both BM and LM in the two duck breeds. Significant positive relationships were observed for the expression of studied genes in BM and LM of both duck breeds. Meanwhile, the expression of these three genes were all showed positive relationships with the percentage of type IIb fibers and negative relationships with the percentage of type I fibers and type IIa fibers. 【Conclusion】The data of the study indicate that the fiber type of the lateral gastrocnemius muscle may transit from type IIb to type I during late-embryonic and PH development, and differential expression and coordinated developmental regulation of the selected genes that comprise the IGF-I-calcineurin-NFATc3 pathwayin the duck skeletal muscles during embryonic and early PH growth and development, and this signaling pathway might play a role in the regulation of the myofiber type transition.

Key words: early development, gene expression, myofiber type; IGF-I-calcineurin-NFATc3 pathway, duck

[1]    Juan C C, Pura B, Carlo C. Myosin heavy chain isoform composition and Ca2+ transients in fibres from enzymatically dissociated murine soleus and extensor digitorum longus muscles. Journal of Physiology, 2010, 588: 267-279.
[2]    Messina G, Biressi S, Monteverde S, Magli A, Cassano M, Perani L, Roncaglia E, Tagliafico E, Starnes L, Campbell C E, Grossi M, Goldhamer D J, Gronostajski R M, Cossu G. Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell, 2010, 140 (4): 554-566.
[3]    Dutka T L, Mollica J P, Posterino G S, Lamb G D. Modulation of contractile apparatus Ca2+ sensitivity and disruption of excitation– contraction coupling by S-nitrosoglutathione in rat muscle fibres. Journal of Physiology, 2011, 589: 2181- 2196.
[4]    Hollingworth S, Kim M M, Baylor S M. Measurement and simulation of myoplasmic calcium transients in mouse slow-twitch muscle fibres. Journal of Physiology, 2012, 590: 575-594.
[5]    Olson E N, Williams R S. Calcineurin signaling and muscle remodeling. Cell, 2000, 101: 689-692.
[6]    Delling U, Tureckova J, Lim H W, Windt J D, Rotwein P, Molkentin J D. A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression. Molecular and Cellular Biology, 2000, 20(17): 6600-6611.
[7]    Robert J T, Jeffrey S O, Matthew R R, Nicole D G, Shelly R S, Simon J L, Francisco J N. Calcineurin activation influences muscle phenotype in a uscle-specific fashion. BMC Cell Biology, 2004, 5: 28.
[8]    Tavi P, Weaterblad H. The role of in vivo Ca2+ signals acting on Ca2+–calmodulin-dependent proteins for skeletal muscle plasticity. Journal of Physiology, 2011, 589(21): 5021-5031.
[9]    Martins K J, St-Louis M, Murdoch G K, MacLean I M, McDonald P, Dixon W T, Putman C T, Michel R N. Nitric oxide synthase inhibition prevents activity-induced calcineurin-NFATc1 signalling and fast-to-slow skeletal muscle fibre type conversions. Journal of Physiology, 2012, 590(Pt 6):1427-1442.
[10]   Tilley R E, Mcneil C J, Ashworth C J, Page K R, McArdle H J. Altered muscle development and expression of the insulin-like growth factor system in growth retarded fetal pigs. Domestic Animal Endocrinology, 2007, 32(3): 167-177.
[11]   Hudson M B, Price S R. Calcineurin: A poorly understood regulator of muscle mass. The International Journal of Biochemistry and Cell Biology, 2013, 45: 2173-2178.
[12]   Musaro A, McCullagh K J, Naya F J, Olson E N, Rosenthal N. IGF-I induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NFATc1. Nature, 1999, 400(6744): 581-585.
[13]   Liu Y W, Shen T S, Randall W R, Schneider M F. Signaling pathway in activity-dependent fiber type plasticity in adult skeletal muscle. Journal of Muscle Research and Cell Motility, 2005, 26(1): 13-21.
[14]   Swoap S J, Hunter R B, Stevenson E J,  Felton H M, Kansagra N V, Lang J M, Esser K A, Kandarian S C. The calcineurin-NFAT pathway and muscle fiber-type gene expression. American Journal of Physiology-Cell Physiology, 2000, 279(4): 915-924.
[15]   Allen D L, Sartorius C A, Sycuro L K, Leinwand L A. Different pathways regulate expression of the skeletal myosin heavy chain genes. Journal of Biological Chemistry, 2001, 276(47): 43524-43533.
[16]   Crabtree, G R. Generic signals and specific outcomes: signaling through Ca2+, calcineurin, and NFAT. Cell, 1999, 96:611-614.
