综述 REVIEW

组蛋白修饰调控骨骼肌再生过程中肌卫星细胞命运的研究进展

  • 邢敬亚 ,
  • 芒来 ,
  • 刘桂芹 ,
  • 张心壮
展开
  • 1. 内蒙古农业大学动物科学学院, 内蒙古自治区马属动物遗传育种与繁殖学重点实验室, 内蒙古农业大学马属动物研究中心, 呼和浩特 010018;
    2. 聊城大学农学院, 山东黑毛驴高效繁育与生态工程技术研究中心, 山东毛驴产业科技协同创新中心, 聊城 252059
邢敬亚(1988—),女,山东临清人,博士,研究方向为马属动物营养。E-mail:467064302@qq.com

收稿日期: 2021-10-24

  网络出版日期: 2022-05-14

基金资助

国家自然科学基金项目(31902188);内蒙古自然科学基金(2021MS03016);国家重点研发计划项目(2017YFE0108700);内蒙古农业大学高层次引进人才启动项目(NDGCC2016-01);内蒙古农业大学动物科学学院青年基金项目(QN202114);内蒙古自治区应用技术研究项目(2019GG242);聊城大学畜牧学学科开放课题(319312101-03);山东省驴产业创新团队项目资助(SDAIT-27);山东省驴产业科技协同创新中心开放课题(3193308);研究生科研创新资助项目(DC2100002428)

Research Progress of Histone Modification Regulates Fate of Satellite Cells During Skeletal Muscle Regeneration

  • XING Jingya ,
  • MANG Lai ,
  • LIU Guiqin ,
  • ZHANG Xinzhuang
Expand
  • 1. Equine Research Center of Inner Mongolia Agricultural University, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China;
    2. Shandong Donkey Industry Technology Collaborative Innovation Center, Shandong Engineering Technology Research Center for Efficient Breeding and Ecological Feeding of Black Donkey, College of Agronomy, Liaocheng University, Liaocheng 252059, China

Received date: 2021-10-24

  Online published: 2022-05-14

摘要

在哺乳动物幼年和青年期,骨骼肌卫星细胞受到组织中环境因子的刺激介导其不断增殖和分化,促进肌肉有效的发育。骨骼肌卫星细胞命运的变化是由于来自肌肉环境的细胞信号传导通过表观遗传机制导致基因表达改变的结果,这种机制包括组蛋白修饰、转录因子的共价结合以及染色质重塑。其中,组蛋白修饰可以通过调控转录机制对特定位点进行修饰实现差异基因表达,进而调控骨骼肌卫星细胞的命运及不同状态肌细胞之间的准确转换。本文概述了骨骼肌再生过程中肌卫星细胞命运转变的发生机理,讨论了组蛋白修饰调控骨骼肌卫星细胞从静息到激活再到增殖和分化的肌源性过程。组蛋白修饰在调控骨骼肌卫星细胞状态的重要性有望成为疾病干预的靶点,以期为促进哺乳动物个体生长、改善肌肉再生和促进病理状态下肌肉平衡提供参考。

本文引用格式

邢敬亚 , 芒来 , 刘桂芹 , 张心壮 . 组蛋白修饰调控骨骼肌再生过程中肌卫星细胞命运的研究进展[J]. 动物营养学报, 2022 , 34(5) : 2741 -2751 . DOI: 10.3969/j.issn.1006-267x.2022.05.003

