Detection of ADP-Ribosylation of the Androgen Receptor Using the Recombinant Macrodomain AF1521 from Archaeoglobus Fulgidus

Overview

Journal Methods Mol Biol

Specialty Molecular Biology

Date 2019 May 2

PMID 31041742

Citations 7

Authors

Teddy Kamata

Chun-Song Yang

Kasey Jividen

Adam Spencer

Natalia Dworak

Luke T Oostdyk

Bryce M Paschal

Affiliations

Soon will be listed here.

Abstract

ADP-ribosylation is a posttranslational modification generated by members of the superfamily of ADP-ribosyltransferases, known as the Parp enzymes. Depending on the superfamily member, Parp enzymes can mono- or poly-ADP-ribosylate a protein substrate. Parp superfamily members confer regulation to a variety of biological processes that include cell signaling, DNA repair, transcription, and stress responses. Here, we describe biochemical methods for detection of ADP-ribose conjugated to the androgen receptor (AR) using the archaeal macrodomain, AF1521, from Archaeoglobus fulgidus. The utility of AF1521 is based on its highly selective recognition of ADP-ribose conjugated to protein. AF1521 immobilized on beads can be used to enrich for ADP-ribosylated proteins, which in our application results in recovery of ADP-ribosylated AR from prostate cancer cell extracts. We engineered tandem AF1521 macrodomains and found this improves the recovery of ADP-ribosylated AR under native conditions, and it enabled development of an assay for detection of ADP-ribosylation on blots. Thus, AF1521 can be used to query ADP-ribosylation of protein under both native and denaturing conditions. Our assays should prove useful for understanding how ADP-ribosylation regulates AR function.

Citing Articles

Oligomerization mediated by the D2 domain of DTX3L is critical for DTX3L-PARP9 reading function of mono-ADP-ribosylated androgen receptor.

Vela-Rodriguez C, Yang C, Alanen H, Eki R, Abbas T, Maksimainen M Protein Sci. 2024; 33(4):e4945.

PMID: 38511494 PMC: 10955461. DOI: 10.1002/pro.4945.

Oligomerisation mediated by the D2 domain of DTX3L is critical for DTX3L-PARP9 reading function of mono-ADP-ribosylated androgen receptor.

Vela-Rodriguez C, Yang C, Alanen H, Eki R, Abbas T, Maksimainen M bioRxiv. 2023; .

PMID: 38076829 PMC: 10705365. DOI: 10.1101/2023.11.29.569193.

Induction of PARP7 Creates a Vulnerability for Growth Inhibition by RBN2397 in Prostate Cancer Cells.

Yang C, Wierbilowicz K, Dworak N, Bae S, Tengse S, Abianeh N Cancer Res Commun. 2023; 3(4):592-606.

PMID: 37077937 PMC: 10108886. DOI: 10.1158/2767-9764.CRC-23-0086.

Uncommon posttranslational modifications in proteomics: ADP-ribosylation, tyrosine nitration, and tyrosine sulfation.

Bashyal A, Brodbelt J Mass Spectrom Rev. 2022; 43(2):289-326.

PMID: 36165040 PMC: 10040477. DOI: 10.1002/mas.21811.

PARP7 mono-ADP-ribosylates the agonist conformation of the androgen receptor in the nucleus.

Kamata T, Yang C, Paschal B Biochem J. 2021; 478(15):2999-3014.

PMID: 34264286 PMC: 9482820. DOI: 10.1042/BCJ20210378.

References

Rouleau M, Patel A, Hendzel M, Kaufmann S, Poirier G . PARP inhibition: PARP1 and beyond. Nat Rev Cancer. 2010; 10(4):293-301. PMC: 2910902. DOI: 10.1038/nrc2812. View

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

Karras G, Kustatscher G, Buhecha H, Allen M, Pugieux C, Sait F . The macro domain is an ADP-ribose binding module. EMBO J. 2005; 24(11):1911-20. PMC: 1142602. DOI: 10.1038/sj.emboj.7600664. View

Siegel R, Miller K, Jemal A . Cancer statistics, 2018. CA Cancer J Clin. 2018; 68(1):7-30. DOI: 10.3322/caac.21442. View

Martello R, Leutert M, Jungmichel S, Bilan V, Larsen S, Young C . Proteome-wide identification of the endogenous ADP-ribosylome of mammalian cells and tissue. Nat Commun. 2016; 7:12917. PMC: 5056437. DOI: 10.1038/ncomms12917. View

Jungmichel S, Rosenthal F, Altmeyer M, Lukas J, Hottiger M, Nielsen M . Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol Cell. 2013; 52(2):272-85. DOI: 10.1016/j.molcel.2013.08.026. View

Allen M, Buckle A, Cordell S, 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. 2003; 330(3):503-11. DOI: 10.1016/s0022-2836(03)00473-x. View

Bennett N, Gardiner R, Hooper J, Johnson D, Gobe G . Molecular cell biology of androgen receptor signalling. Int J Biochem Cell Biol. 2009; 42(6):813-27. DOI: 10.1016/j.biocel.2009.11.013. View

Dani N, Stilla A, Marchegiani A, Tamburro A, Till S, Ladurner A . Combining affinity purification by ADP-ribose-binding macro domains with mass spectrometry to define the mammalian ADP-ribosyl proteome. Proc Natl Acad Sci U S A. 2009; 106(11):4243-8. PMC: 2657436. DOI: 10.1073/pnas.0900066106. View

10.

Gagne J, Pic E, Isabelle M, Krietsch J, Ethier C, Paquet E . Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 2012; 40(16):7788-805. PMC: 3439892. DOI: 10.1093/nar/gks486. View

11.

Heinlein C, Chang C . Androgen receptor (AR) coregulators: an overview. Endocr Rev. 2002; 23(2):175-200. DOI: 10.1210/edrv.23.2.0460. View

12.

Bock F, Chang P . New directions in poly(ADP-ribose) polymerase biology. FEBS J. 2016; 283(22):4017-4031. DOI: 10.1111/febs.13737. View

13.

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

14.

Balk S, Knudsen K . AR, the cell cycle, and prostate cancer. Nucl Recept Signal. 2008; 6:e001. PMC: 2254330. DOI: 10.1621/nrs.06001. View

15.

Till S, Ladurner A . Sensing NAD metabolites through macro domains. Front Biosci (Landmark Ed). 2009; 14(9):3246-58. DOI: 10.2741/3448. View

16.

Schiewer M, Goodwin J, Han S, Brenner J, Augello M, Dean J . Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov. 2012; 2(12):1134-49. PMC: 3519969. DOI: 10.1158/2159-8290.CD-12-0120. View

17.

Gioeli D, Paschal B . Post-translational modification of the androgen receptor. Mol Cell Endocrinol. 2011; 352(1-2):70-8. DOI: 10.1016/j.mce.2011.07.004. View

18.

Bindesboll C, Tan S, Bott D, Cho T, Tamblyn L, MacPherson L . TCDD-inducible poly-ADP-ribose polymerase (TIPARP/PARP7) mono-ADP-ribosylates and co-activates liver X receptors. Biochem J. 2016; 473(7):899-910. DOI: 10.1042/BJ20151077. View

19.

Mateo J, Carreira S, Sandhu S, Miranda S, Mossop H, Perez-Lopez R . DNA-Repair Defects and Olaparib in Metastatic Prostate Cancer. N Engl J Med. 2015; 373(18):1697-708. PMC: 5228595. DOI: 10.1056/NEJMoa1506859. View

20.

Matsubara H, Hasegawa S, Fujimura S, Shima T, Sugimura T . Studies on poly (adenosine diphosphate ribose). V. Mechanism of hydrolysis of poly (adenosine diphosphate ribose) by snake venom phosphodiesterase. J Biol Chem. 1970; 245(14):3606-11. View