Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation

Nature Reviews Molecular Cell Biology volume 14, pages 443–451 (2013)Cite this article

Subjects

A Corrigendum to this article was published on 28 June 2013

This article has been updated

Abstract

ADP-ribosylation of proteins was first described in the early 1960's, and today the function and regulation of poly(ADP-ribosyl)ation (PARylation) is partially understood. By contrast, little is known about intracellular mono(ADP-ribosyl)ation (MARylation) by ADP-ribosyl transferase (ART) enzymes, such as ARTD10. Recent findings indicate that MARylation regulates signalling and transcription by modifying key components in these processes. Emerging evidence also suggests that specific macrodomain-containing proteins, including ARTD8, macroD1, macroD2 and C6orf130, which are distinct from those affecting PARylation, interact with MARylation on target proteins to 'read' and 'erase' this modification. Thus, studying macrodomain-containing proteins is key to understanding the function and regulation of MARylation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Emerging functions of MARylation.
Figure 2: Emerging functions of macrodomains as readers and erasers of MARylation.

Similar content being viewed by others

Accession codes

Accessions

Protein Data Bank

Change history

  • 28 June 2013

    On page 443 of this article, the incorrect references were cited at the end of the following sentence: "Four years ago, macrodomains were shown to be able to bind PAR that has been synthesized in response to DNA damage18,19,20." The authors meant to refer to references 20, 25 and 26 at the end of this sentence. This has been corrected online. The authors apologize to the authors of references 25 and 26 for this mistake and for any confusion caused to readers.

References

  1. Holbourn, K. P., Shone, C. C. & Acharya, K. R. A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J. 273, 4579–4593 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Corda, D. & Di Girolamo, M. Functional aspects of protein mono-ADP-ribosylation. EMBO J. 22, 1953–1958 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Yates, S. P., Jorgensen, R., Andersen, G. R. & Merrill, A. R. Stealth and mimicry by deadly bacterial toxins. Trends Biochem. Sci. 31, 123–133 (2006).

    Article  CAS  PubMed  Google Scholar 

  4. Otto, H. et al. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6, 139 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hottiger, M. O., Hassa, P. O., Luscher, B., Schuler, H. & Koch-Nolte, F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35, 208–219 (2010).

    Article  CAS  PubMed  Google Scholar 

  6. Schreiber, V., Dantzer, F., Ame, J. C. & de Murcia, G. Poly(ADP-ribose): novel functions for an old molecule. Nature Rev. Mol. Cell Biol. 7, 517–528 (2006).

    Article  CAS  Google Scholar 

  7. Gibson, B. A. & Kraus, W. L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nature Rev. Mol. Cell Biol. 13, 411–424 (2012).

    Article  CAS  Google Scholar 

  8. Kleine, H. et al. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol. Cell 32, 57–69 (2008).

    Article  CAS  PubMed  Google Scholar 

  9. Altmeyer, M., Messner, S., Hassa, P. O., Fey, M. & Hottiger, M. O. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res. 37, 3723–3738 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Haenni, S. S. et al. Identification of lysines 36 and 37 of PARP-2 as targets for acetylation and auto-ADP-ribosylation. Int. J. Biochem. Cell Biol. 40, 2274–2283 (2008).

    Article  CAS  PubMed  Google Scholar 

  11. Messner, S. et al. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res. 38, 6350–6362 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chapman, J. D., Gagne, J. P., Poirier, G. G. & Goodlett, D. R. Mapping PARP-1 auto-ADP-ribosylation sites by liquid chromatography-tandem mass spectrometry. J. Proteome Res. 12, 1868–1880 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. Sharifi, R. et al. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J. 32, 1225–1237 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tao, Z., Gao, P. & Liu, H. W. Identification of the ADP-ribosylation sites in the PARP-1 automodification domain: analysis and implications. J. Am. Chem. Soc. 131, 14258–14260 (2009).

