Myostatin promotes proliferation of bovine muscle satellite cells through activating TRPC4/Ca2+/calcineurin/NFATc3 pathway

doi:10.1016/j.jia.2024.04.020

Journal of Integrative Agriculture

2026, Vol. 25

Issue (3): 1125-1136 DOI: 10.1016/j.jia.2024.04.020

Animal Science · Veterinary Medicine

Advanced Online Publication | Current Issue | Archive | Adv Search

Myostatin promotes proliferation of bovine muscle satellite cells through activating TRPC4/Ca²⁺/calcineurin/NFATc3 pathway

Yajie Gao^{1, 2*}, Song Wang^{1, 3*}, Anqi Di¹, Chao Hai¹, Di Wu¹, Zhenting Hao¹, Lige Bu¹, Xuefei Liu¹, Chunling Bai¹, Guanghua Su¹, Lishuang Song¹, Zhuying Wei¹, Zhonghua Liu³, Lei Yang^1#, Guangpeng Li^1#

¹State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, College of Life Science, Inner Mongolia University, Hohhot 010070, China

²The Central Lab, The First Affiliated Hospital of Baotou Medical College, Baotou 014010, China

³College of Life Science, Northeast Agricultural University, Harbin 150030, China

Highlights
● Ca²⁺ content in muscle tissues and muscle satellite cells of MSTN mutated cattle was detected.
● Ca²⁺ signaling pathway was used to explain the phenomenon that MSTN mutation activates cell proliferation and induces animal muscle overgrowth.
● The molecular mechanism by which MSTN mutation activates the TRPC4/Ca²⁺/calcineurin/NFATc3 pathway to promote muscle development was revealed.

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

肌生成抑制素（myostatin，MSTN）主要在骨骼肌中表达，MSTN基因的缺失会促进肌细胞增殖。Ca²⁺是生物体中广泛存在的第二信使，对于肌细胞的增殖和肌肉生长至关重要。然而，MSTN基因与Ca²⁺之间的联系目前仍不清楚。因此，本研究以MSTN基因编辑牛（MSTN^-/-）作为研究对象，从Ca²⁺通道及其调控途径角度探讨MSTN突变促进肌卫星细胞增殖的分子机制。与野生型（WT）相比，MSTN突变促进牛肌卫星细胞增殖。通过电感耦合等离子体—质谱法(Inductively coupled plasma-Mass Spectrometry，ICP-MS）发现，MSTN^-/-牛的肌肉组织和肌卫星细胞中Ca²⁺含量显著升高。同时，转录组测序发现MSTN^-/-牛的TRPC4表达水平显著增加。这些结果表明，MSTN突变激活Ca²⁺通道TRPC4促进细胞增殖。通过使用TRPC4的特异性抑制剂ML204处理MSTN^-/-肌卫星细胞，发现Ca²⁺含量显著降低至WT水平。Calreticulin的Western blot和特异性染色发现，ML204处理后MSTN^-/-肌卫星细胞中Calcineutrin的表达量和NFATc3入核量显著降低，细胞增殖能力受到抑制。综上所述，MSTN突变激活钙离子通道TRPC4，引起胞质内Ca²⁺含量升高，激活Calcineurin活性，致使NFATc3去磷酸化入核，激活增殖相关基因从而促进肌卫星细胞增殖，使MSTN^-/-牛出现“双肌”表型。本研究揭示了MSTN突变激活TRPC4/Ca²⁺/Calcineurin/NFATc3通路促进肌肉发育的分子机制，为进一步探究MSTN对牛肌肉发育的调控机制提供参考。

Abstract

Myostatin (MSTN) is principally expressed in skeletal muscle and negatively regulates muscle growth and development. MSTN mutation can induce muscle overgrowth in cattle by activating cell proliferation, presenting a “double-muscle” phenotype. However, the specific regulatory mechanism is still unclear. Here, we found that Ca²⁺ content in muscle tissue and muscle satellite cells of MSTN mutated (MSTN^–/–) cattle were significantly increased compared to wild-type (WT). Furthermore, transcriptome analysis of muscle satellite cells revealed that TRPC4 was significantly increased in MSTN^–/–cattle. And the expression of TRPC4 in muscle tissue of MSTN^–/– cattle was detected by RT-qPCR and Western blot, which was significantly higher than that of WT. These results suggested that MSTN mutation promoted muscle satellite cells proliferation through activation of TRPC4 channel. To further verify, ML204, a specific inhibitor of TRPC4, was used to treat MSTN^–/– muscle satellite cells. We found that cell proliferation was inhibited, calcineurin expression was downregulated, and the entry of NFATc3 into nuclei was reduced, which was similar to WT group. Thus, MSTN mutation leads to the activation of TRPC4 channel, which increases intracellular Ca²⁺content, further activates calcineurin/NFATc3 pathway, and ultimately promotes the proliferation of muscle satellite cells.