Abstract

In young mammals and adults, skeletal muscle satellite cells are stimulated by environmental factors in the tissue to mediate the continuous proliferation and differentiation of skeletal muscle satellite cells, and promote effective muscle development. Changes in the fate of skeletal muscle satellite cells are caused by differences in gene expression due to cell signaling from the muscle environment. Integration of signals from the muscle environment leads to changes in gene expression through epigenetic mechanism. Such mechanisms, including histone modification changes, covalent binding of transcription factors and chromatin remodeling. Among them, histone modification can modify specific sites to achieve expression of the differential gene by regulating the transcription mechanism, thus regulating the fate of skeletal muscle satellite cells and the accurate conversion between muscle cells in different states. This article summaries the mechanism of skeletal muscle satellite cells fate transition during skeletal muscle regeneration, and discusses the epigenetic control of skeletal muscle satellite cells during the myogenic process from resting to activation to proliferation and differentiation. The importance of histone modification in regulating the state of skeletal muscle satellite cells is expected to become a target for disease intervention, in order to provide a reference for promoting individual mammalian growth, improving muscle regeneration and promoting muscle homeostasis under pathological conditions.

参考文献

[1] SPALDING K L, BHARDWAJ R D, BUCHHOLZ B A, et al.Retrospective birth dating of cells in humans[J].Cell, 2005, 122(1):133-143.  
[2] MOSS F P, LEBLOND C P.Satellite cells as the source of nuclei in muscles of growing rats[J].The Anatomical Record-Advances in Integrative Anatomy and Evolutionary Biology, 1971, 170(4):421-435.
[3] SNOW M H.An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats[J].Cell and Tissue Research, 1978, 186(3):535-540.
[4] SAKUMA K, YAMAGUCHI A.Recent advances in pharmacological, hormonal, and nutritional intervention for sarcopenia[J].Pflügers Archiv-European Journal of Physiology, 2018, 470(3):449-460.  
[5] SEGALÉS J, PERDIGUERO E, MUÑOZ-CÁNOVES P.Epigenetic control of adult skeletal muscle stem cell functions[J].The FEBS Journal, 2015, 282(9):1571-1588.  
[6] BIGOT A, DUDDY W J, OUANDAOGO Z G, et al.Age-associated methylation suppresses SPRY1, leading to a failure of re-quiescence and loss of the reserve stem cell pool in elderly muscle[J].Cell Reports, 2015, 13(6):1172-1182.  
[7] FATICA A, BOZZONI I.Long non-coding RNAs:new players in cell differentiation and development[J].Nature Reviews Genetics, 2014, 15(1):7-21.  
[8] CONSALVI S, BRANCACCIO A, DALL'AGNESE A, et al.Praja1 E3 ubiquitin ligase promotes skeletal myogenesis through degradation of EZH2 upon p38α activation[J].Nature Communications, 2017, 8:13956.
[9] WANG L N, WANG Z, YANG K L, et al.Epigallocatechin gallate reduces slow-twitch muscle fiber formation and mitochondrial biosynthesis in C2C12 cells by repressing AMPK activity and PGC-1α expression[J].Journal of Agricultural and Food Chemistry, 2016, 64(34):6517-6523.  
[10] IRAZOQUI A P, BOLAND R L, BUITRAGO C G.Actions of 1, 25(OH)2-vitamin D3 on the cellular cycle depend on VDR and p38 MAPK in skeletal muscle cells[J].Journal of Molecular Endocrinology, 2014, 53(3):331-343.  
[11] JIN C L, ZHANG Z M, SONG Z W, et al.mTORC1-mediated satellite cell differentiation is required for lysine-induced skeletal muscle growth[J].Journal of Agricultural and Food Chemistry, 2020, 68(17):4884-4892.  
