General ADP-Ribosylation Mechanism Based on the Structure of ADP-Ribosyltransferase–Substrate Complexes
Abstract
:1. Introduction
2. Substrate Recognition Mechanism of ARTC: Iota-like Toxin and C3-like Exoenzyme
3. Substrate Recognition Mechanism of Bacterial ARTD
4. ADP-Ribosylation of Ubiquitin
5. ADP-Ribosylation of DNA by ScARP in the Pierisin Family (ARTC)
6. ADP-Ribosylation of DNA by DarT2 and DarT1 (ARTD)
7. ADP-Ribosylation by Poly(ADP-Ribose) Polymerase (PARP)
8. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Aktories, K. Bacterial protein toxins that modify host regulatory GTPases. Nat. Rev. Microbiol. 2011, 9, 487–498. [Google Scholar] [CrossRef]
- Aravind, L.; Zhang, D.; de Souza, R.F.; Anand, S.; Iyer, L.M. The natural history of ADP-ribosyltransferases and the ADP-ribosylation system. Curr. Top. Microbiol. Immunol. 2015, 384, 3–32. [Google Scholar] [CrossRef]
- Laing, S.; Unger, M.; Koch-Nolte, F.; Haag, F. ADP-ribosylation of arginine. Amino Acids 2011, 41, 257–269. [Google Scholar] [CrossRef]
- Palazzo, L.; Mikoc, A.; Ahel, I. ADP-ribosylation: New facets of an ancient modification. FEBS J. 2017, 284, 2932–2946. [Google Scholar] [CrossRef] [PubMed]
- Honjo, T.; Nishizuka, Y.; Hayaishi, O. Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis. J. Biol. Chem. 1968, 243, 3553–3555. [Google Scholar] [CrossRef]
- Honjo, T.; Nishizuka, Y.; Kato, I.; Hayaishi, O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J. Biol. Chem. 1971, 246, 4251–4260. [Google Scholar] [CrossRef] [PubMed]
- Collier, R.J.; Pappenheimer, A.M., Jr. Studies on the Mode of Action of Diphtheria Toxin. Ii. Effect of Toxin on Amino Acid Incorporation in Cell-Free Systems. J. Exp. Med. 1964, 120, 1019–1039. [Google Scholar] [CrossRef]
- Katada, T.; Ui, M. ADP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J. Biol. Chem. 1982, 257, 7210–7216. [Google Scholar] [CrossRef] [PubMed]
- Aktories, K.; Frevert, J. ADP-ribosylation of a 21–24 kDa eukaryotic protein(s) by C3, a novel botulinum ADP-ribosyltransferase, is regulated by guanine nucleotide. Biochem. J. 1987, 247, 363–368. [Google Scholar] [CrossRef]
- Ohashi, Y.; Narumiya, S. ADP-ribosylation of a Mr 21,000 membrane protein by type D botulinum toxin. J. Biol. Chem. 1987, 262, 1430–1433. [Google Scholar] [CrossRef]
- Aktories, K.; Barmann, M.; Ohishi, I.; Tsuyama, S.; Jakobs, K.H.; Habermann, E. Botulinum C2 toxin ADP-ribosylates actin. Nature 1986, 322, 390–392. [Google Scholar] [CrossRef]
- Tsuge, H.; Nagahama, M.; Nishimura, H.; Hisatsune, J.; Sakaguchi, Y.; Itogawa, Y.; Katunuma, N.; Sakurai, J. Crystal structure and site-directed mutagenesis of enzymatic components from Clostridium perfringens iota-toxin. J. Mol. Biol. 2003, 325, 471–483. [Google Scholar] [CrossRef]
- Langelier, M.F.; Pascal, J.M. PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr. Opin. Struct. Biol. 2013, 23, 134–143. [Google Scholar] [CrossRef]
- Mueller-Dieckmann, C.; Ritter, H.; Haag, F.; Koch-Nolte, F.; Schulz, G.E. Structure of the ecto-ADP-ribosyl transferase ART2.2 from rat. J. Mol. Biol. 2002, 322, 687–696. [Google Scholar] [CrossRef]
