Skip to main content
SpringerLink
Log in

The Role of Protein Deimination in Epigenetics

  • Chapter
  • First Online:
Protein Deimination in Human Health and Disease

  • 1150 Accesses

Abstract

Accumulating evidence suggests that epigenetic factors exemplified by histone posttranslational modification (PTM) cooperate with DNA sequence to control a diverse range of biological processes, including cell differentiation and reprogramming, organism development, and tissue homeostasis. Protein deimination of nucleosomal histones is a relatively less-characterized form of histone PTM. However, it appears to play a unique and incompletely understood role in epigenetics. At a molecular level, histone deimination directly antagonizes arginine methylation on histone tails, thereby interfering with the transcriptional consequences of such an effect. In addition, deimination can also affect the activity of important histone-modifying enzymes, such as the acetyl transferase p300, consequently amplifying the transcriptional outputs. In physiological or pathological conditions, histone deimination mediates chromatin decondensation and elicits cell-specific innate immune response in neutrophils; increased histone deimination has been observed in the normal-appearing white matter of multiple sclerosis (MS) patients. In this chapter, we first review the concepts in epigenetics and then discuss the roles that protein deimination play in human health and disease.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 159.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agarwal N, Hardt T, Brero A, Nowak D, Rothbauer U, Becker A, Leonhardt H, Cardoso MC (2007) MeCP2 interacts with HP1 and modulates its heterochromatin association during myogenic differentiation. Nucleic Acids Res 35:5402–5408

    Article  PubMed  CAS  Google Scholar 

  • An W, Kim J, Roeder RG (2004) Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117:735–748

    Article  PubMed  CAS  Google Scholar 

  • Banerjee T, Chakravarti D (2011) A peek into the complex realm of histone phosphorylation. Mol Cell Biol 31:4858–4873

    Article  PubMed  CAS  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

    Article  PubMed  CAS  Google Scholar 

  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  PubMed  CAS  Google Scholar 

  • Bauer UM, Daujat S, Nielsen SJ, Nightingale K, Kouzarides T (2002) Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep 3:39–44

    Article  PubMed  CAS  Google Scholar 

  • Beniac DR, Wood DD, Palaniyar N, Ottensmeyer FP, Moscarello MA, Harauz G (2000) Cryoelectron microscopy of protein-lipid complexes of human myelin basic protein charge isomers differing in degree of citrullination. J Struct Biol 129:80–95

    Article  PubMed  CAS  Google Scholar 

  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K et al (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326

    Article  PubMed  CAS  Google Scholar 

  • Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128:669–681

    Article  PubMed  CAS  Google Scholar 

  • Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535

    Article  PubMed  CAS  Google Scholar 

  • Cao L, Goodin R, Wood D, Moscarello MA, Whitaker JN (1999) Rapid release and unusual stability of immunodominant peptide 45–89 from citrullinated myelin basic protein. Biochemistry 38:6157–6163

    Article  PubMed  CAS  Google Scholar 

  • Chang X, Han J (2006) Expression of peptidylarginine deiminase type 4 (PAD4) in various tumors. Mol Carcinog 45:183–196

    Article  PubMed  CAS  Google Scholar 

  • Chang B, Chen Y, Zhao Y, Bruick RK (2007) JMJD6 is a histone arginine demethylase. Science 318:444–447

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Huang SM, Stallcup MR (2000) Synergistic, p160 coactivator-dependent enhancement of estrogen receptor function by CARM1 and p300. J Biol Chem 275:40810–40816

    Article  PubMed  CAS  Google Scholar 

  • Cheng X, Blumenthal RM (2008) Mammalian DNA methyltransferases: a structural perspective. Structure 16:341–350

    Article  PubMed  Google Scholar 

  • Cherrington BD, Morency E, Struble AM, Coonrod SA, Wakshlag JJ (2010) Potential role for peptidylarginine deiminase 2 (PAD2) in citrullination of canine mammary epithelial cell histones. PLoS One 5:e11768

    Article  PubMed  Google Scholar 

  • Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K (2009) Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4:80–93