Keywords: myostatin cell proliferation Ca²⁺ TRPC4 NFATc3

Received: 31 October 2023 Accepted: 13 March 2024 Online: 16 May 2024

Fund:

This study was supported by the National Natural Science Foundation of China (32360837 and 32341052), the STI2030 Major Projects, China (2023ZW0404803), the Inner Mongolia Open Competition Projects, China (2022JBGS0025), the Inner Mongolia Science and Technology Leading Team, China (2022LJRC0006), the Inner Mongolia Science and Technology Major Projects, China (2021ZD0009, 2021ZD0008, 2022ZD0008, 2023KJHZ0028), the Inner Mongolia Young Talents Projects, China (NJYT23138), the Inner Mongolia Natural Science Foundation, China (2023MS03004), the Central Government Guides Development, China (2022ZY0212), the National Agricultural Science and Technology Project of China (NK2022130203), the Collaborative Innovation among Universities in Hohhot, China (XTCX2023-06), and the Ministry of Education Engineering Centre Project, China (JYBGCSYS2022).

About author: Yajie Gao, E-mail: gaoyajie1997@163.com; Song Wang, E-mail: wangsong199852@163.com; #Correspondence Lei Yang, Tel: +86-471-5298583, E-mail: leiyang@imu.edu.cn; Guangpeng Li, Tel: +86-471-5298583, E-mail: gpengli@imu.edu.cn * These authors contributed equally to this study.

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Yajie Gao, Song Wang, Anqi Di, Chao Hai, Di Wu, Zhenting Hao, Lige Bu, Xuefei Liu, Chunling Bai, Guanghua Su, Lishuang Song, Zhuying Wei, Zhonghua Liu, Lei Yang, Guangpeng Li. 2026. Myostatin promotes proliferation of bovine muscle satellite cells through activating TRPC4/Ca²⁺/calcineurin/NFATc3 pathway. Journal of Integrative Agriculture, 25(3): 1125-1136.

Abramowitz J, Birnbaumer L. 2009. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB Journal, 23, 297–328.

Allen D G. 2019. Calcium sensitivity and muscle disease. The Journal of Physiology, 597, 4435–4436.

Backs J, Song K, Bezprozvannaya S, Chang S, Olson E N. 2006. CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. Journal of Clinical Investigation, 116, 1853–1864.

Bodnár D, Geyer N, Ruzsnavszky O, Oláh T, Hegyi B, Sztretye M, Fodor J, Dienes B, Balogh Á, Papp Z, Szabó L, Müller G, Csernoch L, Szentesi P. 2014. Hypermuscular mice with mutation in the myostatin gene display altered calcium signalling. The Journal of Physiology, 592, 1353–1365.

Boman I A, Våge D I. 2009. An insertion in the coding region of the myostatin (MSTN) gene affects carcass conformation and fatness in the Norwegian Spaelsau (Ovis aries). BMC Research Notes, 2, 98.

Buchholz M, Ellenrieder V. 2007. An emerging role for Ca2+/calcineurin/NFAT signaling in cancerogenesis. Cell Cycle, 6, 16–19.

Chen M M, Zhao Y P, Zhao Y, Deng S L, Yu K. 2021. Regulation of myostatin on the growth and development of skeletal muscle. Frontiers in Cell and Developmental Biology, 9, 785712.

Chen Y, Yuan J, Jiang G, Zhu J, Zou Y, Lv Q. 2017. Lercanidipine attenuates angiotensin II-induced cardiomyocyte hypertrophy by blocking calcineurin-NFAT3 and CaMKII-HDAC4 signaling. Molecular Medicine Reports, 16, 4545–4552.

Cooley N, Grubb D R, Luo J, Woodcock E A. 2014. The phosphatidy-linositol(4,5)bisphosphate-binding sequence of transient receptor potential channel canonical 4α is critical for its contribution to cardiomyocyte hypertrophy. Molecular Pharmacology, 86, 399–405.