    Article  CAS  PubMed  Google Scholar 

  15. Kalisch, T., Ame, J. C., Dantzer, F. & Schreiber, V. New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci. 37, 381–390 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zaja, R., Mikoc, A., Barkauskaite, E. & Ahel, I. Molecular insights into poly(ADP-ribose) recognition and processing. Biomolecules 3, 1–17 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Pehrson, J. R. & Fried, V. A. MacroH2A, a core histone containing a large nonhistone region. Science 257, 1398–1400 (1992).

    Article  CAS  PubMed  Google Scholar 

  18. Li, G. Y. et al. Structure and identification of ADP-ribose recognition motifs of APLF and role in the DNA damage response. Proc. Natl Acad. Sci. USA 107, 9129–9134 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ahel, I. et al. Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451, 81–85 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Ahel, D. et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325, 1240–1243 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Slade, D. et al. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477, 616–620 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kim, I. K. et al. Structure of mammalian poly(ADP-ribose) glycohydrolase reveals a flexible tyrosine clasp as a substrate-binding element. Nature Struct. Mol. Biol. 19, 653–656 (2012).

    Article  CAS  Google Scholar 

  23. Dunstan, M. S. et al. Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nature Commun. 3, 878 (2012).

    Article  CAS  Google Scholar 

  24. Satoh, M. S. & Lindahl, T. Role of poly(ADP-ribose) formation in DNA repair. Nature 356, 356–358 (1992).

    Article  CAS  PubMed  Google Scholar 

  25. Gottschalk, A. J. et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl Acad. Sci. USA 106, 13770–13774 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Timinszky, G. et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nature Struct. Mol. Biol. 16, 923–929 (2009).

    Article  CAS  Google Scholar 

  27. Kleine, H. & Luscher, B. Learning how to read ADP-ribosylation. Cell 139, 17–19 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Huambachano, O., Herrera, F., Rancourt, A. & Satoh, M. S. Double-stranded DNA binding domain of poly(ADP-ribose) polymerase-1 and molecular insight into the regulation of its activity. J. Biol. Chem. 286, 7149–7160 (2011).

    Article  CAS  PubMed  Google Scholar 

  29. Hsiao, S. J. & Smith, S. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie 90, 83–92 (2008).

    Article  CAS  PubMed  Google Scholar 

  30. Aravind, L. The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem. Sci. 26, 273–275 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. Callow, M. G. et al. Ubiquitin ligase RNF146 regulates tankyrase and Axin to promote Wnt signaling. PLoS ONE 6, e22595 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zhang, Y. et al. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nature Cell Biol. 13, 623–629 (2011).

    Article  CAS  PubMed  Google Scholar 

  33. MacDonald, B. T., Tamai, K. & He, X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9–26 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Pleschke, J. M., Kleczkowska, H. E., Strohm, M. & Althaus, F. R. Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem. 275, 40974–40980 (2000).

    Article  CAS  PubMed  Google Scholar 

  35. Gagne, J. P. et al. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 36, 6959–6976 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Krietsch, J. et al. Reprogramming cellular events by poly(ADP-ribose)-binding proteins. Mol. Aspects Med. 23 Dec 2012 (10.1016/j.mam.2012.12.005).

  37. Tucker, J. A. et al. Structures of the human poly (ADP-ribose) glycohydrolase catalytic domain confirm catalytic mechanism and explain inhibition by ADP-HPD derivatives. PLoS ONE 7, e50889 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Oka, S., Kato, J. & Moss, J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J. Biol. Chem. 281, 705–713 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Mueller-Dieckmann, C. et al. The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. Proc. Natl Acad. Sci. USA 103, 15026–15031 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rosenthal, F. et al. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nature Struct. Mol. Biol. 20, 502–507 (2013).