    Article  PubMed  CAS  Google Scholar 

  • Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, Schneider R, Gregory PD, Tempst P, Bannister AJ et al (2004) Histone deimination antagonizes arginine methylation. Cell 118:545–553

    Article  PubMed  CAS  Google Scholar 

  • de Seze J, Dubucquoi S, Lefranc D, Virecoulon F, Nuez I, Dutoit V, Vermersch P, Prin L (2001) IgG reactivity against citrullinated myelin basic protein in multiple sclerosis. J Neuroimmunol 117:149–155

    Article  PubMed  Google Scholar 

  • Denis H, Deplus R, Putmans P, Yamada M, Metivier R, Fuks F (2009) Functional connection between deimination and deacetylation of histones. Mol Cell Biol 29:4982–4993

    Article  PubMed  CAS  Google Scholar 

  • Deraos G, Chatzantoni K, Matsoukas MT, Tselios T, Deraos S, Katsara M, Papathanasopoulos P, Vynios D, Apostolopoulos V, Mouzaki A et al (2008) Citrullination of linear and cyclic altered peptide ligands from myelin basic protein (MBP(87–99)) epitope elicits a Th1 polarized response by T cells isolated from multiple sclerosis patients: implications in triggering disease. J Med Chem 51:7834–7842

    Article  PubMed  CAS  Google Scholar 

  • Di Lorenzo A, Bedford MT (2011) Histone arginine methylation. FEBS Lett 585:2024–2031

    Article  PubMed  Google Scholar 

  • Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3:224–229

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA et al (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38:1378–1385

    Article  PubMed  CAS  Google Scholar 

  • Feil R, Fraga MF (2011) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13:97–109

    Google Scholar 

  • Greer EL, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13:343–357

    Article  PubMed  CAS  Google Scholar 

  • Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, Schuchlautz H, Luscher B, Amati B (2007) Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449:933–937

    Article  PubMed  CAS  Google Scholar 

  • Guo Q, Fast W (2011) Citrullination of inhibitor of growth 4 (ING4) by peptidylarginine deminase 4 (PAD4) disrupts the interaction between ING4 and p53. J Biol Chem 286:17069–17078

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara T, Hidaka Y, Yamada M (2005) Deimination of histone H2A and H4 at arginine 3 in HL-60 granulocytes. Biochemistry 44:5827–5834

    Article  PubMed  CAS  Google Scholar 

  • Hassan YI, Zempleni J (2006) Epigenetic regulation of chromatin structure and gene function by biotin. J Nutr 136:1763–1765

    PubMed  CAS  Google Scholar 

  • Heyn H, Esteller M (2012) DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 13:679–682

    Article  PubMed  CAS  Google Scholar 

  • Hyllus D, Stein C, Schnabel K, Schiltz E, Imhof A, Dou Y, Hsieh J, Bauer UM (2007) PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 21:3369–3380

    Article  PubMed  CAS  Google Scholar 

  • Illingworth R, Kerr A, Desousa D, Jorgensen H, Ellis P, Stalker J, Jackson D, Clee C, Plumb R, Rogers J et al (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6:e22

    Article  PubMed  Google Scholar 

  • Kan R, Yurttas P, Kim B, Jin M, Wo L, Lee B, Gosden R, Coonrod SA (2011) Regulation of mouse oocyte microtubule and organelle dynamics by PADI6 and the cytoplasmic lattices. Dev Biol 350:311–322

    Article  PubMed  CAS  Google Scholar 

  • Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bahler J, Green RD, Kouzarides T (2007) Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449:928–932

    Article  PubMed  CAS  Google Scholar 

  • Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Green RD, Kouzarides T (2009) Distinct transcriptional outputs associated with mono- and dimethylated histone H3 arginine 2. Nat Struct Mol Biol 16:449–451

    Article  PubMed  CAS  Google Scholar 

  • Kleinschmidt MA, de Graaf P, van Teeffelen HA, Timmers HT (2012) Cell cycle regulation by the PRMT6 arginine methyltransferase through repression of cyclin-dependent kinase inhibitors. PLoS One 7:e41446

