Coactivator-associated arginine methyltransferase 1: A versatile player in cell differentiation and development

Zhongrui Ma; Xinxing Lyu; Ning Qin; Haoyu Liu; Mengrui Zhang; Yongchao Lai; Bo Dong; Peiyuan Lu

doi:10.1016/j.gendis.2022.05.021

您当前的位置：

首页 >

文章列表页 >

Coactivator-associated arginine methyltransferase 1: A versatile player in cell differentiation and development

Review article | 更新时间：2024-02-04

- Coactivator-associated arginine methyltransferase 1: A versatile player in cell differentiation and development
- Genes & Diseases Vol. 1, Issue 6, Pages: 2383-2392(2023)
- 作者机构：
  
  1. Medical Research Center, The First Affiliated Hospital of Shandong First Medical University,Shandong,Jinan,China,250014
  2. Department of Immunology, Medical Science and Technology Innovation Center, Shandong First Medical University & Shandong Academy of Medical Sciences,Shandong,Jinan,China,250117
  3. Department of Biochemistry and Molecular Biology, School of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences,Shandong,Jinan,China,250117
  4. Department of Cardiology, Shandong Provincial Hospital Affiliated to Shandong First Medical University,Shandong,Jinan,China,250021
- 作者简介：
- 基金信息：
- DOI：10.1016/j.gendis.2022.05.021
  CLC：
- Published：2023，
  
  Published Online：1 November 2023，
扫描看全文
Zhongrui Ma, Xinxing Lyu, Ning Qin, et al. Coactivator-associated arginine methyltransferase 1: A versatile player in cell differentiation and development. [J]. Genes & Diseases 1(6):2383-2392(2023)
DOI：

Zhongrui Ma, Xinxing Lyu, Ning Qin, et al. Coactivator-associated arginine methyltransferase 1: A versatile player in cell differentiation and development. [J]. Genes & Diseases 1(6):2383-2392(2023) DOI： 10.1016/j.gendis.2022.05.021.

摘要

Abstract

Protein arginine methylation is a common post-translational modification involved in the regulation of various cellular functions. Coactivator-associated arginine methyltransferase 1 (CARM1) is a protein arginine methyltransferase that asymmetrically dimethylates histone H3 and non-histone proteins to regulate gene transcription. CARM1 has been found to play important roles in cell differentiation and development

cell cycle progression

autophagy

metabolism

pre-mRNA splicing and transportation

and DNA replication. In this review

we describe the molecular characteristics of CARM1 and summarize its roles in the regulation of cell differentiation and development in mammals.

关键词

Keywords

Arginine methylationCARM1Cell differentiationDevelopmentEpigenetic regulation

references

1 M.T. Bedford, S.G. ClarkeProtein arginine methylation in mammals: who, what, and why Mol Cell, 33 (1) (2009), pp. 1-13

2 H.W. Lee, S. Kim, W.K. PaikS-adenosylmethionine: protein-arginine methyltransferase. Purification and mechanism of the enzyme Biochemistry, 16 (1) (1977), pp. 78-85

3 Y. Yang, M.T. BedfordProtein arginine methyltransferases and cancer Nat Rev Cancer, 13 (1) (2013), pp. 37-50

4 R.S. Blanc, S. RichardArginine methylation: the coming of age Mol Cell, 65 (1) (2017), pp. 8-24

5 E. Guccione, S. RichardThe regulation, functions and clinical relevance of arginine methylation Nat Rev Mol Cell Biol, 20 (10) (2019), pp. 642-657

6 J. Jarrold, C.C. DaviesPRMTs and arginine methylation: cancer's best-kept secret? Trends Mol Med, 25 (11) (2019), pp. 993-1009

7 S.C. Larsen, K.B. Sylvestersen, A. Mund, et al.Proteome-wide analysis of arginine monomethylation reveals widespread occurrence in human cells Sci Signal, 9 (443) (2016), p. rs9

8 D. Chen, H. Ma, H. Hong, et al.Regulation of transcription by a protein methyltransferase Science, 284 (5423) (1999), pp. 2174-2177