Eder P, Molkentin J D. 2011. TRPC channels as effectors of cardiac hypertrophy. Circulation Research, 108, 265–272.

Elliott B, Renshaw D, Getting S, Mackenzie R. 2012. The central role of myostatin in skeletal muscle and whole body homeostasis. Acta Physiologica (Oxford, England), 205, 324–340.

Farfariello V, Gordienko D V, Mesilmany L, Touil Y, Germain E, Fliniaux I, Desruelles E, Gkika D, Roudbaraki M, Shapovalov G, Noyer L, Lebas M, Allart L, Zienthal-Gelus N, Iamshanova O, Bonardi F, Figeac M, Laine W, Kluza J, Marchetti P, et al. 2022. TRPC3 shapes the ER-mitochondria Ca2+ transfer characterizing tumour-promoting senescence. Nature Communications, 13, 956.

Figeac N, Daczewska M, Marcelle C, Jagla K. 2007. Muscle stem cells and model systems for their investigation. Developmental Dynamic (An official publication of the American Association of Anatomists), 236, 3332–3342.

Fu C, Donadio N, Cardenas M E, Heitman J. 2018. Dissecting the roles of the calcineurin pathway in unisexual reproduction, stress responses, and virulence in Cryptococcus deneoformans. Genetics, 208, 639–653.

Gao H, Wang F, Wang W, Makarewich C A, Zhang H, Kubo H, Berretta R M, Barr L A, Molkentin J D, Houser S R. 2012. Ca2+ influx through L-type Ca2+ channels and transient receptor potential channels activates pathological hypertrophy signaling. Journal of Molecular and Cellular Cardiology, 53, 657–667.

Ge L, Dong X, Gong X, Kang J, Zhang Y, Quan F. 2020. Mutation in myostatin 3´UTR promotes C2C12 myoblast proliferation and differentiation by blocking the translation of MSTN. International Journal of Biological Macromolecules, 154, 634–643.

Girgenrath S, Song K, Whittemore L A. 2005. Loss of myostatin expression alters fiber-type distribution and expression of myosin heavy chain isoforms in slow- and fast-type skeletal muscle. Muscle & Nerve, 31, 34–40.

Graef I A, Chen F, Crabtree G R. 2001. NFAT signaling in vertebrate development. Current Opinion in Genetics & Development, 11, 505–512.

Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan P G, Rao A. 2006. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature, 441, 646–650.

Han J, Tian H, Liu Y, Fan F. 2019. Sarpogrelate attenuates pulmonary arterial hypertension via calcium/calcineurin axis. Frontiers in Bioscience (Landmark edition), 24, 607–615.

Han S Z, Gao K, Chang S Y, Choe H M, Paek H J, Quan B H, Liu X Y, Yang L H, Lv S T, Yin X J, Quan L H, Kang J D. 2022. miR-455-3p is negatively regulated by myostatin in skeletal muscle and promotes myoblast differentiation. Journal of Agricultural and Food Chemistry, 70, 10121–10133.

Hardingham G E, Chawla S, Johnson C M, Bading H. 1997. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature, 385, 260–265.

Hasegawa K, Fujii S, Matsumoto S, Tajiri Y, Kikuchi A, Kiyoshima T. 2021. YAP signaling induces PIEZO1 to promote oral squamous cell carcinoma cell proliferation. The Journal of Pathology, 253, 80–93.

Hendrikx S, Coso S, Prat-Luri B, Wetterwald L, Sabine A, Franco C A, Nassiri S, Zangger N, Gerhardt H, Delorenzi M, Petrova T V. 2019. Endothelial calcineurin signaling restrains metastatic outgrowth by regulating Bmp2. Cell Reports, 26, 1227–1241.e6.

Hennebry A, Berry C, Siriett V, O’callaghan P, Chau L, Watson T, Sharma M, Kambadur R. 2009. Myostatin regulates fiber-type composition of skeletal muscle by regulating MEF2 and MyoD gene expression. American Journal of Physiology Cell Physiology, 296, C525–C534.

Hoey T, Sun Y L, Williamson K, Xu X. 1995. Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity, 2, 461–472.

Hofmann T, Schaefer M, Schultz G, Gudermann T. 2002. Subunit composition of mammalian transient receptor potential channels in living cells. Proceedings of the National Academy of Sciences of the United States of America, 99, 7461–7466.