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Koh SS, Zhang X, Cheng X, Stallcup MR (2002) Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol Cell Biol 22:3621–3632

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Coonrod SA, Kraus WL, Jelinek MA, Stallcup MR (2005) Regulation of coactivator complex assembly and function by protein arginine methylation and demethylimination. Proc Natl Acad Sci U S A 102:3611–3616

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Ma H, Tan TZ, Ng SS, Soong R, Mori S, Fu XY, Zernicka-Goetz M, Wu Q (2012) Protein arginine methyltransferase 6 regulates embryonic stem cell identity. Stem Cells Dev 28:2613–22

    Article  Google Scholar 

  • Li P, Yao H, Zhang Z, Li M, Luo Y, Thompson PR, Gilmour DS, Wang Y (2008) Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol Cell Biol 28:4745–4758

    Article  PubMed  CAS  Google Scholar 

  • Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y (2010a) PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 207:1853–1862

    Article  PubMed  CAS  Google Scholar 

  • Li P, Wang D, Yao H, Doret P, Hao G, Shen Q, Qiu H, Zhang X, Wang Y, Chen G (2010b) Coordination of PAD4 and HDAC2 in the regulation of p53-target gene expression. Oncogene 29:3153–3162

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM et al (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322

    Article  PubMed  CAS  Google Scholar 

  • Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260

    Article  PubMed  CAS  Google Scholar 

  • Luger K, Dechassa ML, Tremethick DJ (2012) New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat Rev Mol Cell Biol 13:436–447

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Baumann CT, Li H, Strahl BD, Rice R, Jelinek MA, Aswad DW, Allis CD, Hager GL, Stallcup MR (2001) Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr Biol 11:1981–1985

    Article  PubMed  CAS  Google Scholar 

  • Masson-Bessiere C, Sebbag M, Girbal-Neuhauser E, Nogueira L, Vincent C, Senshu T, Serre G (2001) The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol 166:4177–4184

    PubMed  CAS  Google Scholar 

  • Mastronardi FG, Wood DD, Mei J, Raijmakers R, Tseveleki V, Dosch HM, Probert L, Casaccia-Bonnefil P, Moscarello MA (2006) Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: a role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. J Neurosci 26:11387–11396

    Article  PubMed  CAS  Google Scholar 

  • Mastronardi FG, Noor A, Wood DD, Paton T, Moscarello MA (2007) Peptidyl argininedeiminase 2 CpG island in multiple sclerosis white matter is hypomethylated. J Neurosci Res 85:2006–2016

    Article  PubMed  CAS  Google Scholar 

  • Maunakea AK, Chepelev I, Zhao K (2010) Epigenome mapping in normal and disease States. Circ Res 107:327–339

    Article  PubMed  CAS  Google Scholar 

  • Messner S, Hottiger MO (2011) Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol 21:534–542

    Article  PubMed  CAS  Google Scholar 

  • Migliori V, Muller J, Phalke S, Low D, Bezzi M, Mok WC, Sahu SK, Gunaratne J, Capasso P, Bassi C et al (2012) Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat Struct Mol Biol 19:136–144

    Article  PubMed  CAS  Google Scholar 

  • Moscarello MA, Wood DD, Ackerley C, Boulias C (1994) Myelin in multiple sclerosis is developmentally immature. J Clin Invest 94:146–154

    Article  PubMed  CAS  Google Scholar 

  • Moscarello MA, Mastronardi FG, Wood DD (2007) The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res 32:251–256

    Article  PubMed  CAS  Google Scholar 

  • Musse AA, Li Z, Ackerley CA, Bienzle D, Lei H, Poma R, Harauz G, Moscarello MA, Mastronardi FG (2008) Peptidylarginine deiminase 2 (PAD2) overexpression in transgenic mice leads to myelin loss in the central nervous system. Dis Model Mech 1:229–240

    Article  PubMed  CAS  Google Scholar 

  • Neault M, Mallette FA, Vogel G, Michaud-Levesque J, Richard S (2012) Ablation of PRMT6 reveals a role as a negative transcriptional regulator of the p53 tumor suppressor. Nucleic Acids Res 40:9513–9521