9 S. Suresh, S. Huard, T. DuboisCARM1/PRMT4: making its mark beyond its function as a transcriptional coactivator Trends Cell Biol, 31 (5) (2021), pp. 402-417

10 M. Chevillard-Briet, D. Trouche, L. VandelControl of CBP co-activating activity by arginine methylation EMBO J, 21 (20) (2002), pp. 5457-5466

11 W. Xu, H. Chen, K. Du, et al.A transcriptional switch mediated by cofactor methylation Science, 294 (5551) (2001), pp. 2507-2511

12 S. El Messaoudi, E. Fabbrizio, C. Rodriguez, et al.Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the Cyclin E1 gene Proc Natl Acad Sci U S A, 103 (36) (2006), pp. 13351-13356

13 H.J. Shin, H. Kim, S. Oh, et al.AMPK-SKP2-CARM1 signalling cascade in transcriptional regulation of autophagy Nature, 534 (7608) (2016), pp. 553-557

14 C. Li, L. Yu, H. Xue, et al.Nuclear AMPK regulated CARM1 stabilization impacts autophagy in aged heart Biochem Biophys Res Commun, 486 (2) (2017), pp. 398-405

15 X. Wei, X. Li, W. Yan, X. Zhang, Y. Sun, F. ZhangSKP2 promotes hepatocellular carcinoma progression through nuclear AMPK-SKP2-CARM1 signaling transcriptionally regulating nutrient-deprived autophagy induction Cell Physiol Biochem, 47 (6) (2018), pp. 2484-2497

16 Y.S. Yu, H.R. Shin, D. Kim, et al.Pontin arginine methylation by CARM1 is crucial for epigenetic regulation of autophagy Nat Commun, 11 (1) (2020), p. 6297

17 Y.P. Wang, W. Zhou, J. Wang, et al.Arginine methylation of MDH1 by CARM1 inhibits glutamine metabolism and suppresses pancreatic cancer Mol Cell, 64 (4) (2016), pp. 673-687

18 F. Liu, F. Ma, Y. Wang, et al.PKM2 methylation by CARM1 activates aerobic glycolysis to promote tumorigenesis Nat Cell Biol, 19 (11) (2017), pp. 1358-1370

19 X.Y. Zhong, X.M. Yuan, Y.Y. Xu, et al.CARM1 methylates GAPDH to regulate glucose metabolism and is suppressed in liver cancer Cell Rep, 24 (12) (2018), pp. 3207-3223

20 Y. Liu, T. Wang, Y.J. Ji, et al.A C9orf72-CARM1 axis regulates lipid metabolism under glucose starvation-induced nutrient stress Genes Dev, 32 (21–22) (2018), pp. 1380-1397

21 Y.H. Lee, M.T. Bedford, M.R. StallcupRegulated recruitment of tumor suppressor BRCA1 to the p21 gene by coactivator methylation Genes Dev, 25 (2) (2011), pp. 176-188

22 N. Ohkura, M. Takahashi, H. Yaguchi, Y. Nagamura, T. TsukadaCoactivator-associated arginine methyltransferase 1, CARM1, affects pre-mRNA splicing in an isoform-specific manner J Biol Chem, 280 (32) (2005), pp. 28927-28935

23 D. Cheng, J. Côté, S. Shaaban, M.T. BedfordThe arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing Mol Cell, 25 (1) (2007), pp. 71-83

24 P. Kuhn, R. Chumanov, Y. Wang, Y. Ge, R.R. Burgess, W. XuAutomethylation of CARM1 allows coupling of transcription and mRNA splicing Nucleic Acids Res, 39 (7) (2011), pp. 2717-2726

25 M.M. Genois, J.P. Gagné, T. Yasuhara, et al.CARM1 regulates replication fork speed and stress response by stimulating PARP1 Mol Cell, 81 (4) (2021), pp. 784-800

26 N. Gupta, M.P. Madapura, U.A. Bhat, M.R. RaoMapping of post-translational modifications of transition proteins, TP1 and TP2, and identification of protein arginine methyltransferase 4 and lysine methyltransferase 7 as methyltransferase for TP2 J Biol Chem, 290 (19) (2015), pp. 12101-12122