- Ritter, H.; Koch-Nolte, F.; Marquez, V.E.; Schulz, G.E. Substrate binding and catalysis of ecto-ADP-ribosyltransferase 2.2 from rat. Biochemistry 2003, 42, 10155–10162. [Google Scholar] [CrossRef]
- Berti, P.J.; Blanke, S.R.; Schramm, V.L. Transition State Structure for the Hydrolysis of NAD Catalyzed by Diphtheria Toxin. J. Am. Chem. Soc. 1997, 119, 12079–12088. [Google Scholar] [CrossRef]
- Parikh, S.L.; Schramm, V.L. Transition state structure for ADP-ribosylation of eukaryotic elongation factor 2 catalyzed by diphtheria toxin. Biochemistry 2004, 43, 1204–1212. [Google Scholar] [CrossRef]
- Scheuring, J.; Schramm, V.L. Kinetic isotope effect characterization of the transition state for oxidized nicotinamide adenine dinucleotide hydrolysis by pertussis toxin. Biochemistry 1997, 36, 4526–4534. [Google Scholar] [CrossRef]
- Takamura-Enya, T.; Watanabe, M.; Totsuka, Y.; Kanazawa, T.; Matsushima-Hibiya, Y.; Koyama, K.; Sugimura, T.; Wakabayashi, K. Mono(ADP-ribosyl)ation of 2′-deoxyguanosine residue in DNA by an apoptosis-inducing protein, pierisin-1, from cabbage butterfly. Proc. Natl. Acad. Sci. USA 2001, 98, 12414–12419. [Google Scholar] [CrossRef] [PubMed]
- Nakano, T.; Matsushima-Hibiya, Y.; Yamamoto, M.; Enomoto, S.; Matsumoto, Y.; Totsuka, Y.; Watanabe, M.; Sugimura, T.; Wakabayashi, K. Purification and molecular cloning of a DNA ADP-ribosylating protein, CARP-1, from the edible clam Meretrix lamarckii. Proc. Natl. Acad. Sci. USA 2006, 103, 13652–13657. [Google Scholar] [CrossRef] [PubMed]
- Jankevicius, G.; Ariza, A.; Ahel, M.; Ahel, I. The Toxin-Antitoxin System DarTG Catalyzes Reversible ADP-Ribosylation of DNA. Mol. Cell 2016, 64, 1109–1116. [Google Scholar] [CrossRef]
- Dabbs, E.R.; Yazawa, K.; Mikami, Y.; Miyaji, M.; Morisaki, N.; Iwasaki, S.; Furihata, K. Ribosylation by mycobacterial strains as a new mechanism of rifampin inactivation. Antimicrob. Agents Chemother. 1995, 39, 1007–1009. [Google Scholar] [CrossRef]
- Baysarowich, J.; Koteva, K.; Hughes, D.W.; Ejim, L.; Griffiths, E.; Zhang, K.; Junop, M.; Wright, G.D. Rifamycin antibiotic resistance by ADP-ribosylation: Structure and diversity of Arr. Proc. Natl. Acad. Sci. USA 2008, 105, 4886–4891. [Google Scholar] [CrossRef]
- Ho, T.L.; Ho, H.C.; Hamilton, L.D. Biochemical significance of the hard and soft acids and bases principle. Chem. Biol. Interact. 1978, 23, 65–84. [Google Scholar] [CrossRef]
- Tsuge, H.; Nagahama, M.; Oda, M.; Iwamoto, S.; Utsunomiya, H.; Marquez, V.E.; Katunuma, N.; Nishizawa, M.; Sakurai, J. Structural basis of actin recognition and arginine ADP-ribosylation by Clostridium perfringens iota-toxin. Proc. Natl. Acad. Sci. USA 2008, 105, 7399–7404. [Google Scholar] [CrossRef]
- Toda, A.; Tsurumura, T.; Yoshida, T.; Tsumori, Y.; Tsuge, H. Rho GTPase Recognition by C3 Exoenzyme Based on C3-RhoA Complex Structure. J. Biol. Chem. 2015, 290, 19423–19432. [Google Scholar] [CrossRef]
- Yoshida, T.; Tsuge, H. Substrate N(2) atom recognition mechanism in pierisin family DNA-targeting, guanine-specific ADP-ribosyltransferase ScARP. J. Biol. Chem. 2018, 293, 13768–13774. [Google Scholar] [CrossRef]