[12] CHEN X L, XIANG L, JIA G, et al.Leucine regulates slow-twitch muscle fibers expression and mitochondrial function by Sirt1/AMPK signaling in porcine skeletal muscle satellite cells[J].Animal Science Journal, 2019, 90(2):255-263.  
[13] NARLIKAR G J, FAN H Y, KINGSTON R E.Cooperation between complexes that regulate chromatin structure and transcription[J].Cell, 2002, 108(4):475-487.  
[14] JIN W, PENG J, JIANG S W.The epigenetic regulation of embryonic myogenesis and adult muscle regeneration by histone methylation modification[J].Biochemistry and Biophysics Reports, 2016, 6:209-219.
[15] FRONTERA W R, OCHALA J.Skeletal muscle:a brief review of structure and function[J].Calcified Tissue International, 2015, 96(3):183-195.  
[16] TANG Z L, LI Y, WAN P, et al.LongSAGE analysis of skeletal muscle at three prenatal stages in Tongcheng and Landrace pigs[J].Genome Biology, 2007, 8(6):R115.
[17] ALMADA A E, WAGERS A J.Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease[J].Nature Reviews Molecular Cell Biology, 2016, 17(5):267-279.  
[18] SINGH K, DILWORTH F J.Differential modulation of cell cycle progression distinguishes members of the myogenic regulatory factor family of transcription factors[J].The FEBS Journal, 2013, 280(17):3991-4003.  
[19] SOLEIMANI V D, PUNCH V G, KAWABE Y I, et al.Transcriptional dominance of Pax7 in adult myogenesis is due to high-affinity recognition of homeodomain motifs[J].Developmental Cell, 2012, 22(6):1208-1220.  
[20] GVNTHER S, KIM J, KOSTIN S, et al.Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells[J].Cell Stem Cell, 2013, 13(5):590-601.  
[21] GARCÍA-PRAT L, PERDIGUERO E, ALONSO-MARTÍN S, et al.FoxO maintains a genuine muscle stem-cell quiescent state until geriatric age[J].Nature Cell Biology, 2020, 22(11):1307-1318.  
[22] BEAUCHAMP J R, HESLOP L, YU D S, et al.Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells[J].Journal of Cell Biology, 2000, 151(6):1221-1234.  
[23] YABLONKA-REUVENI Z, RUDNICKI M A, RIVERA A J, et al.The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD[J].Developmental Biology, 1999, 210(2):440-455.  
[24] HINTERBERGER T J, SASSOON D A, RHODES S J, et al.Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development[J].Developmental Biology, 1991, 147(1):144-156.  
[25] LAZURE F, BLACKBURN D M, CORCHADO A H, et al.Myf6/MRF4 is a myogenic niche regulator required for the maintenance of the muscle stem cell pool[J].EMBO Reports, 2020, 21(12):e49499.
[26] ZHU Z, MILLER J B.MRF4 can substitute for myogenin during early stages of myogenesis[J].Developmental Dynamics, 1997, 209(2):233-241.  
[27] CAO Y, YAO Z Z, SARKAR D, et al.Genome-wide MyoD binding in skeletal muscle cells:a potential for broad cellular reprogramming[J].Developmental Cell, 2010, 18(4):662-674.  
[28] BLUM R, VETHANTHAM V, BOWMAN C, et al.Genome-wide identification of enhancers in skeletal muscle:the role of MyoD1[J].Genes & Development, 2012, 26(24):2763-2779.  
[29] LLUÍS F, PERDIGUERO E, NEBREDA A R, et al.Regulation of skeletal muscle gene expression by p38 MAP kinases[J].Trends in Cell Biology, 2006, 16(1):36-44.  
[30] MACHADO L, ESTEVES DE LIMA J, FABRE O, et al.In situ fixation redefines quiescence and early activation of skeletal muscle stem cells[J].Cell Reports, 2017, 21(7):1982-1993.  
[31] YUE L, WAN R, LUAN S Y, et al.Dek modulates global intron retention during muscle stem cells quiescence exit[J].Developmental Cell, 2020, 53(6):661-676.e6.  