[17]   单艳菊,束婧婷,徐文娟,章双杰,宋卫涛,胡艳,李慧芳. 不同鸭种胚胎期和岀雏早期生长轴GH、GHR和IGF-Ⅰ基因mRNA差异表达分析,农业生物技术学报,2013, 21(4): 421-427.
Shan Y J, Shu J T, Xu W J, Zhang S J, Song W T, Hu Y, Li H F. The expression analysis of growth axis genes (GH, GHR and IGF-I) during embryonic and post-hatch development in different duck breeds. Journal of Agricultural Biotechnology, 2013, 21(4): 421-427. (in Chinese)
[18]   Matsuoka Y, Inoue A. Controlled differentiation of myoblast cells into fast and slow muscle fibers. Cell and Tissue Research, 2008, 332: 123-132.
[19]   Picard B, Lefaucheur L, Berri C, Duclos M J. Muscle fibre ontogenesis in farm animal species. Reproduction Nutrition Development, 2002, 42 (5): 415-431.
[20]   Wigmore P M, Dunglison G F. The generation of fiber diversity during myogenesis. International Journal of Developmental Biology,
1998, 42: 117-125.
[21]   Condon K, Silberstein L, Blau H M, Thompson W J. Development of muscle fiber types in the prenatal rat hindlimb. Developmental Biology, 1990, 138(2): 256-274.
[22]   Dupont J, Holzenberger M. Biology of insulin-like growth factors in development. Birth Defects Research (Part C), 2003, 69: 257-271.
[23]   李伯江,李平华,吴望军,李齐发,黄瑞华,刘红林. 骨骼肌肌纤维形成机制的研究进展,中国农业科学,2014, 47(6):1200-1207.
Li B J, Li P H, Wu W J, Li Q F, Huang R H, Liu H L. Progresses in research of the mechanisms of skeletal muscle fiber formation. Scientia Agricultual Sinica, 2014, 47(6):1200-1207. (in Chinese)
[24]   Parson S A, Millay D P, Wilkin S B J, Bueno O F, Tsika G L, Neilson J R, Liberatore C M, Yutzey K E, Crabtree G R, Tsika R W, Molkentin J D. Genetic loss of calcineurin blocks mechanical overload- induced skeletal muscle fiber type switching but not hypertrophy. The Journal of Biological Chemistry, 2004, 25(279): 26192- 26200.
[25]   Bandman E, Rosser B W. Evolutionary significance of myosin heavy chain heterogeneity in birds. Microscopy Research And Technique, 2000, 50: 473-491.
[26]   Hudson M B, Price S R. Calcineurin: A poorly understood regulator of muscle mass. The International Journal of Biochemistry & Cell Biology, 2013, 45: 2173-2178.
[27]   Semsarian C, Wu M J, Ju Y K, Marciniec T, Yeoh T, Allen D G. Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signaling pathway. Nature, 1999, 400: 576-581.
[28]   Parsons S A, Wilkins B J, Bueno O F, Molkentin J D. Altered skeletal muscle phenotypes in calcineurin Aα and Aβ gene-targeted mice. Molecular and Cellular Biology, 2003, 23:4331-4343.
[29]   Wan L, Ma J S, Xu G Y, Wang D H, Wang N L. Molecular cloning, structural analysis and tissue expression of protein phosphatase 3 catalytic subunit alpha isoform (ppp3ca) gene in Tianfu goat muscle. International Journal of Molecular Sciences. 2014, 15: 2346-2358.
[1] ZHANG KeKun,CHEN KeQin,LI WanPing,QIAO HaoRong,ZHANG JunXia,LIU FengZhi,FANG YuLin,WANG HaiBo. Effects of Irrigation Amount on Berry Development and Aroma Components Accumulation of Shine Muscat Grape in Root-Restricted Cultivation [J]. Scientia Agricultura Sinica, 2023, 56(1): 129-143.
[2] GU LiDan,LIU Yang,LI FangXiang,CHENG WeiNing. Cloning of Small Heat Shock Protein Gene Hsp21.9 in Sitodiplosis mosellana and Its Expression Characteristics During Diapause and Under Temperature Stresses [J]. Scientia Agricultura Sinica, 2023, 56(1): 79-89.
[3] LAI ChunWang, ZHOU XiaoJuan, CHEN Yan, LIU MengYu, XUE XiaoDong, XIAO XueChen, LIN WenZhong, LAI ZhongXiong, LIN YuLing. Identification of Ethylene Synthesis Pathway Genes in Longan and Its Response to ACC Treatment [J]. Scientia Agricultura Sinica, 2022, 55(3): 558-574.
[4] SHU JingTing,SHAN YanJu,JI GaiGe,ZHANG Ming,TU YunJie,LIU YiFan,JU XiaoJun,SHENG ZhongWei,TANG YanFei,LI Hua,ZOU JianMin. Relationship Between Expression Levels of Guangxi Partridge Chicken m6A Methyltransferase Genes, Myofiber Types and Myogenic Differentiation [J]. Scientia Agricultura Sinica, 2022, 55(3): 589-601.
[5] GUO ShaoLei,XU JianLan,WANG XiaoJun,SU ZiWen,ZHANG BinBin,MA RuiJuan,YU MingLiang. Genome-Wide Identification and Expression Analysis of XTH Gene Family in Peach Fruit During Storage [J]. Scientia Agricultura Sinica, 2022, 55(23): 4702-4716.
[6] KANG Chen,ZHAO XueFang,LI YaDong,TIAN ZheJuan,WANG Peng,WU ZhiMing. Genome-Wide Identification and Analysis of CC-NBS-LRR Family in Response to Downy Mildew and Powdery Mildew in Cucumis sativus [J]. Scientia Agricultura Sinica, 2022, 55(19): 3751-3766.
[7] YuXia WEN,Jian ZHANG,Qin WANG,Jing WANG,YueHong PEI,ShaoRui TIAN,GuangJin FAN,XiaoZhou MA,XianChao SUN. Cloning, Expression and Anti-TMV Function Analysis of Nicotiana benthamiana NbMBF1c [J]. Scientia Agricultura Sinica, 2022, 55(18): 3543-3555.
[8] JIN MengJiao,LIU Bo,WANG KangKang,ZHANG GuangZhong,QIAN WanQiang,WAN FangHao. Light Energy Utilization and Response of Chlorophyll Synthesis Under Different Light Intensities in Mikania micrantha [J]. Scientia Agricultura Sinica, 2022, 55(12): 2347-2359.
[9] YUAN JingLi,ZHENG HongLi,LIANG XianLi,MEI Jun,YU DongLiang,SUN YuQiang,KE LiPing. Influence of Anthocyanin Biosynthesis on Leaf and Fiber Color of Gossypium hirsutum L. [J]. Scientia Agricultura Sinica, 2021, 54(9): 1846-1855.
[10] SHU JingTing,JI GaiGe,SHAN YanJu,ZHANG Ming,JU XiaoJun,LIU YiFan,TU YunJie,SHENG ZhongWei,TANG YanFei,JIANG HuaLian,ZOU JianMin. Expression Analysis of IGF1-PI3K-Akt-Dependent Pathway Genes in Skeletal Muscle and Liver Tissue of Yellow Feather Broilers [J]. Scientia Agricultura Sinica, 2021, 54(9): 2027-2038.
[11] ZHAO Ke,ZHENG Lin,DU MeiXia,LONG JunHong,HE YongRui,CHEN ShanChun,ZOU XiuPing. Response Characteristics of Plant SAR and Its Signaling Gene CsSABP2 to Huanglongbing Infection in Citrus [J]. Scientia Agricultura Sinica, 2021, 54(8): 1638-1652.
[12] ZHAO Le,YANG HaiLi,LI JiaLu,YANG YongHeng,ZHANG Rong,CHENG WenQiang,CHENG Lei,ZHAO YongJu. Expression Patterns of TETs and Programmed Cell Death Related Genes in Oviduct and Uterus of Early Pregnancy Goats [J]. Scientia Agricultura Sinica, 2021, 54(4): 845-854.
[13] ZHU FangFang,DONG YaHui,REN ZhenZhen,WANG ZhiYong,SU HuiHui,KU LiXia,CHEN YanHui. Over-expression of ZmIBH1-1 to Improve Drought Resistance in Maize Seedlings [J]. Scientia Agricultura Sinica, 2021, 54(21): 4500-4513.
[14] YUE YingXiao,HE JinGang,ZHAO JiangLi,YAN ZiRu,CHENG YuDou,WU XiaoQi,WANG YongXia,GUAN JunFeng. Comparison Analysis on Volatile Compound and Related Gene Expression in Yali Pear During Cellar and Cold Storage Condition [J]. Scientia Agricultura Sinica, 2021, 54(21): 4635-4649.
[15] LIU ChangYun,LI XinYu,TIAN ShaoRui,WANG Jing,PEI YueHong,MA XiaoZhou,FAN GuangJin,WANG DaiBin,SUN XianChao. Cloning, Expression and Anti-Virus Function Analysis of Solanum lycopersicum SlN-like [J]. Scientia Agricultura Sinica, 2021, 54(20): 4348-4357.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!