- Dong, Y.; Mu, Y.; Xie, Y.; Zhang, Y.; Han, Y.; Zhou, Y.; Wang, W.; Liu, Z.; Wu, M.; Wang, H.; et al. Structural basis of ubiquitin modification by the Legionella effector SdeA. Nature 2018, 557, 674–678. [Google Scholar] [CrossRef]
- Wang, Y.; Shi, M.; Feng, H.; Zhu, Y.; Liu, S.; Gao, A.; Gao, P. Structural Insights into Non-canonical Ubiquitination Catalyzed by SidE. Cell 2018, 173, 1231–1243.e16. [Google Scholar] [CrossRef] [PubMed]
- Jorgensen, R.; Merrill, A.R.; Yates, S.P.; Marquez, V.E.; Schwan, A.L.; Boesen, T.; Andersen, G.R. Exotoxin A-eEF2 complex structure indicates ADP ribosylation by ribosome mimicry. Nature 2005, 436, 979–984. [Google Scholar] [CrossRef] [PubMed]
- Schuller, M.; Butler, R.E.; Ariza, A.; Tromans-Coia, C.; Jankevicius, G.; Claridge, T.D.W.; Kendall, S.L.; Goh, S.; Stewart, G.R.; Ahel, I. Molecular basis for DarT ADP-ribosylation of a DNA base. Nature 2021, 596, 597–602. [Google Scholar] [CrossRef] [PubMed]
- Schuller, M.; Raggiaschi, R.; Mikolcevic, P.; Rack, J.G.M.; Ariza, A.; Zhang, Y.; Ledermann, R.; Tang, C.; Mikoc, A.; Ahel, I. Molecular basis for the reversible ADP-ribosylation of guanosine bases. Mol. Cell 2023, 83, 2303–2315.e6. [Google Scholar] [CrossRef] [PubMed]
- Tan, J.; Xu, Y.; Wang, X.; Yan, F.; Xian, W.; Liu, X.; Chen, Y.; Zhu, Y.; Zhou, Y. Molecular basis of threonine ADP-ribosylation of ubiquitin by bacterial ARTs. Nat. Chem. Biol. 2024, 20, 463–472. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Rondon-Cordero, H.M.; Das, C. Crystal structure of bacterial ubiquitin ADP-ribosyltransferase CteC reveals a substrate-recruiting insertion. J. Biol. Chem. 2024, 300, 105604. [Google Scholar] [CrossRef] [PubMed]
- Schering, B.; Barmann, M.; Chhatwal, G.S.; Geipel, U.; Aktories, K. ADP-ribosylation of skeletal muscle and non-muscle actin by Clostridium perfringens iota toxin. Eur. J. Biochem. 1988, 171, 225–229. [Google Scholar] [CrossRef] [PubMed]
- Popoff, M.R.; Boquet, P. Clostridium spiroforme toxin is a binary toxin which ADP-ribosylates cellular actin. Biochem. Biophys. Res. Commun. 1988, 152, 1361–1368. [Google Scholar] [CrossRef] [PubMed]
- Popoff, M.R.; Rubin, E.J.; Gill, D.M.; Boquet, P. Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect. Immun. 1988, 56, 2299–2306. [Google Scholar] [CrossRef]
- Han, S.; Craig, J.A.; Putnam, C.D.; Carozzi, N.B.; Tainer, J.A. Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex. Nat. Struct. Biol. 1999, 6, 932–936. [Google Scholar]
- Morii, N.; Sekine, A.; Ohashi, Y.; Nakao, K.; Imura, H.; Fujiwara, M.; Narumiya, S. Purification and properties of the cytosolic substrate for botulinum ADP-ribosyltransferase. Identification as an Mr 22,000 guanine nucleotide-binding protein. J. Biol. Chem. 1988, 263, 12420–12426. [Google Scholar] [CrossRef]
- Sekine, A.; Fujiwara, M.; Narumiya, S. Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J. Biol. Chem. 1989, 264, 8602–8605. [Google Scholar] [CrossRef]
- Han, S.; Arvai, A.S.; Clancy, S.B.; Tainer, J.A. Crystal structure and novel recognition motif of rho ADP-ribosylating C3 exoenzyme from Clostridium botulinum: Structural insights for recognition specificity and catalysis. J. Mol. Biol. 2001, 305, 95–107. [Google Scholar] [CrossRef]