[32] MASSENET J, GARDNER E, CHAZAUD B, et al.Epigenetic regulation of satellite cell fate during skeletal muscle regeneration[J].Skeletal Muscle, 2021, 11(1):4.
[33] VAN VELTHOVEN C T J, DE MORREE A, EGNER I M, et al.Transcriptional profiling of quiescent muscle stem cells in vivo[J].Cell Reports, 2017, 21(7):1994-2004.  
[34] LIU L, CHEUNG T H, CHARVILLE G W, et al.Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging[J].Cell Reports, 2013, 4(1):189-204.  
[35] LIU L, CHEUNG T H, CHARVILLE G W, et al.Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting[J].Nature Protocols, 2015, 10(10):1612-1624.  
[36] SOUSA-VICTOR P, GUTARRA S, GARCÍA-PRAT L, et al.Geriatric muscle stem cells switch reversible quiescence into senescence[J].Nature, 2014, 506(7488):316-321.  
[37] GOPINATH S D, WEBB A E, BRUNET A, et al.FoxO3 promotes quiescence in adult muscle stem cells during the process of self-renewal[J].Stem Cell Reports, 2014, 2(4):414-426.  
[38] BJORNSON C R R, CHEUNG T H, LIU L, et al.Notch signaling is necessary to maintain quiescence in adult muscle stem cells[J].Stem Cells, 2012, 30(2):232-242.  
[39] BRACK A S, RANDO T A.Tissue-specific stem cells:lessons from the skeletal muscle satellite cell[J].Cell Stem Cell, 2012, 10(5):504-514.  
[40] BOONSANAY V, ZHANG T, GEORGIEVA A, et al.Regulation of skeletal muscle stem cell quiescence by Suv4-20h1-dependent facultative heterochromatin formation[J].Cell Stem Cell, 2016, 18(2):229-242.  
[41] JUAN A H, DERFOUL A, FENG X S, et al.Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells[J].Genes & Development, 2011, 25(8):789-794.  
[42] LI Y F, DILWORTH F J.Compacting chromatin to ensure muscle satellite cell quiescence[J].Cell Stem Cell, 2016, 18(2):162-164.  
[43] DILWORTH F J, BLAIS A.Epigenetic regulation of satellite cell activation during muscle regeneration[J].Stem Cell Research & Therapy, 2011, 2(2):18.
[44] ADDICKS G C, BRUN C E, SINCENNES M C, et al.MLL1 is required for PAX7 expression and satellite cell self-renewal in mice[J].Nature Communications, 2019, 10(1):4256.
[45] PALACIOS D, MOZZETTA C, CONSALVI S, et al.TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration[J].Cell Stem Cell, 2010, 7(4):455-469.  
[46] WOODHOUSE S, PUGAZHENDHI D, BRIEN P, et al.Ezh2 maintains a key phase of muscle satellite cell expansion but does not regulate terminal differentiation[J].Journal of Cell Science, 2013, 126(Pt 2):565-579.
[47] LEE S H, JOO S T, RYU Y C.Skeletal muscle fiber type and myofibrillar proteins in relation to meat quality[J].Meat Science, 2010, 86(1):166-170.  
[48] SINGH K, CASSANO M, PLANET E, et al.A KAP1 phosphorylation switch controls MyoD function during skeletal muscle differentiation[J].Genes & Development, 2015, 29(5):513-525.  
[49] PURI P L, IEZZI S, STIEGLER P, et al.Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis[J].Molecular Cell, 2001, 8(4):885-897.  
[50] LING B M T, BHARATHY N, CHUNG T K, et al.Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation[J].Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(3):841-846.  
[51] DILWORTH F J, SEAVER K J, FISHBURN A L, et al.In vitro transcription system delineates the distinct roles of the coactivators pCAF and p300 during MyoD/E47-dependent transactivation[J].Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(32):11593-11598.  
[52] CHOI J, JANG H, KIM H, et al.Histone demethylase LSD1 is required to induce skeletal muscle differentiation by regulating myogenic factors[J].Biochemical and Biophysical Research Communications, 2010, 401(3):327-332.  