Hong M H, Na S W, Jang Y J, Yoon J J, Lee Y J, Lee H S, Kim H Y, Kang D G. 2021. Betulinic acid improves cardiac-renal dysfunction caused by hypertrophy through calcineurin-NFATc3 signaling. Nutrients, 13, 3484.

Hook S S, Means A R. 2001. Ca2+/CaM-dependent kinases: From activation to function. Annual Review of Pharmacology and Toxicology, 41, 471–505.

Horsley V, Pavlath G K. 2002. NFAT: Ubiquitous regulator of cell differentiation and adaptation. The Journal of Cell Biology, 156, 771–774.

Jiang H N, Zeng B, Chen G L, Lai B, Lu S H, Qu J M. 2016. Lipopolysaccharide potentiates endothelin-1-induced proliferation of pulmonary arterial smooth muscle cells by upregulating TRPC channels. Biomedicine & Pharmacotherapy, 82, 20–27.

Junli H, Hongyan T, Ya L, Fenling F. 2018. 5-HT promotes pulmonary arterial smooth muscle cell proliferation through the TRPC channel. Cellular and Molecular Biology (Noisy-le-Grand, France), 64, 89–96.

Kambadur R, Sharma M, Smith T P, Bass J J. 1997. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Research, 7, 910–916.

Kirschmer N, Bandleon S, Von Ehrlich-Treuenstätt V, Hartmann S, Schaaf A, Lamprecht A K, Miranda-Laferte E, Langsenlehner T, Ritter O, Eder P. 2016. TRPC4α and TRPC4β similarly affect neonatal cardiomyocyte survival during chronic GPCR stimulation. PLoS ONE, 11, e0168446.

Kollias H D, Mcdermott J C. 2008. Transforming growth factor-beta and myostatin signaling in skeletal muscle. Journal of Applied Physiology, 104, 579–587.

Kreusser M M, Backs J. 2014. Integrated mechanisms of CaMKII-dependent ventricular remodeling. Frontiers in Pharmacology, 5, 36.

Lee S J. 2021. Targeting the myostatin signaling pathway to treat muscle loss and metabolic dysfunction. The Journal of Clinical Investigation, 131, e148372.

Li H, Rao A, Hogan P G. 2011. Interaction of calcineurin with substrates and targeting proteins. Trends in Cell Biology, 21, 91–103.

Li N, Si B, Ju J F, Zhu M, You F, Wang D, Ren J, Ning Y S, Zhang F Q, Dong K, Huang J, Yu W Q, Wang T J, Qiao B. 2016. Nicotine induces cardiomyocyte hypertrophy through TRPC3-mediated Ca2+/NFAT signalling pathway. The Canadian Journal of Cardiology, 32, 1260.e1.

Lin C Y, Shibu M A, Wen R, Day C H, Chen R J, Kuo C H, Ho T J, Viswanadha V P, Kuo W W, Huang C Y. 2021. Leu27 IGF-II-induced hypertrophy in H9c2 cardiomyoblasts is ameliorated by saffron by regulation of calcineurin/NFAT and CaMKIIδ signaling. Environmental Toxicology, 36, 2475–2483.

Liu J, Pan M, Huang D, Guo Y, Yang M, Zhang W, Mai K. 2020. Myostatin-1 inhibits cell proliferation by inhibiting the mTOR signal pathway and MRFs, and activating the ubiquitin-proteasomal system in skeletal muscle cells of japanese flounder Paralichthys olivaceus. Cells, 9, 2376.

Luo P, Wang L, Luo L, Wang L, Yang K, Shu G, Wang S, Zhu X, Gao P, Jiang Q. 2019. Ca2+-calcineurin-NFAT pathway mediates the effect of thymol on oxidative metabolism and fiber-type switch in skeletal muscle. Food & Function, 10, 5166–5173.

Makarewich C A, Zhang H, Davis J, Correll R N, Trappanese D M, Hoffman N E, Troupes C D, Berretta R M, Kubo H, Madesh M, Chen X, Gao E, Molkentin J D, Houser S R. 2014. Transient receptor potential channels contribute to pathological structural and functional remodeling after myocardial infarction. Circulation Research, 115, 567–580.

Masaki T, Shimada M. 2022. Decoding the phosphatase code: Regulation of cell proliferation by calcineurin. International Journal of Molecular Sciences, 23, 1122.