- Schleberger, C.; Hochmann, H.; Barth, H.; Aktories, K.; Schulz, G.E. Structure and action of the binary C2 toxin from Clostridium botulinum. J. Mol. Biol. 2006, 364, 705–715. [Google Scholar] [CrossRef]
- Margarit, S.M.; Davidson, W.; Frego, L.; Stebbins, C.E. A steric antagonism of actin polymerization by a salmonella virulence protein. Structure 2006, 14, 1219–1229. [Google Scholar] [CrossRef]
- Vogelsgesang, M.; Stieglitz, B.; Herrmann, C.; Pautsch, A.; Aktories, K. Crystal structure of the Clostridium limosum C3 exoenzyme. FEBS Lett. 2008, 582, 1032–1036. [Google Scholar] [CrossRef]
- Sundriyal, A.; Roberts, A.K.; Shone, C.C.; Acharya, K.R. Structural basis for substrate recognition in the enzymatic component of ADP-ribosyltransferase toxin CDTa from Clostridium difficile. J. Biol. Chem. 2009, 284, 28713–28719. [Google Scholar] [CrossRef]
- Tsurumura, T.; Tsumori, Y.; Qiu, H.; Oda, M.; Sakurai, J.; Nagahama, M.; Tsuge, H. Arginine ADP-ribosylation mechanism based on structural snapshots of iota-toxin and actin complex. Proc. Natl. Acad. Sci. USA 2013, 110, 4267–4272. [Google Scholar] [CrossRef]
- Jank, T.; Aktories, K. Strain-alleviation model of ADP-ribosylation. Proc. Natl. Acad. Sci. USA 2013, 110, 4163–4164. [Google Scholar] [CrossRef]
- Choe, S.; Bennett, M.J.; Fujii, G.; Curmi, P.M.; Kantardjieff, K.A.; Collier, R.J.; Eisenberg, D. The crystal structure of diphtheria toxin. Nature 1992, 357, 216–222. [Google Scholar] [CrossRef]
- Bell, C.E.; Eisenberg, D. Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 1996, 35, 1137–1149. [Google Scholar] [CrossRef] [PubMed]
- Jorgensen, R.; Wang, Y.; Visschedyk, D.; Merrill, A.R. The nature and character of the transition state for the ADP-ribosyltransferase reaction. EMBO Rep. 2008, 9, 802–809. [Google Scholar] [CrossRef] [PubMed]
- Hershko, A.; Ciechanover, A. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 1992, 61, 761–807. [Google Scholar] [CrossRef]
- Bhogaraju, S.; Kalayil, S.; Liu, Y.; Bonn, F.; Colby, T.; Matic, I.; Dikic, I. Phosphoribosylation of Ubiquitin Promotes Serine Ubiquitination and Impairs Conventional Ubiquitination. Cell 2016, 167, 1636–1649.e13. [Google Scholar] [CrossRef]
- Qiu, J.; Sheedlo, M.J.; Yu, K.; Tan, Y.; Nakayasu, E.S.; Das, C.; Liu, X.; Luo, Z.Q. Ubiquitination independent of E1 and E2 enzymes by bacterial effectors. Nature 2016, 533, 120–124. [Google Scholar] [CrossRef]
- Yan, F.; Huang, C.; Wang, X.; Tan, J.; Cheng, S.; Wan, M.; Wang, Z.; Wang, S.; Luo, S.; Li, A.; et al. Threonine ADP-Ribosylation of Ubiquitin by a Bacterial Effector Family Blocks Host Ubiquitination. Mol. Cell 2020, 78, 641–652.e9. [Google Scholar] [CrossRef]
- Koyama, K.; Wakabayashi, K.; Masutani, M.; Koiwai, K.; Watanabe, M.; Yamazaki, S.; Kono, T.; Miki, K.; Sugimura, T. Presence in Pieris rapae of cytotoxic activity against human carcinoma cells. Jpn. J. Cancer Res. 1996, 87, 1259–1262. [Google Scholar] [CrossRef]
- Watanabe, M.; Kono, T.; Koyama, K.; Sugimura, T.; Wakabayashi, K. Purification of pierisin, an inducer of apoptosis in human gastric carcinoma cells, from cabbage butterfly, Pieris rapae. Jpn. J. Cancer Res. 1998, 89, 556–561. [Google Scholar] [CrossRef]