[53] SOLEIMANI V D, YIN H, JAHANI-ASL A, et al.Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis[J].Molecular Cell, 2012, 47(3):457-468.  
[54] LUO D, DE MORREE A, BOUTET S, et al.Deltex2 represses MyoD expression and inhibits myogenic differentiation by acting as a negative regulator of Jmjd1c[J].Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(15):E3071-E3080.
[55] TAKAHASHI Y, RAYMAN J B, DYNLACHT B D.Analysis of promoter binding by the E2F and pRB families in vivo:distinct E2F proteins mediate activation and repression[J].Genes & Development, 2000, 14(7):804-816.  
[56] TAUBERT S, GORRINI C, FRANK S R, et al.E2F-dependent histone acetylation and recruitment of the Tip60 acetyltransferase complex to chromatin in late G1[J].Molecular and Cellular Biology, 2004, 24(10):4546-4556.  
[57] RAO V K, OW J R, SHANKAR S R, et al.G9a promotes proliferation and inhibits cell cycle exit during myogenic differentiation[J].Nucleic Acids Research, 2016, 44(17):8129-8143.  
[58] NIGHTINGALE K P, GENDREIZIG S, WHITE D A, et al.Cross-talk between histone modifications in response to histone deacetylase inhibitors:MLL4 links histone H3 acetylation and histone H3K4 methylation[J].Journal of Biological Chemistry, 2007, 282(7):4408-4416.  
[59] SEBASTIAN S, SREENIVAS P, SAMBASIVAN R, et al.MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation[J].Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(12):4719-4724.  
[60] YI X, TAO Y, LIN X, et al.Histone methyltransferase Setd2 is critical for the proliferation and differentiation of myoblasts[J].Biochimica et Biophysica Acta-Molecular Cell Research, 2017, 1864(4):697-707.  
[61] BYRNE K, MCWILLIAM S, VUOCOLO T, et al.Genomic architecture of histone 3 lysine 27 trimethylation during late ovine skeletal muscle development[J].Animal Genetics, 2014, 45(3):427-438.  
[62] BLAIS A, DYNLACHT B D.E2F-associated chromatin modifiers and cell cycle control[J].Current Opinion in Cell Biology, 2007, 19(6):658-662.  
[63] BLAIS A, VAN OEVELEN C J C, MARGUERON R, et al.Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit[J].Journal of Cell Biology, 2007, 179(7):1399-1412.  
[64] BALCIUNAITE E, SPEKTOR A, LENTS N H, et al.Pocket protein complexes are recruited to distinct targets in quiescent and proliferating cells[J].Molecular and Cellular Biology, 2005, 25(18):8166-8178.  
[65] DIMOVA D K, STEVAUX O, FROLOV M V, et al.Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway[J].Genes & Development, 2003, 17(18):2308-2320.  
[66] HSU J, ARAND J, CHAIKOVSKY A, et al.E2F4 regulates transcriptional activation in mouse embryonic stem cells independently of the RB family[J].Nature Communications, 2019, 10(1):2939.
[67] SCHWARTZ Y B, PIRROTTA V.Polycomb silencing mechanisms and the management of genomic programmes[J].Nature Reviews Genetics, 2007, 8(1):9-22.  
[68] TROJER P, LI G H, SIMS R J, et al.L3MBTL1, a histone-methylation-dependent chromatin lock[J].Cell, 2007, 129(5):915-928.  
[69] VERRIER L, ESCAFFIT F, CHAILLEUX C, et al.A new isoform of the histone demethylase JMJD2A/KDM4A is required for skeletal muscle differentiation[J].Plos Genetics, 2011, 7(6):e1001390.
[70] DACWAG C S, OHKAWA Y, PAL S, et al.The protein arginine methyltransferase Prmt5 is required for myogenesis because it facilitates ATP-dependent chromatin remodeling[J].Molecular and Cellular Biology, 2007, 27(1):384-394.  
[71] CASTIGLIONI I, CACCIA R, GARCIA-MANTEIGA J M, et al.The trithorax protein ash1L promotes myoblast fusion by activating Cdon expression[J].Nature Communications, 2018, 9(1):5026.
文章导航

/