    Article  CAS  Google Scholar 

  41. Hottiger, M. O. et al. Progress in the function and regulation of ADP-ribosylation. Sci. Signal. 4, mr5 (2011).

    Article  CAS  PubMed  Google Scholar 

  42. Yu, M. et al. PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 24, 1982–1993 (2005).

    Article  CAS  PubMed  Google Scholar 

  43. Kleine, H. et al. Dynamic subcellular localization of the mono-ADP-ribosyltransferase ARTD10 and interaction with the ubiquitin receptor p62. Cell Commun. Signal. 10, 28 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Verheugd, P. et al. Regulation of NF-κB signaling by the mono-ADP-ribosyltransferase ARTD10. Nature Commun. 4, 1683 (2013).

    Article  CAS  Google Scholar 

  45. Chen, Z. J. Ubiquitination in signaling to and activation of IKK. Immunol. Rev. 246, 95–106 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Herzog, N. et al. Caspase-dependent cleavage of the mono-ADP-ribosyltransferase ARTD10 interferes with its pro-apoptotic function. FEBS J. 280, 13 (2013).

    Article  CAS  Google Scholar 

  47. Feijs, K. L. et al. ARTD10 substrate identification on protein microarrays: regulation of GSK3β by mono-ADP-ribosylation. Cell Commun. Signal. 11, 5 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wu, D. & Pan, W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 35, 161–168 (2010).

    Article  CAS  PubMed  Google Scholar 

  49. Goenka, S. & Boothby, M. Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc. Natl Acad. Sci. USA 103, 4210–4215 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mehrotra, P. et al. PARP-14 functions as a transcriptional switch for Stat6-dependent gene activation. J. Biol. Chem. 286, 1767–1776 (2011).

    Article  CAS  PubMed  Google Scholar 

  51. Goenka, S., Cho, S. H. & Boothby, M. Collaborator of Stat6 (CoaSt6)-associated poly(ADP-ribose) polymerase activity modulates Stat6-dependent gene transcription. J. Biol. Chem. 282, 18732–18739 (2007).

    Article  CAS  PubMed  Google Scholar 

  52. Yang, J. et al. Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. EMBO J. 21, 4950–4958 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Mehrotra, P. et al. Poly (ADP-ribose) polymerase 14 and its enzyme activity regulates TH2 differentiation and allergic airway disease. J. Allergy Clin. Immunol. 131, 521–531.e12 (2013).

    Article  CAS  PubMed  Google Scholar 

  54. Macpherson, L. et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin poly(ADP-ribose) polymerase (TiPARP, ARTD14) is a mono-ADP-ribosyltransferase and repressor of aryl hydrocarbon receptor transactivation. Nucleic Acids Res. 41, 1604–1621 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Jwa, M. & Chang, P. PARP16 is a tail-anchored endoplasmic reticulum protein required for the PERK- and IRE1α-mediated unfolded protein response. Nature Cell Biol. 14, 1223–1230 (2012).

    Article  CAS  PubMed  Google Scholar 

  56. Di Paola, S., Micaroni, M., Di Tullio, G., Buccione, R. & Di Girolamo, M. PARP16/ARTD15 is a novel endoplasmic-reticulum-associated mono-ADP-ribosyltransferase that interacts with, and modifies karyopherin-ss1. PLoS ONE 7, e37352 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hetz, C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nature Rev. Mol. Cell Biol. 13, 89–102 (2012).

    Article  CAS  Google Scholar 

  58. Karlberg, T., Thorsell, A. G., Kallas, A. & Schuler, H. Crystal structure of human ADP-ribose transferase ARTD15/PARP16 reveals a novel putative regulatory domain. J. Biol. Chem. 287, 24077–24081 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Anantharaman, V., Koonin, E. V. & Aravind, L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 30, 1427–1464 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Till, S. & Ladurner, A. G. Sensing NAD metabolites through macro domains. Front. Biosci. 14, 3246–3258 (2009).

    Article  CAS  Google Scholar 

  61. Han, W., Li, X. & Fu, X. The macro domain protein family: structure, functions, and their potential therapeutic implications. Mutat. Res. 727, 86–103 (2011).