- Takamura-Enya, T.; Watanabe, M.; Koyama, K.; Sugimura, T.; Wakabayashi, K. Mono(ADP-ribosyl)ation of the N2 amino groups of guanine residues in DNA by pierisin-2, from the cabbage butterfly, Pieris brassicae. Biochem. Biophys. Res. Commun. 2004, 323, 579–582. [Google Scholar] [CrossRef]
- Matsumoto, Y.; Nakano, T.; Yamamoto, M.; Matsushima-Hibiya, Y.; Odagiri, K.; Yata, O.; Koyama, K.; Sugimura, T.; Wakabayashi, K. Distribution of cytotoxic and DNA ADP-ribosylating activity in crude extracts from butterflies among the family Pieridae. Proc. Natl. Acad. Sci. USA 2008, 105, 2516–2520. [Google Scholar] [CrossRef]
- Yamamoto, M.; Nakano, T.; Matsushima-Hibiya, Y.; Totsuka, Y.; Takahashi-Nakaguchi, A.; Matsumoto, Y.; Sugimura, T.; Wakabayashi, K. Molecular cloning of apoptosis-inducing Pierisin-like proteins, from two species of white butterfly, Pieris melete and Aporia crataegi. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 154, 326–333. [Google Scholar] [CrossRef] [PubMed]
- Matsushima-Hibiya, Y.; Watanabe, M.; Kono, T.; Kanazawa, T.; Koyama, K.; Sugimura, T.; Wakabayashi, K. Purification and cloning of pierisin-2, an apoptosis-inducing protein from the cabbage butterfly, Pieris brassicae. Eur. J. Biochem. 2000, 267, 5742–5750. [Google Scholar] [CrossRef] [PubMed]
- Subbarayan, S.; Marimuthu, S.K.; Nachimuthu, S.K.; Zhang, W.; Subramanian, S. Characterization and cytotoxic activity of apoptosis-inducing pierisin-5 protein from white cabbage butterfly. Int. J. Biol. Macromol. 2016, 87, 16–27. [Google Scholar] [CrossRef]
- Sarathbabu, S.; Marimuthu, S.K.; Ghatak, S.; Vidyalakshmi, S.; Gurusubramanian, G.; Ghosh, S.K.; Subramanian, S.; Zhang, W.; Kumar, N.S. Induction of Apoptosis by Pierisin-6 in HPV Positive HeLa and HepG2 Cancer Cells is Mediated by the Caspase-3 Dependent Mitochondrial Pathway. Anticancer Agents Med. Chem. 2019, 19, 337–346. [Google Scholar] [CrossRef]
- Nakano, T.; Matsushima-Hibiya, Y.; Yamamoto, M.; Takahashi-Nakaguchi, A.; Fukuda, H.; Ono, M.; Takamura-Enya, T.; Kinashi, H.; Totsuka, Y. ADP-ribosylation of guanosine by SCO5461 protein secreted from Streptomyces coelicolor. Toxicon 2013, 63, 55–63. [Google Scholar] [CrossRef]
- Lyons, B.; Ravulapalli, R.; Lanoue, J.; Lugo, M.R.; Dutta, D.; Carlin, S.; Merrill, A.R. Scabin, a Novel DNA-acting ADP-ribosyltransferase from Streptomyces scabies. J. Biol. Chem. 2016, 291, 11198–11215. [Google Scholar] [CrossRef]
- Lyons, B.; Lugo, M.R.; Carlin, S.; Lidster, T.; Merrill, A.R. Characterization of the catalytic signature of Scabin toxin, a DNA-targeting ADP-ribosyltransferase. Biochem. J. 2018, 475, 225–245. [Google Scholar] [CrossRef]
- Nakano, T.; Takahashi-Nakaguchi, A.; Yamamoto, M.; Watanabe, M. Pierisins and CARP-1: ADP-ribosylation of DNA by ARTCs in butterflies and shellfish. Curr. Top. Microbiol. Immunol. 2015, 384, 127–149. [Google Scholar] [CrossRef]
- Oda, T.; Hirabayashi, H.; Shikauchi, G.; Takamura, R.; Hiraga, K.; Minami, H.; Hashimoto, H.; Yamamoto, M.; Wakabayashi, K.; Shimizu, T.; et al. Structural basis of autoinhibition and activation of the DNA-targeting ADP-ribosyltransferase pierisin-1. J. Biol. Chem. 2017, 292, 15445–15455. [Google Scholar] [CrossRef]
- LeRoux, M.; Srikant, S.; Teodoro, G.I.C.; Zhang, T.; Littlehale, M.L.; Doron, S.; Badiee, M.; Leung, A.K.L.; Sorek, R.; Laub, M.T. The DarTG toxin-antitoxin system provides phage defence by ADP-ribosylating viral DNA. Nat. Microbiol. 2022, 7, 1028–1040. [Google Scholar] [CrossRef]
- Hilz, H. ADP-ribose. A historical overview. Adv. Exp. Med. Biol. 1997, 419, 15–24. [Google Scholar]
- Masutani, M. The pioneering spirit of Takashi Sugimura: His studies of the biochemistry of poly(ADP-ribosylation) and of cancer. J. Biochem. 2012, 151, 221–228. [Google Scholar] [CrossRef]
- Hottiger, M.O.; Hassa, P.O.; Luscher, B.; Schuler, H.; Koch-Nolte, F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 2010, 35, 208–219. [Google Scholar] [CrossRef]
- Steffen, J.D.; Brody, J.R.; Armen, R.S.; Pascal, J.M. Structural Implications for Selective Targeting of PARPs. Front. Oncol. 2013, 3, 301. [Google Scholar] [CrossRef]
- Munnur, D.; Ahel, I. Reversible mono-ADP-ribosylation of DNA breaks. FEBS J. 2017, 284, 4002–4016. [Google Scholar] [CrossRef]
- Slade, D.; Dunstan, M.S.; Barkauskaite, E.; Weston, R.; Lafite, P.; Dixon, N.; Ahel, M.; Leys, D.; Ahel, I. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 2011, 477, 616–620. [Google Scholar] [CrossRef]
- Martin-Hernandez, K.; Rodriguez-Vargas, J.M.; Schreiber, V.; Dantzer, F. Expanding functions of ADP-ribosylation in the maintenance of genome integrity. Semin. Cell Dev. Biol. 2017, 63, 92–101. [Google Scholar] [CrossRef]
- Liu, C.; Vyas, A.; Kassab, M.A.; Singh, A.K.; Yu, X. The role of poly ADP-ribosylation in the first wave of DNA damage response. Nucleic Acids Res. 2017, 45, 8129–8141. [Google Scholar] [CrossRef]
- Pinto, A.F.; Schuler, H. Comparative structural analysis of the putative mono-ADP-ribosyltransferases of the ARTD/PARP family. Curr. Top. Microbiol. Immunol. 2015, 384, 153–166. [Google Scholar] [CrossRef]
- Frigon, L.; Pascal, J.M. Structural and biochemical analysis of the PARP1-homology region of PARP4/vault PARP. Nucleic Acids Res. 2023, 51, 12492–12507. [Google Scholar] [CrossRef]
- Gibbs-Seymour, I.; Fontana, P.; Rack, J.G.M.; Ahel, I. HPF1/C4orf27 Is a PARP-1-Interacting Protein that Regulates PARP-1 ADP-Ribosylation Activity. Mol. Cell 2016, 62, 432–442. [Google Scholar] [CrossRef] [PubMed]
- Leidecker, O.; Bonfiglio, J.J.; Colby, T.; Zhang, Q.; Atanassov, I.; Zaja, R.; Palazzo, L.; Stockum, A.; Ahel, I.; Matic, I. Serine is a new target residue for endogenous ADP-ribosylation on histones. Nat. Chem. Biol. 2016, 12, 998–1000. [Google Scholar] [CrossRef] [PubMed]
- Suskiewicz, M.J.; Zobel, F.; Ogden, T.E.H.; Fontana, P.; Ariza, A.; Yang, J.C.; Zhu, K.; Bracken, L.; Hawthorne, W.J.; Ahel, D.; et al. HPF1 completes the PARP active site for DNA damage-induced ADP-ribosylation. Nature 2020, 579, 598–602. [Google Scholar] [CrossRef] [PubMed]
- Sun, F.H.; Zhao, P.; Zhang, N.; Kong, L.L.; Wong, C.C.L.; Yun, C.H. HPF1 remodels the active site of PARP1 to enable the serine ADP-ribosylation of histones. Nat. Commun. 2021, 12, 1028. [Google Scholar] [CrossRef] [PubMed]
- Langelier, M.F.; Planck, J.L.; Roy, S.; Pascal, J.M. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 2012, 336, 728–732. [Google Scholar] [CrossRef] [PubMed]
- Bilokapic, S.; Suskiewicz, M.J.; Ahel, I.; Halic, M. Bridging of DNA breaks activates PARP2-HPF1 to modify chromatin. Nature 2020, 585, 609–613. [Google Scholar] [CrossRef] [PubMed]
- Li, P.; Zhen, Y.; Yu, Y. Site-specific analysis of the Asp- and Glu-ADP-ribosylated proteome by quantitative mass spectrometry. Methods Enzymol. 2019, 626, 301–321. [Google Scholar] [CrossRef] [PubMed]
- Vyas, S.; Matic, I.; Uchima, L.; Rood, J.; Zaja, R.; Hay, R.T.; Ahel, I.; Chang, P. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 2014, 5, 4426. [Google Scholar] [CrossRef] [PubMed]
- Abramson, J.; Adler, J.; Dunger, J.; Evans, R.; Green, T.; Pritzel, A.; Ronneberger, O.; Willmore, L.; Ballard, A.J.; Bambrick, J.; et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 2024, 630, 493–500. [Google Scholar] [CrossRef] [PubMed]
- Marquez, V.E.; Tseng, C.K.; Gebeyehu, G.; Cooney, D.A.; Ahluwalia, G.S.; Kelley, J.A.; Dalal, M.; Fuller, R.W.; Wilson, Y.A.; Johns, D.G. Thiazole-4-carboxamide adenine dinucleotide (TAD). Analogues stable to phosphodiesterase hydrolysis. J. Med. Chem. 1986, 29, 1726–1731. [Google Scholar] [CrossRef] [PubMed]
- Zatorski, A.; Watanabe, K.A.; Carr, S.F.; Goldstein, B.M.; Pankiewicz, K.W. Chemical synthesis of benzamide adenine dinucleotide: Inhibition of inosine monophosphate dehydrogenase (types I and II). J. Med. Chem. 1996, 39, 2422–2426. [Google Scholar] [CrossRef] [PubMed]
- Rudolph, J.; Jung, K.; Luger, K. Inhibitors of PARP: Number crunching and structure gazing. Proc. Natl. Acad. Sci. USA 2022, 119, e2121979119. [Google Scholar] [CrossRef]
ART Class | Target | Residue or Base |
---|---|---|
ARTC | ||
Ia (Iota toxin A subunit) | actin | Arg 177 |
C3 exotoxin | RhoA | Asn 41 |
ScARP | GDP | guanine |
SdeA | Ubiqutin | Arg 42 |
ARTD | ||
ExoA | eEF2 | diphthamide 699 |
DarT2 | DNA | thymidine |
DarT1 | DNA | guanine |
Chimeric featured ART | ||
CteC | Ubiqutin | Thr 66 |
Turn 1 | Turn 2 | |||||||
---|---|---|---|---|---|---|---|---|
X | X | ϕ | X | X | E/Q | X | E | |
Ia | P | G | Y | A | G | E | Y | E |
C3cer | T | A | Y | P | G | Q | Y | E |
SdeA | H | G | E | G | T | E | S | E |
SdeB | H | M | T | G | S | E | D | E |
SdeC | H | M | A | G | S | E | D | E |
SidE | H | V | S | G | S | E | S | E |
ScARP | H | K | W | A | D | Q | V | E |
Scabin | H | K | W | A | D | Q | V | E |
Pierisin-1 | S | P | W | P | N | Q | M | E |
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Tsuge, H.; Habuka, N.; Yoshida, T. General ADP-Ribosylation Mechanism Based on the Structure of ADP-Ribosyltransferase–Substrate Complexes. Toxins 2024, 16, 313. https://doi.org/10.3390/toxins16070313
Tsuge H, Habuka N, Yoshida T. General ADP-Ribosylation Mechanism Based on the Structure of ADP-Ribosyltransferase–Substrate Complexes. Toxins. 2024; 16(7):313. https://doi.org/10.3390/toxins16070313
Chicago/Turabian StyleTsuge, Hideaki, Noriyuki Habuka, and Toru Yoshida. 2024. "General ADP-Ribosylation Mechanism Based on the Structure of ADP-Ribosyltransferase–Substrate Complexes" Toxins 16, no. 7: 313. https://doi.org/10.3390/toxins16070313