Advertisement

ADP-Ribosyl-Acceptor Hydrolase Activities Catalyzed by the ARH Family of Proteins

  • Masato Mashimo
  • Joel Moss
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1813)

Abstract

The ARH family of ADP-ribosyl-acceptor hydrolases is composed of three 39-kDa proteins (ARH1, 2, and 3), which hydrolyze specific ADP-ribosylated substrates. ARH1 hydrolyzes mono(ADP-ribosyl)ated arginine, which results from actions of cholera toxin and other nicotinamide adenine dinucleotide (NAD+):arginine ADP-ribosyl-transferases, while ARH3 hydrolyzes poly(ADP-ribose) and O-acetyl-ADP-ribose, resulting from the action of poly(ADP-ribose) polymerases and sirtuins, respectively. ARH2 has not been reported to have enzymatic activity, because of differences in the catalytic domain. Thus, the substrate specificities of ARH1 and ARH3 proteins result in unique cellular functions. In this chapter, we introduce several methods to monitor the activities of the ARH family members.

Key words

ADP-ribosylation ADP-ribosyl-acceptor hydrolase (ARH) ADP-ribosylated arginine Poly(ADP-ribose) polymerase (PARP) 1 O-acetyl-ADP-ribose (OAADPr) Cholera toxin 

Notes

Acknowledgment

Funding: The study was funded by the Intramural Research Program, NIH, NHLBI.