Masson B, Saint-Martin Willer A, Dutheil M, Penalva L, Le Ribeuz H, El Jekmek K, Ruchon Y, Cohen-Kaminsky S, Sabourin J, Humbert M, Mercier O, Montani D, Capuano V, Antigny F. 2023. Contribution of transient receptor potential canonical channels in human and experimental pulmonary arterial hypertension. American Journal of Physiology Lung Cellular and Molecular Physiology, 325, L246–L261.

Matikainen N, Pekkarinen T, Ryhänen E M, Schalin-Jäntti C. 2021. Physiology of calcium homeostasis: An overview. Endocrinology and Metabolism Clinics of North America, 50, 575–590.

McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. 2003. Myostatin negatively regulates satellite cell activation and self-renewal. The Journal of Cell Biology, 162, 1135–1147.

McPherron A C, Lawler A M, Lee S J. 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature, 387, 83–90.

McPherron A C, Lee S J. 1997. Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences of the United States of America, 94, 12457–12461.

Mojsa B, Mora S, Bossowski J P, Lassot I, Desagher S. 2015. Control of neuronal apoptosis by reciprocal regulation of NFATc3 and Trim17. Cell Death and Differentiation, 22, 274–286.

Mosher D S, Quignon P, Bustamante C D, Sutter N B, Mellersh C S, Parker H G, Ostrander E A. 2007. A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genetics, 3, e79.

Mu X, Brown L D, Liu Y, Schneider M F. 2007. Roles of the calcineurin and CaMK signaling pathways in fast-to-slow fiber type transformation of cultured adult mouse skeletal muscle fibers. Physiological Genomics, 30, 300–312.

Nakayama H, Wilkin B J, Bodi I, Molkentin J D. 2006. Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB Journal, 20, 1660–1670.

Nelson P L, Beck A, Cheng H. 2011. Transient receptor proteins illuminated: Current views on TRPs and disease. Veterinary Journal (London, England: 1997), 187, 153–164.

Park Y J, Yoo S A, Kim M, Kim W U. 2020. The role of Calcium-calcineurin-NFAT signaling pathway in health and autoimmune diseases. Frontiers in Immunology, 11, 195.

Pinto M C, Kihara A H, Goulart V A, Tonelli F M, Gomes K N, Ulrich H, Resende R R. 2015. Calcium signaling and cell proliferation. Cellular Signalling, 27, 2139–2149.

Puri B K. 2020. Calcium signaling and gene expression. Advances in Experimental Medicine and Biology, 1131, 537–545.

Rao A, Luo C, Hogan P G. 1997. Transcription factors of the NFAT family: Regulation and function. Annual Review of Immunology, 15, 707–747.

Ren R, Guo J, Chen Y, Zhang Y, Chen L, Xiong W. 2021. The role of Ca2+ /calcineurin/NFAT signalling pathway in osteoblastogenesis. Cell Proliferation, 54, e13122.

Rosenberg P, Hawkins A, Stiber J, Shelton J M, Hutcheson K, Bassel-Duby R, Shin D M, Yan Z, Williams R S. 2004. TRPC3 channels confer cellular memory of recent neuromuscular activity. Proceedings of the National Academy of Sciences of the United States of America, 101, 9387–9392.

Rusnak F, Mertz P. 2000. Calcineurin: Form and function. Physiological Reviews, 80, 1483–1521.

Schiaffino S, Reggiani C. 2011. Fiber types in mammalian skeletal muscles. Physiological Reviews, 91, 1447–1531.

Serrano-Pérez M C, Fernández M, Neria F, Berjón-Otero M, Doncel-Pérez E, Cano E, Tranque P. 2015. NFAT transcription factors regulate survival, proliferation, migration, and differentiation of neural precursor cells. Glia, 63, 987–1004.

Snoeck H W. 2020. Calcium regulation of stem cells. EMBO Reports, 21, e50028.

Sukumaran P, Nascimento Da Conceicao V, Sun Y, Ahamad N, Saraiva L R, Selvaraj S, Singh B B. 2021. Calcium signaling regulates autophagy and apoptosis. Cells, 10, 2125.

Sweeney H L, Hammers D W. 2018. Muscle contraction. Cold Spring Harbor Perspectives in Biology, 10, a023200.

Tham Y K, Bernardo B C, Ooi J Y, Weeks K L, Mcmullen J R. 2015. Pathophysiology of cardiac hypertrophy and heart failure: Signaling pathways and novel therapeutic targets. Archives of Toxicology, 89, 1401–1438.

Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R. 2000. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. The Journal of Biological Chemistry, 275, 40235–40243.

Wang B, Guo J, Zhang M, Liu Z, Zhou R, Guo F, Li K, Mu Y. 2021. Insulin-Degrading enzyme regulates the proliferation and apoptosis of porcine skeletal muscle stem cells via Myostatin/MYOD pathway. Frontiers in Cell and Developmental Biology, 9, 685593.

Wang Z, Wang Y, Tian X, Shen H, Dou Y, Li H, Chen G. 2016. Transient receptor potential channel 1/4 reduces subarachnoid hemorrhage-induced early brain injury in rats via calcineurin-mediated NMDAR and NFAT dephosphorylation. Scientific Reports, 6, 33577.

Yu Y, Fantozzi I, Remillard C V, Landsberg J W, Kunichika N, Platoshyn O, Tigno D D, Thistlethwaite P A, Rubin L J, Yuan J X. 2004. Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proceedings of the National Academy of Sciences of the United States of America, 101, 13861–13866.

Zhan C, Shi Y. 2017. TRPC channels and cell proliferation. Advances in Experimental Medicine and Biology, 976, 149–155.

Zhang B, Chen L, Bai Y G, Song J B, Cheng J H, Ma H Z, Ma J, Xie M J. 2020. miR–137 and its target T-type CaV 3.1 channel modulate dedifferentiation and proliferation of cerebrovascular smooth muscle cells in simulated microgravity rats by regulating calcineurin/NFAT pathway. Cell Proliferation, 53, e12774.

Zhang G, He M, Wu P, Zhang X, Zhou K, Li T, Zhang T, Xie K, Dai G, Wang J. 2021. MicroRNA-27b-3p targets the myostatin gene to regulate myoblast proliferation and is involved in myoblast differentiation. Cells, 10, 423.

Zhang J, Zhang L, Nie J, Lin Y, Li Y, Xu W, Zhao J Y, Zhao S M, Wang C. 2021. Calcineurin inactivation inhibits pyruvate dehydrogenase complex activity and induces the Warburg effect. Oncogene, 40, 6692–6702.

Zhang Q, Qi H, Cao Y, Shi P, Song C, Ba L, Chen Y, Gao J, Li S, Li B, Sun H. 2018. Activation of transient receptor potential vanilloid 3 channel (TRPV3) aggravated pathological cardiac hypertrophy via calcineurin/NFATc3 pathway in rats. Journal of Cellular and Molecular Medicine, 22, 6055–6067.

Zhao L, Sullivan M N, Chase M, Gonzales A L, Earley S. 2014. Calcineurin/nuclear factor of activated T cells-coupled vanilliod transient receptor potential channel 4 ca2+ sparklets stimulate airway smooth muscle cell proliferation. American Journal of Respiratory Cell and Molecular Biology, 50, 1064–1075.

Zhao Y, Yang L, Su G, Wei Z, Liu X, Song L, Hai C, Wu D, Hao Z, Wu Y, Zhang L, Bai C, Li G. 2022. Growth traits and sperm proteomics analyses of myostatin gene-edited Chinese Yellow Cattle. Life (Basel, Switzerland), 12, 627.

[1]	LIU Hui, LIU Chang, ZHAO Yu-hang, HAN Xue-jie, ZHOU Zheng-wei, WANG Chen, LI Rong-feng, LI Xue-ling . Comparing successful gene knock-in efficiencies of CRISPR/Cas9 with ZFNs and TALENs gene editing systems in bovine and dairy goat fetal fibroblasts[J]. >Journal of Integrative Agriculture, 2018, 17(2): 406-414.
[2]	LIU Dong-hua, HAN Hao-yuan, ZHANG Xin, SUN Ting, LAN Xian-yong, CHEN Hong, LEI Chu-zhao, DANG Rui-hua . *The genetic diversity analysis in the donkey myostatin* gene**[J]. >Journal of Integrative Agriculture, 2017, 16(03): 656-663.
[3]	QIAN Li-li, MA De-zun, GAO Peng-fei, JIANG Sheng-wang, WANG Qing-qing, CAI Chun-bo, XIAO Gao-jun, AN Xiao-rong, CUI Wen-tao. Muscle hypertrophy in transgenic mice due to over-expression of porcine myostatin mutated at its cleavage site[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2571-2577.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors