Macrodomain-containing Proteins: Regulating New Intracellular Functions of Mono(ADP-ribosyl)ation

Overview

Journal Nat Rev Mol Cell Biol

Specialties Cell Biology
Molecular Biology

Date 2013 Jun 6

PMID 23736681

Citations 89

Authors

Karla L H Feijs

Alexandra H Forst

Patricia Verheugd

Bernhard Luscher

Affiliations

Soon will be listed here.

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.

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References

Chaurushiya M, Weitzman M . Viral manipulation of DNA repair and cell cycle checkpoints. DNA Repair (Amst). 2009; 8(9):1166-76. PMC: 2725192. DOI: 10.1016/j.dnarep.2009.04.016. View

Brockschmidt A, Chung B, Weber S, Fischer D, Kolatsi-Joannou M, Christ L . CHD1L: a new candidate gene for congenital anomalies of the kidneys and urinary tract (CAKUT). Nephrol Dial Transplant. 2011; 27(6):2355-64. DOI: 10.1093/ndt/gfr649. View

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. 2012; 7(6):e37352. PMC: 3372510. DOI: 10.1371/journal.pone.0037352. View

Karlberg T, Thorsell A, Kallas A, Schuler H . Crystal structure of human ADP-ribose transferase ARTD15/PARP16 reveals a novel putative regulatory domain. J Biol Chem. 2012; 287(29):24077-81. PMC: 3397834. DOI: 10.1074/jbc.M112.379289. View

Tong L, Denu J . Function and metabolism of sirtuin metabolite O-acetyl-ADP-ribose. Biochim Biophys Acta. 2010; 1804(8):1617-25. PMC: 3310390. DOI: 10.1016/j.bbapap.2010.02.007. View

Moss J, Oppenheimer N, West Jr R, Stanley S . Amino acid specific ADP-ribosylation: substrate specificity of an ADP-ribosylarginine hydrolase from turkey erythrocytes. Biochemistry. 1986; 25(19):5408-14. DOI: 10.1021/bi00367a010. View

Holbourn K, Shone C, Acharya K . A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J. 2006; 273(20):4579-93. DOI: 10.1111/j.1742-4658.2006.05442.x. View

Egloff M, Malet H, Putics A, Heinonen M, Dutartre H, Frangeul A . Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J Virol. 2006; 80(17):8493-502. PMC: 1563857. DOI: 10.1128/JVI.00713-06. View

Williams J, Butler I, Rosenberg H, Verani R, Scott C, Conley S . Progressive neurologic deterioration and renal failure due to storage of glutamyl ribose-5-phosphate. N Engl J Med. 1984; 311(3):152-5. DOI: 10.1056/NEJM198407193110305. View

10.

Zaja R, Mikoc A, Barkauskaite E, Ahel I . Molecular Insights into Poly(ADP-ribose) Recognition and Processing. Biomolecules. 2014; 3(1):1-17. PMC: 4030884. DOI: 10.3390/biom3010001. View

11.

Jankevicius G, Hassler M, Golia B, Rybin V, Zacharias M, Timinszky G . A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat Struct Mol Biol. 2013; 20(4):508-14. PMC: 7097781. DOI: 10.1038/nsmb.2523. View

12.

Gibson B, Kraus W . New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol. 2012; 13(7):411-24. DOI: 10.1038/nrm3376. View

13.

Verheugd P, Forst A, Milke L, Herzog N, Feijs K, Kremmer E . Regulation of NF-κB signalling by the mono-ADP-ribosyltransferase ARTD10. Nat Commun. 2013; 4:1683. DOI: 10.1038/ncomms2672. View

14.

Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P . PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res. 2010; 38(19):6350-62. PMC: 2965223. DOI: 10.1093/nar/gkq463. View

15.

Schreiber V, Dantzer F, Ame J, de Murcia G . Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006; 7(7):517-28. DOI: 10.1038/nrm1963. View

16.

Dunstan M, Barkauskaite E, Lafite P, Knezevic C, Brassington A, Ahel M . Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nat Commun. 2012; 3:878. DOI: 10.1038/ncomms1889. View

17.

Peterson F, Chen D, Lytle B, Rossi M, Ahel I, Denu J . Orphan macrodomain protein (human C6orf130) is an O-acyl-ADP-ribose deacylase: solution structure and catalytic properties. J Biol Chem. 2011; 286(41):35955-35965. PMC: 3195580. DOI: 10.1074/jbc.M111.276238. View

18.

Jwa M, Chang P . PARP16 is a tail-anchored endoplasmic reticulum protein required for the PERK- and IRE1α-mediated unfolded protein response. Nat Cell Biol. 2012; 14(11):1223-30. PMC: 3494284. DOI: 10.1038/ncb2593. View

19.

Tucker J, Bennett N, Brassington C, Durant S, Hassall G, Holdgate G . Structures of the human poly (ADP-ribose) glycohydrolase catalytic domain confirm catalytic mechanism and explain inhibition by ADP-HPD derivatives. PLoS One. 2012; 7(12):e50889. PMC: 3519477. DOI: 10.1371/journal.pone.0050889. View

20.

Yang J, Aittomaki S, Pesu M, Carter K, Saarinen J, Kalkkinen N . Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. EMBO J. 2002; 21(18):4950-8. PMC: 126276. DOI: 10.1093/emboj/cdf463. View