27 L. Wang, P. Charoensuksai, N.J. Watson, et al.CARM1 automethylation is controlled at the level of alternative splicing Nucleic Acids Res, 41 (14) (2013), pp. 6870-6880

28 N.C. Chang, M.C. Sincennes, F.P. Chevalier, et al.The dystrophin glycoprotein complex regulates the epigenetic activation of muscle stem cell commitment Cell Stem Cell, 22 (5) (2018), pp. 755-768

29 C. Teyssier, D. Chen, M.R. StallcupRequirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function J Biol Chem, 277 (48) (2002), pp. 46066-46072

30 N. Troffer-Charlier, V. Cura, P. Hassenboehler, D. Moras, J. CavarelliFunctional insights from structures of coactivator-associated arginine methyltransferase 1 domains EMBO J, 26 (20) (2007), pp. 4391-4401

31 W.W. Yue, M. Hassler, S.M. Roe, V. Thompson-Vale, L.H. PearlInsights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase EMBO J, 26 (20) (2007), pp. 4402-4412

32 E. Shishkova, H. Zeng, F. Liu, et al.Global mapping of CARM1 substrates defines enzyme specificity and substrate recognition Nat Commun, 8 (2017), Article 15571

33 H. Wei, R. Mundade, K.C. Lange, T. LuProtein arginine methylation of non-histone proteins and its role in diseases Cell Cycle, 13 (1) (2014), pp. 32-41

34 J. Fuhrmann, K.W. Clancy, P.R. ThompsonChemical biology of protein arginine modifications in epigenetic regulation Chem Rev, 115 (11) (2015), pp. 5413-5461

35 Y. Morales, T. Cáceres, K. May, J.M. HevelBiochemistry and regulation of the protein arginine methyltransferases (PRMTs) Arch Biochem Biophys, 590 (2016), pp. 138-152

36 K. Higashimoto, P. Kuhn, D. Desai, X. Cheng, W. XuPhosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase 1 Proc Natl Acad Sci U S A, 104 (30) (2007), pp. 12318-12323

37 Q. Feng, B. He, S.Y. Jung, et al.Biochemical control of CARM1 enzymatic activity by phosphorylation J Biol Chem, 284 (52) (2009), pp. 36167-36174

38 S. Carascossa, P. Dudek, B. Cenni, P.A. Briand, D. PicardCARM1 mediates the ligand-independent and tamoxifen-resistant activation of the estrogen receptor alpha by cAMP Genes Dev, 24 (7) (2010), pp. 708-719

39 C.S. Lim, D.L. AlkonProtein kinase C stimulates HuD-mediated mRNA stability and protein expression of neurotrophic factors and enhances dendritic maturation of hippocampal neurons in culture Hippocampus, 22 (12) (2012), pp. 2303-2319

40 X. Li, Y. Lai, J. Li, M. Zou, C. ZouOxidative stress destabilizes protein arginine methyltransferase 4 via glycogen synthase kinase 3β to impede lung epithelial cell migration Am J Physiol Cell Physiol, 313 (3) (2017), pp. C285-C294

41 W.D. Cheung, K. Sakabe, M.P. Housley, W.B. Dias, G.W. HartO-linked beta-N-acetylglucosaminyltransferase substrate specificity is regulated by myosin phosphatase targeting and other interacting proteins J Biol Chem, 283 (49) (2008), pp. 33935-33941

42 K. Sakabe, G.W. HartO-GlcNAc transferase regulates mitotic chromatin dynamics J Biol Chem, 285 (45) (2010), pp. 34460-34468

43 P. Charoensuksai, P. Kuhn, L. Wang, N. Sherer, W. XuO-GlcNAcylation of co-activator-associated arginine methyltransferase 1 regulates its protein substrate specificity Biochem J, 466 (3) (2015), pp. 587-599

44 D. Kim, S. Lim, M. Park, et al.Ubiquitination-dependent CARM1 degradation facilitates Notch1-mediated podocyte apoptosis in diabetic nephropathy Cell Signal, 26 (9) (2014), pp. 1774-1782

45 M.R. Pawlak, C.A. Scherer, J. Chen, M.J. Roshon, H.E. RuleyArginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable Mol Cell Biol, 20 (13) (2000), pp. 4859-4869

46 W.W. Tee, M. Pardo, T.W. Theunissen, et al.Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency Genes Dev, 24 (24) (2010), pp. 2772-2777

47 N. Yadav, J. Lee, J. Kim, et al.Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice Proc Natl Acad Sci U S A, 100 (11) (2003), pp. 6464-6468

48 T. Ito, N. Yadav, J. Lee, et al.Arginine methyltransferase CARM1/PRMT4 regulates endochondral ossification BMC Dev Biol, 9 (2009), p. 47

49 J. Kim, J. Lee, N. Yadav, et al.Loss of CARM1 results in hypomethylation of thymocyte cyclic AMP-regulated phosphoprotein and deregulated early T cell development J Biol Chem, 279 (24) (2004), pp. 25339-25344

50 J. Li, Z. Zhao, C. Carter, L.I. Ehrlich, M.T. Bedford, E.R. RichieCoactivator-associated arginine methyltransferase 1 regulates fetal hematopoiesis and thymocyte development J Immunol, 190 (2) (2013), pp. 597-604

51 N. Yadav, D. Cheng, S. Richard, et al.CARM1 promotes adipocyte differentiation by coactivating PPARgamma EMBO Rep, 9 (2) (2008), pp. 193-198

52 K.B. O'Brien, M. Alberich-Jordà, N. Yadav, et al.CARM1 is required for proper control of proliferation and differentiation of pulmonary epithelial cells Development, 137 (13) (2010), pp. 2147-2156

53 M.E. Torres-Padilla, D.E. Parfitt, T. Kouzarides, M. Zernicka-GoetzHistone arginine methylation regulates pluripotency in the early mouse embryo Nature, 445 (7124) (2007), pp. 214-218

54 M. Goolam, A. Scialdone, S.J.L. Graham, et al.Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos Cell, 165 (1) (2016), pp. 61-74

55 M.D. White, J.F. Angiolini, Y.D. Alvarez, et al.Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo Cell, 165 (1) (2016), pp. 75-87

56 J. Wang, L. Wang, G. Feng, et al.Asymmetric expression of LincGET biases cell fate in two-cell mouse embryos Cell, 175 (7) (2018), pp. 1887-1901

57 A. Hupalowska, A. Jedrusik, M. Zhu, M.T. Bedford, D.M. Glover, M. Zernicka-GoetzCARM1 and paraspeckles regulate pre-implantation mouse embryo development Cell, 175 (7) (2018), pp. 1902-1916

58 S.L. Chen, K.A. Loffler, D. Chen, M.R. Stallcup, G.E. MuscatThe coactivator-associated arginine methyltransferase is necessary for muscle differentiation: CARM1 coactivates myocyte enhancer factor-2 J Biol Chem, 277 (6) (2002), pp. 4324-4333

59 Y. Kawabe, Y.X. Wang, I.W. McKinnell, M.T. Bedford, M.A. RudnickiCarm1 regulates Pax7 transcriptional activity through MLL1/2 recruitment during asymmetric satellite stem cell divisions Cell Stem Cell, 11 (3) (2012), pp. 333-345

60 J. Bao, S. Rousseaux, J. Shen, K. Lin, Y. Lu, M.T. BedfordThe arginine methyltransferase CARM1 represses p300•ACT•CREMτ activity and is required for spermiogenesis Nucleic Acids Res, 46 (9) (2018), pp. 4327-4343

61 J. Shi, Q. Chen, X. Li, et al.Dynamic transcriptional symmetry-breaking in pre-implantation mammalian embryo development revealed by single-cell RNA-seq Development, 142 (20) (2015), pp. 3468-3477

62 Y.S. Mao, H. Sunwoo, B. Zhang, D.L. SpectorDirect visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs Nat Cell Biol, 13 (1) (2011), pp. 95-101

63 H. Sun, J. Su, T. Wu, et al.CARM1 is heterogeneous in mouse four-cell embryo and important to blastocyst development Reproduction, 159 (1) (2020), pp. 91-104

64 H. Chakravarthy, B.D. Ormsbee, S.K. Mallanna, A. RizzinoRapid activation of the bivalent gene Sox21 requires displacement of multiple layers of gene-silencing machinery FASEB J, 25 (1) (2011), pp. 206-218

65 G. Yang, C. Zhou, R. Wang, et al.Base-editing-mediated R17H substitution in histone H3 reveals methylation-dependent regulation of Yap signaling and early mouse embryo development Cell Rep, 26 (2) (2019), pp. 302-312

66 M. Panamarova, A. Cox, K.B. Wicher, et al.The BAF chromatin remodelling complex is an epigenetic regulator of lineage specification in the early mouse embryo Development, 143 (8) (2016), pp. 1271-1283

67 S.M. Greenblatt, N. Man, P.J. Hamard, et al.CARM1 is essential for myeloid leukemogenesis but dispensable for normal hematopoiesis Cancer Cell, 34 (5) (2018), p. 868

68 W.V. Cardoso, J. LüRegulation of early lung morphogenesis: questions, facts and controversies Development, 133 (9) (2006), pp. 1611-1624

69 Y. Maeda, V. Davé, J.A. WhitsettTranscriptional control of lung morphogenesis Physiol Rev, 87 (1) (2007), pp. 219-244

70 T.J. Desai, D.G. Brownfield, M.A. KrasnowAlveolar progenitor and stem cells in lung development, renewal and cancer Nature, 507 (7491) (2014), pp. 190-194

71 S.B. Chargé, M.A. RudnickiCellular and molecular regulation of muscle regeneration Physiol Rev, 84 (1) (2004), pp. 209-238

72 N.A. Dumont, C.F. Bentzinger, M.C. Sincennes, M.A. RudnickiSatellite cells and skeletal muscle regeneration Compr Physiol, 5 (3) (2015), pp. 1027-1059

73 C.A. Collins, I. Olsen, P.S. Zammit, et al.Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche Cell, 122 (2) (2005), pp. 289-301

74 D. Montarras, J. Morgan, C. Collins, et al.Direct isolation of satellite cells for skeletal muscle regeneration Science, 309 (5743) (2005), pp. 2064-2067

75 S. Kuang, K. Kuroda, F. Le Grand, M.A. RudnickiAsymmetric self-renewal and commitment of satellite stem cells in muscle Cell, 129 (5) (2007), pp. 999-1010

76 C.S. Dacwag, M.T. Bedford, S. Sif, A.N. ImbalzanoDistinct protein arginine methyltransferases promote ATP-dependent chromatin remodeling function at different stages of skeletal muscle differentiation Mol Cell Biol, 29 (7) (2009), pp. 1909-1921

77 C. Mallappa, Y.J. Hu, P. Shamulailatpam, S. Tae, S. Sif, A.N. ImbalzanoThe expression of myogenic microRNAs indirectly requires protein arginine methyltransferase (Prmt)5 but directly requires Prmt4 Nucleic Acids Res, 39 (4) (2011), pp. 1243-1255

78 P.C.R.E.M. Sassone-CorsiA master-switch regulating the balance between differentiation and apoptosis in male germ cells Mol Reprod Dev, 56 (2 Suppl) (2000), pp. 228-229

79 D. Kim, J. Lee, D. Cheng, et al.Enzymatic activity is required for the in vivo functions of CARM1 J Biol Chem, 285 (2) (2010), pp. 1147-1152

80 G. Sanchez, E. Bondy-Chorney, J. Laframboise, et al.A novel role for CARM1 in promoting nonsense-mediated mRNA decay: potential implications for spinal muscular atrophy Nucleic Acids Res, 44 (6) (2016), pp. 2661-2676

81 Y. Liu, J. Li, Y. Shang, Y. Guo, Z. LiCARM1 contributes to skeletal muscle wasting by mediating FoxO3 activity and promoting myofiber autophagy Exp Cell Res, 374 (1) (2019), pp. 198-209

82 R. Hu, M.Q. Wang, L.Y. Liu, et al.Calycosin inhibited autophagy and oxidative stress in chronic kidney disease skeletal muscle atrophy by regulating AMPK/SKP2/CARM1 signalling pathway J Cell Mol Med, 24 (19) (2020), pp. 11084-11099

83 D.I. Kim, M.J. Park, S.K. Lim, et al.High-glucose-induced CARM1 expression regulates apoptosis of human retinal pigment epithelial cells via histone 3 arginine 17 dimethylation: role in diabetic retinopathy Arch Biochem Biophys, 560 (2014), pp. 36-43

84 N. Guo, A. Nulahou, Q. Bu, et al.MiR-542-5p regulates the progression of diabetic retinopathy by targeting CARM1 Acta Biochim Pol, 67 (3) (2020), pp. 373-378

85 L. Pang, H. Tian, N. Chang, et al.Loss of CARM1 is linked to reduced HuR function in replicative senescence BMC Mol Biol, 14 (2013), p. 15

86 R.S. Sarker, G. John-Schuster, A. Bohla, et al.Coactivator-associated arginine methyltransferase-1 function in alveolar epithelial senescence and elastase-induced emphysema susceptibility Am J Respir Cell Mol Biol, 53 (6) (2015), pp. 769-781

87 Z. Xu, W. Wu, F. Shen, Y. Yu, Y. Wang, C. XiangHistone arginine methylation-mediated epigenetic regulation of discoidin domain receptor 2 controls the senescence of human bone marrow mesenchymal stem cells Stem Cells Int, 2019 (2019), Article 7670316

88 K.J. Veazey, D. Cheng, K. Lin, et al.CARM1 inhibition reduces histone acetyltransferase activity causing synthetic lethality in CREBBP/EP300-mutated lymphomas Leukemia, 34 (12) (2020), pp. 3269-3285

89 S. Kumar, Z. Zeng, A. Bagati, et al.CARM1 inhibition enables immunotherapy of resistant tumors by dual action on tumor cells and T cells Cancer Discov, 11 (8) (2021), pp. 2050-2071

90 Z. Zhang, Z. Guo, X. Xu, et al.Structure-based discovery of potent CARM1 inhibitors for solid tumor and cancer immunology therapy J Med Chem, 64 (22) (2021), pp. 16650-16674

91 F. Inoue, K. Sone, Y. Toyohara, et al.Histone arginine methyltransferase CARM1 selective inhibitor TP-064 induces apoptosis in endometrial cancer Biochem Biophys Res Commun, 601 (2022), pp. 123-128

查看原文

Views

下载量

CSCD

Alert me when the article has been cited

提交

Tools

Publicity Resources

The Wnt-dependent and Wnt-independent functions of BCL9 in development, tumorigenesis, and immunity: Implications in therapeutic opportunities

New insights into the roles for DYRK family in mammalian development and congenital diseases

Long noncoding RNA (lncRNA) H19: An essential developmental regulator with expanding roles in cancer, stem cell differentiation, and metabolic diseases

The function and mechanism of lactate and lactylation in tumor metabolism and microenvironment

Long noncoding RNA XIST: Mechanisms for X chromosome inactivation, roles in sex-biased diseases, and therapeutic opportunities

Related Author

Jianxiang Chen

Fangtian Bu

Haojin Gao

Mengqing Sun

Chao Xu

Heng Dong

Minjie Wu

Kiyotsugu Yoshida

Related Institution

Key Laboratory of Elemene Class Anti-Cancer Chinese Medicines, Engineering Laboratory of Development and Application of Traditional Chinese Medicines, Collaborative Innovation Center of Traditional Chinese Medicines of Zhejiang Province, Hangzhou Normal University

Laboratory of Cancer Genomics, Division of Cellular and Molecular Research, National Cancer Centre

College of Pharmacy and Department of Hepatology, Institute of Hepatology and Metabolic Diseases, The Affiliated Hospital of Hangzhou Normal University, Hangzhou Normal University

Department of Biochemistry, The Jikei University School of Medicine, Minato-, Tokyo 61

Laboratory of Craniofacial Suture Biology and Development, Department of Surgery Section of Plastic Surgery, The University of Chicago Medical Center

⁰