    Article  PubMed  CAS  Google Scholar 

  • Nicholas AP, Sambandam T, Echols JD, Barnum SR (2005) Expression of citrullinated proteins in murine experimental autoimmune encephalomyelitis. J Comp Neurol 486:254–266

    Article  PubMed  CAS  Google Scholar 

  • Raijmakers R, Zendman AJ, Egberts WV, Vossenaar ER, Raats J, Soede-Huijbregts C, Rutjes FP, van Veelen PA, Drijfhout JW, Pruijn GJ (2007) Methylation of arginine residues interferes with citrullination by peptidylarginine deiminases in vitro. J Mol Biol 367:1118–1129

    Article  PubMed  CAS  Google Scholar 

  • Rajakumara E, Wang Z, Ma H, Hu L, Chen H, Lin Y, Guo R, Wu F, Li H, Lan F et al (2011) PHD finger recognition of unmodified histone H3R2 links UHRF1 to regulation of euchromatic gene expression. Mol Cell 43:275–284

    Article  PubMed  CAS  Google Scholar 

  • Rando OJ (2012) Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr Opin Genet Dev 22:148–155

    Article  PubMed  CAS  Google Scholar 

  • Shanshiashvili LV, Kalandadze IV, Ramsden JJ, Mikeladze DG (2012) Adhesive properties and inflammatory potential of citrullinated myelin basic protein Peptide 45–89. Neurochem Res 37:1959–1966

    Article  PubMed  CAS  Google Scholar 

  • Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR et al (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96–99

    Article  PubMed  CAS  Google Scholar 

  • Slack JL, Causey CP, Thompson PR (2011) Protein arginine deiminase 4: a target for an epigenetic cancer therapy. Cell Mol Life Sci 68:709–720

    Article  PubMed  CAS  Google Scholar 

  • Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

    Article  PubMed  CAS  Google Scholar 

  • Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, Suzuki M, Nagasaki M, Nakayama-Hamada M, Kawaida R, Ono M et al (2003) Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet 34:395–402

    Article  PubMed  CAS  Google Scholar 

  • Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, Buchou T, Cheng Z, Rousseaux S, Rajagopal N et al (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1016–1028

    Article  PubMed  CAS  Google Scholar 

  • Tanikawa C, Ueda K, Nakagawa H, Yoshida N, Nakamura Y, Matsuda K (2009) Regulation of protein Citrullination through p53/PADI4 network in DNA damage response. Cancer Res 69:8761–8769

    Article  PubMed  CAS  Google Scholar 

  • Tanikawa C, Espinosa M, Suzuki A, Masuda K, Yamamoto K, Tsuchiya E, Ueda K, Daigo Y, Nakamura Y, Matsuda K (2012) Regulation of histone modification and chromatin structure by the p53-PADI4 pathway. Nat Commun 3:676

    Article  PubMed  Google Scholar 

  • Thompson PR, Fast W (2006) Histone citrullination by protein arginine deiminase: is arginine methylation a green light or a roadblock? ACS Chem Biol 1:433–441

    Article  PubMed  CAS  Google Scholar 

  • Unoki M, Brunet J, Mousli M (2009) Drug discovery targeting epigenetic codes: the great potential of UHRF1, which links DNA methylation and histone modifications, as a drug target in cancers and toxoplasmosis. Biochem Pharmacol 78:1279–1288

    Article  PubMed  CAS  Google Scholar 

  • Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ (2003) PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 25:1106–1118

    Article  PubMed  CAS  Google Scholar 

  • Waddington CH (1942) The epigenotype. Int J Epidemiol 41:10–13

    Article  Google Scholar 

  • Wang Y, Wysocka J, Sayegh J, Lee YH, Perlin JR, Leonelli L, Sonbuchner LS, McDonald CH, Cook RG, Dou Y et al (2004) Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306:279–283

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ et al (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897–903

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA et al (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184:205–213

    Article  PubMed  CAS  Google Scholar 

  • Williams K, Christensen J, Helin K (2012) DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 13:28–35

    Article  CAS  Google Scholar 

  • Wu J, Xu W (2012) Histone H3R17me2a mark recruits human RNA polymerase-associated factor 1 complex to activate transcription. Proc Natl Acad Sci U S A 109:5675–5680

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Zhang Y (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25:2436–2452

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–448

    Article  PubMed  CAS  Google Scholar 

  • Yamada R, Suzuki A, Chang X, Yamamoto K (2005) Citrullinated proteins in rheumatoid arthritis. Front Biosci 10:54–64

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Lu Y, Espejo A, Wu J, Xu W, Liang S, Bedford MT (2010) TDRD3 is an effector molecule for arginine-methylated histone marks. Mol Cell 40:1016–1023

    Article  PubMed  CAS  Google Scholar 

  • York B, O'Malley BW (2010) Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem 285:38743–38750

    Article  PubMed  CAS  Google Scholar 

  • Yun M, Wu J, Workman JL, Li B (2011) Readers of histone modifications. Cell Res 21:564–578

    Article  PubMed  CAS  Google Scholar 

  • Yurttas P, Vitale AM, Fitzhenry RJ, Cohen-Gould L, Wu W, Gossen JA, Coonrod SA (2008) Role for PADI6 and the cytoplasmic lattices in ribosomal storage in oocytes and translational control in the early mouse embryo. Development 135:2627–2636

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Gamble MJ, Stadler S, Cherrington BD, Causey CP, Thompson PR, Roberson MS, Kraus WL, Coonrod SA (2011) Genome-wide analysis reveals PADI4 cooperates with Elk-1 to activate c-Fos expression in breast cancer cells. PLoS Genet 7:e1002112

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Bolt M, Guertin MJ, Chen W, Zhang S, Cherrington BD, Slade DJ, Dreyton CJ, Subramanian V, Bicker KL et al (2012) Peptidylarginine deiminase 2-catalyzed histone H3 arginine 26 citrullination facilitates estrogen receptor alpha target gene activation. Proc Natl Acad Sci U S A 109:13331–13336

    Article  PubMed  CAS  Google Scholar 

  • Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, Cerruti L, Curtis DJ, Patel DJ, Allis CD et al (2009) PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 16:304–311

    Article  PubMed  CAS  Google Scholar 

  • Zhou SR, Whitaker JN, Wood DD, Moscarello MA (1993) Immunological analysis of the amino terminal and the C8 isomer of human myelin basic protein. J Neuroimmunol 46:91–96

    Article  PubMed  CAS  Google Scholar 

  • Zhou SR, Moscarello MA, Whitaker JN (1995) The effects of citrullination or variable amino-terminus acylation on the encephalitogenicity of human myelin basic protein in the PL/J mouse. J Neuroimmunol 62:147–152

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Center of Excellence on Myelin Disorders, Friedman Brain Institute and Graduate School of Biological Sciences, Mount Sinai School of Medicine, New York, NY, 10029, USA

    Jialiang Liang

  2. Departments of Neuroscience, Genetics and Genomic Sciences, Center of Excellence on Myelin Disorders, Friedman Brain Institute and Graduate School of Biological Sciences, Mount Sinai School of Medicine, New York, NY, 10029, USA

    Patrizia Casaccia

Authors
  1. Jialiang Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrizia Casaccia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrizia Casaccia .

Editor information

Editors and Affiliations

  1. Department of Neurology, University of Alabama at Birmingham and The Birmingham Veterans Administration Medical Center, Birmingham, Alabama, USA

    Anthony P. Nicholas

  2. Bascom Palmer Eye Institute, University of Miami, MIAMI, Florida, USA

    Sanjoy K. Bhattacharya

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Liang, J., Casaccia, P. (2014). The Role of Protein Deimination in Epigenetics. In: Nicholas, A., Bhattacharya, S. (eds) Protein Deimination in Human Health and Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8317-5_18

Download citation

Publish with us

Policies and ethics

Search

Navigation