References

  1. 1.
    Verheugd P, Butepage M, Eckei L, Luscher B (2016) Players in ADP-ribosylation: readers and erasers. Curr Protein Pept Sci 17(7):654–667CrossRefPubMedGoogle Scholar
  2. 2.
    Palazzo L, Mikoc A, Ahel I (2017) ADP-ribosylation: new facets of an ancient modification. FEBS J 284:2932. https://doi.org/10.1111/febs.14078 CrossRefPubMedGoogle Scholar
  3. 3.
    Okazaki IJ, Moss J (1996) Mono-ADP-ribosylation: a reversible posttranslational modification of proteins. Adv Pharmacol 35:247–280CrossRefPubMedGoogle Scholar
  4. 4.
    Corda D, Di Girolamo M (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J 22(9):1953–1958. https://doi.org/10.1093/emboj/cdg209 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bütepage M, Eckei L, Verheugd P, Luscher B (2015) Intracellular mono-ADP-ribosylation in signaling and disease. Cell 4(4):569–595. https://doi.org/10.3390/cells4040569 CrossRefGoogle Scholar
  6. 6.
    Ogata N, Ueda K, Kagamiyama H, Hayaishi O (1980) ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. J Biol Chem 255(16):7616–7620PubMedGoogle Scholar
  7. 7.
    Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO (2009) Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 37(11):3723–3738. https://doi.org/10.1093/nar/gkp229 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Zhang Y, Wang J, Ding M, Yu Y (2013) Site-specific characterization of the Asp- and Glu-ADP-ribosylated proteome. Nat Methods 10(10):981–984. https://doi.org/10.1038/nmeth.2603 CrossRefPubMedGoogle Scholar
  9. 9.
    Leidecker O, Bonfiglio JJ, Colby T, Zhang Q, Atanassov I, Zaja R, Palazzo L, Stockum A, Ahel I, Matic I (2016) Serine is a new target residue for endogenous ADP-ribosylation on histones. Nat Chem Biol 12(12):998–1000. https://doi.org/10.1038/nchembio.2180 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Iglewski BH, Kabat D (1975) NAD-dependent inhibition of protein synthesis by Pseudomonas aeruginosa toxin. Proc Natl Acad Sci U S A 72(6):2284–2288CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Pappenheimer AM Jr (1977) Diphtheria toxin. Annu Rev Biochem 46:69–94. https://doi.org/10.1146/annurev.bi.46.070177.000441 CrossRefPubMedGoogle Scholar
  12. 12.
    Cassel D, Pfeuffer T (1978) Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc Natl Acad Sci U S A 75(6):2669–2673CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Tamura M, Nogimori K, Murai S, Yajima M, Ito K, Katada T, Ui M, Ishii S (1982) Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 21(22):5516–5522CrossRefPubMedGoogle Scholar
  14. 14.
    Vyas S, Chesarone-Cataldo M, Todorova T, Huang YH, Chang P (2013) A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat Commun 4:2240. https://doi.org/10.1038/ncomms3240 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bock FJ, Chang P (2016) New directions in poly(ADP-ribose) polymerase biology. FEBS J 283(22):4017–4031. https://doi.org/10.1111/febs.13737 CrossRefPubMedGoogle Scholar
  16. 16.
    Gupte R, Liu Z, Kraus WL (2017) PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes. Genes Dev 31(2):101–126. https://doi.org/10.1101/gad.291518.116 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Borra MT, O'Neill FJ, Jackson MD, Marshall B, Verdin E, Foltz KR, Denu JM (2002) Conserved enzymatic production and biological effect of O-acetyl-ADP-ribose by silent information regulator 2-like NAD+-dependent deacetylases. J Biol Chem 277(15):12632–12641. https://doi.org/10.1074/jbc.M111830200 CrossRefPubMedGoogle Scholar
  18. 18.
    Liou GG, Tanny JC, Kruger RG, Walz T, Moazed D (2005) Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation. Cell 121(4):515–527. https://doi.org/10.1016/j.cell.2005.03.035 CrossRefPubMedGoogle Scholar
  19. 19.
    Grubisha O, Rafty LA, Takanishi CL, Xu X, Tong L, Perraud AL, Scharenberg AM, Denu JM (2006) Metabolite of SIR2 reaction modulates TRPM2 ion channel. J Biol Chem 281(20):14057–14065. https://doi.org/10.1074/jbc.M513741200 CrossRefPubMedGoogle Scholar
  20. 20.
    Moss J, Jacobson MK, Stanley SJ (1985) Reversibility of arginine-specific mono(ADP-ribosyl)ation: identification in erythrocytes of an ADP-ribose-L-arginine cleavage enzyme. Proc Natl Acad Sci U S A 82(17):5603–5607CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Oka S, Kato J, Moss J (2006) Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem 281(2):705–713. https://doi.org/10.1074/jbc.M510290200 CrossRefPubMedGoogle Scholar
  22. 22.
    Mashimo M, Kato J, Moss J (2014) Structure and function of the ARH family of ADP-ribosyl-acceptor hydrolases. DNA Repair (Amst) 23:88–94. https://doi.org/10.1016/j.dnarep.2014.03.005 CrossRefGoogle Scholar
  23. 23.
    Konczalik P, Moss J (1999) Identification of critical, conserved vicinal aspartate residues in mammalian and bacterial ADP-ribosylarginine hydrolases. J Biol Chem 274(24):16736–16740CrossRefPubMedGoogle Scholar
  24. 24.
    Ono T, Kasamatsu A, Oka S, Moss J (2006) 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 U S A 103(45):16687–16691. https://doi.org/10.1073/pnas.0607911103 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Moss J, Tsai SC, Adamik R, Chen HC, Stanley SJ (1988) Purification and characterization of ADP-ribosylarginine hydrolase from Turkey erythrocytes. Biochemistry 27(15):5819–5823CrossRefPubMedGoogle Scholar
  26. 26.
    Moss J, Balducci E, Cavanaugh E, Kim HJ, Konczalik P, Lesma EA, Okazaki IJ, Park M, Shoemaker M, Stevens LA, Zolkiewska A (1999) Characterization of NAD:arginine ADP-ribosyltransferases. Mol Cell Biochem 193(1–2):109–113CrossRefPubMedGoogle Scholar
  27. 27.
    Freissmuth M, Gilman AG (1989) Mutations of GS alpha designed to alter the reactivity of the protein with bacterial toxins. Substitutions at ARG187 result in loss of GTPase activity. J Biol Chem 264(36):21907–21914PubMedGoogle Scholar
  28. 28.
    Gill DM, Meren R (1978) ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase. Proc Natl Acad Sci U S A 75(7):3050–3054CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kahn RA, Gilman AG (1984) Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. J Biol Chem 259(10):6228–6234PubMedGoogle Scholar
  30. 30.
    Kahn RA, Gilman AG (1986) The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem 261(17):7906–7911PubMedGoogle Scholar
  31. 31.
    Kato J, Zhu J, Liu C, Moss J (2007) Enhanced sensitivity to cholera toxin in ADP-ribosylarginine hydrolase-deficient mice. Mol Cell Biol 27(15):5534–5543. https://doi.org/10.1128/MCB.00302-07 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kato J, Zhu J, Liu C, Stylianou M, Hoffmann V, Lizak MJ, Glasgow CG, Moss J (2011) ADP-ribosylarginine hydrolase regulates cell proliferation and tumorigenesis. Cancer Res 71(15):5327–5335. https://doi.org/10.1158/0008-5472.CAN-10-0733 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kato J, Vekhter D, Heath J, Zhu J, Barbieri JT, Moss J (2015) Mutations of the functional ARH1 allele in tumors from ARH1 heterozygous mice and cells affect ARH1 catalytic activity, cell proliferation and tumorigenesis. Oncogene 4:e151. https://doi.org/10.1038/oncsis.2015.5 CrossRefGoogle Scholar
  34. 34.
    Kasamatsu A, Nakao M, Smith BC, Comstock LR, Ono T, Kato J, Denu JM, Moss J (2011) Hydrolysis of O-acetyl-ADP-ribose isomers by ADP-ribosylhydrolase 3. J Biol Chem 286(24):21110–21117. https://doi.org/10.1074/jbc.M111.237636 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Mashimo M, Kato J, Moss J (2013) ADP-ribosyl-acceptor hydrolase 3 regulates poly (ADP-ribose) degradation and cell death during oxidative stress. Proc Natl Acad Sci U S A 110(47):18964–18969. https://doi.org/10.1073/pnas.1312783110 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Fontana P, Bonfiglio JJ, Palazzo L, Bartlett E, Matic I, Ahel I (2017) Serine ADP-ribosylation reversal by the hydrolase ARH3. elife 6. https://doi.org/10.7554/eLife.28533
  37. 37.
    Mashimo M, Moss J (2016) Functional role of ADP-Ribosyl-acceptor hydrolase 3 in poly(ADP-ribose) polymerase-1 response to oxidative stress. Curr Protein Pept Sci 17(7):633–640CrossRefPubMedGoogle Scholar
  38. 38.
    Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297(5579):259–263. https://doi.org/10.1126/science.1072221 CrossRefPubMedGoogle Scholar
  39. 39.
    Andrabi SA, Kang HC, Haince JF, Lee YI, Zhang J, Chi Z, West AB, Koehler RC, Poirier GG, Dawson TM, Dawson VL (2011) Iduna protects the brain from glutamate excitotoxicity and stroke by interfering with poly(ADP-ribose) polymer-induced cell death. Nat Med 17(6):692–699. https://doi.org/10.1038/nm.2387 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Lee Y, Karuppagounder SS, Shin JH, Lee YI, Ko HS, Swing D, Jiang H, Kang SU, Lee BD, Kang HC, Kim D, Tessarollo L, Dawson VL, Dawson TM (2013) Parthanatos mediates AIMP2-activated age-dependent dopaminergic neuronal loss. Nat Neurosci 16(10):1392–1400. https://doi.org/10.1038/nn.3500 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Wang Y, An R, Umanah GK, Park H, Nambiar K, Eacker SM, Kim B, Bao L, Harraz MM, Chang C, Chen R, Wang JE, Kam TI, Jeong JS, Xie Z, Neifert S, Qian J, Andrabi SA, Blackshaw S, Zhu H, Song H, Ming GL, Dawson VL, Dawson TM (2016) A nuclease that mediates cell death induced by DNA damage and poly(ADP-ribose) polymerase-1. Science 354(6308):aad6872. https://doi.org/10.1126/science.aad6872 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Andrabi SA, Umanah GK, Chang C, Stevens DA, Karuppagounder SS, Gagne JP, Poirier GG, Dawson VL, Dawson TM (2014) Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc Natl Acad Sci U S A 111(28):10209–10214. https://doi.org/10.1073/pnas.1405158111 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Niere M, Mashimo M, Agledal L, Dolle C, Kasamatsu A, Kato J, Moss J, Ziegler M (2012) ADP-ribosylhydrolase 3 (ARH3), not poly(ADP-ribose) glycohydrolase (PARG) isoforms, is responsible for degradation of mitochondrial matrix-associated poly(ADP-ribose). J Biol Chem 287(20):16088–16102. https://doi.org/10.1074/jbc.M112.349183 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Parihar P, Solanki I, Mansuri ML, Parihar MS (2015) Mitochondrial sirtuins: emerging roles in metabolic regulations, energy homeostasis and diseases. Exp Gerontol 61:130–141. https://doi.org/10.1016/j.exger.2014.12.004 CrossRefPubMedGoogle Scholar
  45. 45.
    Osborne B, Bentley NL, Montgomery MK, Turner N (2016) The role of mitochondrial sirtuins in health and disease. Free Radic Biol Med 100:164–174. https://doi.org/10.1016/j.freeradbiomed.2016.04.197 CrossRefPubMedGoogle Scholar
  46. 46.
    Alvarez-Gonzalez R, Juarez-Salinas H, Jacobson EL, Jacobson MK (1983) Evaluation of immobilized boronates for studies of adenine and pyridine nucleotide metabolism. Anal Biochem 135(1):69–77CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Pharmaceutical Sciences, Department of PharmacologyDoshisha Women’s College of Liberal ArtsKyotanabeJapan
  2. 2.Pulmonary Branch, National Heart, Lung, and Blood InstituteNational Institutes of HealthBethesdaUSA

Personalised recommendations