    Article  CAS  PubMed  Google Scholar 

  62. Karras, G. I. et al. The macro domain is an ADP-ribose binding module. EMBO J. 24, 1911–1920 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chen, D. et al. Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J. Biol. Chem. 286, 13261–13271 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Peterson, F. C. et al. Orphan macrodomain protein (human C6orf130) is an O-acyl-ADP-ribose deacylase: solution structure and catalytic properties. J. Biol. Chem. 286, 35955–35965 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Tong, L. & Denu, J. M. Function and metabolism of sirtuin metabolite O-acetyl-ADP-ribose. Biochim. Biophys. Acta 1804, 1617–1625 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Neuvonen, M. & Ahola, T. Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J. Mol. Biol. 385, 212–225 (2009).

    Article  CAS  PubMed  Google Scholar 

  67. Egloff, M. P. et al. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J. Virol. 80, 8493–8502 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Saikatendu, K. S. et al. Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1′′-phosphate dephosphorylation by a conserved domain of nsP3. Structure 13, 1665–1675 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Shull, N. P., Spinelli, S. L. & Phizicky, E. M. A highly specific phosphatase that acts on ADP-ribose 1′′-phosphate, a metabolite of tRNA splicing in Saccharomyces cerevisiae. Nucleic Acids Res. 33, 650–660 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Putics, A., Filipowicz, W., Hall, J., Gorbalenya, A. E. & Ziebuhr, J. ADP-ribose-1”-monophosphatase: a conserved coronavirus enzyme that is dispensable for viral replication in tissue culture. J. Virol. 79, 12721–12731 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pines, A. et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 199, 235–249 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Aguiar, R. C. et al. BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. Blood 96, 4328–4334 (2000).

    CAS  PubMed  Google Scholar 

  73. Takeyama, K. et al. The BAL-binding protein BBAP and related Deltex family members exhibit ubiquitin-protein isopeptide ligase activity. J. Biol. Chem. 278, 21930–21937 (2003).

    Article  CAS  PubMed  Google Scholar 

  74. Yan, Q. et al. BAL1 and its partner E3 ligase, BBAP, link PARP activation, ubiquitylation and double-strand DNA repair independent of ATM, MDC1 and RNF8. Mol Cell. Biol. 33, 845–857 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Aguiar, R. C., Takeyama, K., He, C., Kreinbrink, K. & Shipp, M. A. B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J. Biol. Chem. 280, 33756–33765 (2005).

    Article  CAS  PubMed  Google Scholar 

  76. Jankevicius, G. et al. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nature Struct. Mol. Biol. 20, 508–514 (2013).

    Article  CAS  Google Scholar 

  77. Gagne, J. P. et al. Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 40, 7788–7805 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Dani, N. et al. Combining affinity purification by ADP-ribose-binding macro domains with mass spectrometry to define the mammalian ADP-ribosyl proteome. Proc. Natl Acad. Sci. USA 106, 4243–4248 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Forst, A. H. et al. Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains. Structure 21, 462–475 (2013).

    Article  CAS  PubMed  Google Scholar 

  80. Filippakopoulos, P. et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 149, 214–231 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Ono, T., Kasamatsu, A., Oka, S. & Moss, J. The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. Proc. Natl Acad. Sci. USA 103, 16687–16691 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Moss, J., Oppenheimer, N. J., West, R. E. Jr & Stanley, S. J. Amino acid specific ADP-ribosylation: substrate specificity of an ADP-ribosylarginine hydrolase from turkey erythrocytes. Biochemistry 25, 5408–5414 (1986).

    Article  CAS  PubMed  Google Scholar 

  83. Wang, Y. et al. Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci. Signal. 4, ra20 (2011).

    PubMed  PubMed Central  Google Scholar 

  84. Williams, J. C., Chambers, J. P. & Liehr, J. G. Glutamyl ribose 5-phosphate storage disease. A hereditary defect in the degradation of poly(ADP-ribosylated) proteins. J. Biol. Chem. 259, 1037–1042 (1984).

    CAS  PubMed  Google Scholar 

  85. Williams, J. C. et al. Progressive neurologic deterioration and renal failure due to storage of glutamyl ribose-5-phosphate. N. Engl. J. Med. 311, 152–155 (1984).

    Article  CAS  PubMed  Google Scholar 

  86. Allen, M. D., Buckle, A. M., Cordell, S. C., Lowe, J. & Bycroft, M. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330, 503–511 (2003).

    Article  CAS  PubMed  Google Scholar 

  87. Kustatscher, G., Hothorn, M., Pugieux, C., Scheffzek, K. & Ladurner, A. G. Splicing regulates NAD metabolite binding to histone macroH2A. Nature Struct. Mol. Biol. 12, 624–625 (2005).

    Article  CAS  Google Scholar 

  88. Patel, C. N., Koh, D. W., Jacobson, M. K. & Oliveira, M. A. Identification of three critical acidic residues of poly(ADP-ribose) glycohydrolase involved in catalysis: determining the PARG catalytic domain. Biochem. J. 388, 493–500 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Cho, S. H. et al. PARP-14, a member of the B aggressive lymphoma family, transduces survival signals in primary B cells. Blood 113, 2416–2425 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ma, N. F. et al. Isolation and characterization of a novel oncogene, amplified in liver cancer 1, within a commonly amplified region at 1q21 in hepatocellular carcinoma. Hepatology 47, 503–510 (2008).

    Article  CAS  PubMed  Google Scholar 

  91. Brockschmidt, A. et al. CHD1L: a new candidate gene for congenital anomalies of the kidneys and urinary tract (CAKUT). Nephrol. Dial. Transplant. 27, 2355–2364 (2012).

    Article  CAS  PubMed  Google Scholar 

  92. Kapoor, A. et al. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468, 1105–1109 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Sporn, J. C. et al. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28, 3423–3428 (2009).

    Article  CAS  PubMed  Google Scholar 

  94. Park, E. & Griffin, D. E. The nsP3 macro domain is important for Sindbis virus replication in neurons and neurovirulence in mice. Virology 388, 305–314 (2009).

    Article  CAS  PubMed  Google Scholar 

  95. Chaurushiya, M. S. & Weitzman, M. D. Viral manipulation of DNA repair and cell cycle checkpoints. DNA Repair (Amst.) 8, 1166–1176 (2009).

    Article  CAS  Google Scholar 

  96. Haince, J. F., Ouellet, M. E., McDonald, D., Hendzel, M. J. & Poirier, G. G. Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim. Biophys. Acta 1763, 226–237 (2006).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank their colleagues for insightful discussions and A. Ladurner and I. Ahel for providing manuscripts prior to publication. They apologize to researchers whose work could not be included owing to space restrictions. The work in the author's laboratory was supported by the START program of the Medical School of the Rheinisch-Westfaelische Technische Hochschule (RWTH) Aachen University and by the Deutsche Forschungsgemeinschaft DFG (LU466/15-1).

Author information

Authors and Affiliations

  1. Karla L. H. Feijs, Alexandra H. Forst, Patricia Verheugd and Bernhard Lüscher are at the Institute of Biochemistry and Molecular Biology, Rheinisch-Westfaelische Technische Hochschule (RWTH) Aachen University, Pauwelsstraße 30, 52074 Aachen, Germany.,

    Karla L. H. Feijs, Alexandra H. Forst, Patricia Verheugd & Bernhard Lüscher

Authors
  1. Karla L. H. Feijs
    View author publications

    Search author on:PubMed Google Scholar

  2. Alexandra H. Forst
    View author publications

    Search author on:PubMed Google Scholar

  3. Patricia Verheugd
    View author publications

    Search author on:PubMed Google Scholar

  4. Bernhard Lüscher
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Bernhard Lüscher.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

FURTHER INFORMATION

Bernhard Lüscher's homepage

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feijs, K., Forst, A., Verheugd, P. et al. Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nat Rev Mol Cell Biol 14, 443–451 (2013). https://doi.org/10.1038/nrm3601

Download citation

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nrm3601

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing