PARPs and ADP-Ribosylation in Chronic Inflammation: A Focus on Macrophages
Abstract
:1. Introduction
2. PARylation, Macrophages, and Chronic Inflammation
2.1. ADP-Ribosylation and DNA Damage
2.2. PARP1/ARTD1 Promotes Transcription of Pro-Inflammatory and Apoptosis-Related Genes
2.3. PARP1/ARTD1 Mediates Host–Pathogen Interactions in Chagas Heart Disease
2.4. PARP1/ARTD1 in Cardiovascular Inflammation
3. MARylation, Macrophages, and Chronic Inflammation
3.1. PARP7/ARTD14 Mediates Epithelial Inflammation
3.2. PARP9/ARTD9 Mediates Viral and Bacterial Host–Pathogen Interactions
3.3. PARP14/ARTD8 Mediates Chronic Inflammation and Response to Arboviruses
3.4. PARP9/ARTD9 and PARP14/ARTD8 Mediate Macrophage Activation in Atherosclerosis
4. SARS-CoV-2, ADP-Ribosylation, and Innate Immune Response
5. Mass Spectrometry and ADP-Ribosylation
5.1. Enrichment Strategies and Activation Methods Influence the Identification of ADP-Ribosylated Proteins in Macrophages
5.2. An Innovative Spectral Annotation Strategy Facilitates the Report of ADP-Ribosylated Peptides in IFN-γ-Stimulated Mice
6. Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Kim, D.S.; Challa, S.; Jones, A.; Kraus, W.L. PARPs and ADP-ribosylation in RNA biology: From RNA expression and processing to protein translation and proteostasis. Genes. Dev. 2020, 34, 302–320. [Google Scholar] [CrossRef] [PubMed]
- Luscher, B.; Ahel, I.; Altmeyer, M.; Ashworth, A.; Bai, P.; Chang, P.; Cohen, M.; Corda, D.; Dantzer, F.; Daugherty, M.D.; et al. ADP-ribosyltransferases, an update on function and nomenclature. FEBS J. 2022, 289, 7399–7410. [Google Scholar] [CrossRef] [PubMed]
- Xue, G.; Braczyk, K.; Goncalves-Carneiro, D.; Dawidziak, D.M.; Sanchez, K.; Ong, H.; Wan, Y.; Zadrozny, K.K.; Ganser-Pornillos, B.K.; Bieniasz, P.D.; et al. Poly(ADP-ribose) potentiates ZAP antiviral activity. PLoS Pathog. 2022, 18, e1009202. [Google Scholar] [CrossRef] [PubMed]
- 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] [Green Version]
- Poltronieri, P.; Miwa, M.; Masutani, M. ADP-Ribosylation as Post-Translational Modification of Proteins: Use of Inhibitors in Cancer Control. Int. J. Mol. Sci. 2021, 22, 10829. [Google Scholar] [CrossRef] [PubMed]
- Hengel, S.M.; Shaffer, S.A.; Nunn, B.L.; Goodlett, D.R. Tandem mass spectrometry investigation of ADP-ribosylated kemptide. J. Am. Soc. Mass. Spectrom. 2009, 20, 477–483. [Google Scholar] [CrossRef] [Green Version]
- Fontana, P.; Bonfiglio, J.J.; Palazzo, L.; Bartlett, E.; Matic, I.; Ahel, I. Serine ADP-ribosylation reversal by the hydrolase ARH3. Elife 2017, 6, e28533. [Google Scholar] [CrossRef]
- Abplanalp, J.; Leutert, M.; Frugier, E.; Nowak, K.; Feurer, R.; Kato, J.; Kistemaker, H.V.A.; Filippov, D.V.; Moss, J.; Caflisch, A.; et al. Proteomic analyses identify ARH3 as a serine mono-ADP-ribosylhydrolase. Nat. Commun. 2017, 8, 2055. [Google Scholar] [CrossRef] [Green Version]
- Abplanalp, J.; Hopp, A.K.; Hottiger, M.O. Mono-ADP-Ribosylhydrolase Assays. Methods Mol. Biol. 2018, 1813, 205–213. [Google Scholar] [CrossRef]
- Stevens, L.A.; Kato, J.; Kasamatsu, A.; Oda, H.; Lee, D.Y.; Moss, J. The ARH and Macrodomain Families of alpha-ADP-ribose-acceptor Hydrolases Catalyze alpha-NAD(+) Hydrolysis. ACS Chem. Biol. 2019, 14, 2576–2584. [Google Scholar] [CrossRef]
- Yang, X.; Ma, Y.; Li, Y.; Dong, Y.; Yu, L.L.; Wang, H.; Guo, L.; Wu, C.; Yu, X.; Liu, X. Molecular basis for the MacroD1-mediated hydrolysis of ADP-ribosylation. DNA Repair. 2020, 94, 102899. [Google Scholar] [CrossRef]
- Chen, D.; Vollmar, M.; Rossi, M.N.; Phillips, C.; Kraehenbuehl, R.; Slade, D.; Mehrotra, P.V.; von Delft, F.; Crosthwaite, S.K.; Gileadi, O.; et al. Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J. Biol. Chem. 2011, 286, 13261–13271. [Google Scholar] [CrossRef] [Green Version]
- Zong, W.; Gong, Y.; Sun, W.; Li, T.; Wang, Z.Q. PARP1: Liaison of Chromatin Remodeling and Transcription. Cancers 2022, 14, 4162. [Google Scholar] [CrossRef] [PubMed]
- Vyas, S.; Chesarone-Cataldo, M.; Todorova, T.; Huang, Y.H.; Chang, P. A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat. Commun. 2013, 4, 2240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leung, A.K.; Vyas, S.; Rood, J.E.; Bhutkar, A.; Sharp, P.A.; Chang, P. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 2011, 42, 489–499. [Google Scholar] [CrossRef] [Green Version]
- Ryu, K.W.; Nandu, T.; Kim, J.; Challa, S.; DeBerardinis, R.J.; Kraus, W.L. Metabolic regulation of transcription through compartmentalized NAD(+) biosynthesis. Science 2018, 360, eaan5780. [Google Scholar] [CrossRef] [Green Version]
- Erener, S.; Hesse, M.; Kostadinova, R.; Hottiger, M.O. Poly(ADP-ribose)polymerase-1 (PARP1) controls adipogenic gene expression and adipocyte function. Mol. Endocrinol. 2012, 26, 79–86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- van Beek, L.; McClay, E.; Patel, S.; Schimpl, M.; Spagnolo, L.; Maia de Oliveira, T. PARP Power: A Structural Perspective on PARP1, PARP2, and PARP3 in DNA Damage Repair and Nucleosome Remodelling. Int. J. Mol. Sci. 2021, 22, 5112. [Google Scholar] [CrossRef] [PubMed]
- Challa, S.; Stokes, M.S.; Kraus, W.L. MARTs and MARylation in the Cytosol: Biological Functions, Mechanisms of Action, and Therapeutic Potential. Cells 2021, 10, 313. [Google Scholar] [CrossRef]
- Fehr, A.R.; Singh, S.A.; Kerr, C.M.; Mukai, S.; Higashi, H.; Aikawa, M. The impact of PARPs and ADP-ribosylation on inflammation and host-pathogen interactions. Genes. Dev. 2020, 34, 341–359. [Google Scholar] [CrossRef] [Green Version]
- Singh, N.; Poirier, G.; Cerutti, P. Tumor promoter phorbol-12-myristate-13-acetate induces poly ADP-ribosylation in human monocytes. Biochem. Biophys. Res. Commun. 1985, 126, 1208–1214. [Google Scholar] [CrossRef] [PubMed]
- Berton, G.; Sorio, C.; Laudanna, C.; Menegazzi, M.; Carcereri De Prati, A.; Suzuki, H. Activation of human monocyte-derived macrophages by interferon gamma is accompanied by increase of poly(ADP-ribose) polymerase activity. Biochim. Biophys. Acta 1991, 1091, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Heer, C.D.; Sanderson, D.J.; Voth, L.S.; Alhammad, Y.M.O.; Schmidt, M.S.; Trammell, S.A.J.; Perlman, S.; Cohen, M.S.; Fehr, A.R.; Brenner, C. Coronavirus infection and PARP expression dysregulate the NAD metabolome: An actionable component of innate immunity. J. Biol. Chem. 2020, 295, 17986–17996. [Google Scholar] [CrossRef]
- Tutt, A.N.J.; Garber, J.E.; Kaufman, B.; Viale, G.; Fumagalli, D.; Rastogi, P.; Gelber, R.D.; de Azambuja, E.; Fielding, A.; Balmana, J.; et al. Adjuvant Olaparib for Patients with BRCA1- or BRCA2-Mutated Breast Cancer. N. Engl. J. Med. 2021, 384, 2394–2405. [Google Scholar] [CrossRef]
- Tattersall, A.; Ryan, N.; Wiggans, A.J.; Rogozinska, E.; Morrison, J. Poly(ADP-ribose) polymerase (PARP) inhibitors for the treatment of ovarian cancer. Cochrane Database Syst. Rev. 2022, 2, CD007929. [Google Scholar] [CrossRef]
- Yarchoan, M.; Myzak, M.C.; Johnson, B.A., 3rd; De Jesus-Acosta, A.; Le, D.T.; Jaffee, E.M.; Azad, N.S.; Donehower, R.C.; Zheng, L.; Oberstein, P.E.; et al. Olaparib in combination with irinotecan, cisplatin, and mitomycin C in patients with advanced pancreatic cancer. Oncotarget 2017, 8, 44073–44081. [Google Scholar] [CrossRef]
- Hussain, M.; Mateo, J.; Fizazi, K.; Saad, F.; Shore, N.; Sandhu, S.; Chi, K.N.; Sartor, O.; Agarwal, N.; Olmos, D.; et al. Survival with Olaparib in Metastatic Castration-Resistant Prostate Cancer. N. Engl. J. Med. 2020, 383, 2345–2357. [Google Scholar] [CrossRef]
- Wang, L.; Wang, D.; Sonzogni, O.; Ke, S.; Wang, Q.; Thavamani, A.; Batalini, F.; Stopka, S.A.; Regan, M.S.; Vandal, S.; et al. PARP-inhibition reprograms macrophages toward an anti-tumor phenotype. Cell Rep. 2022, 41, 111462. [Google Scholar] [CrossRef] [PubMed]
- Demeny, M.A.; Virag, L. The PARP Enzyme Family and the Hallmarks of Cancer Part 2: Hallmarks Related to Cancer Host Interactions. Cancers 2021, 13, 2057. [Google Scholar] [CrossRef]
- Xue, T.; Zhang, X.; Xing, Y.; Liu, S.; Zhang, L.; Wang, X.; Yu, M. Advances About Immunoinflammatory Pathogenesis and Treatment in Diabetic Peripheral Neuropathy. Front. Pharmacol. 2021, 12, 748193. [Google Scholar] [CrossRef]
- Gupta, S.; You, P.; SenGupta, T.; Nilsen, H.; Sharma, K. Crosstalk between Different DNA Repair Pathways Contributes to Neurodegenerative Diseases. Biology 2021, 10, 163. [Google Scholar] [CrossRef]
- Krug, S.; Parveen, S.; Bishai, W.R. Host-Directed Therapies: Modulating Inflammation to Treat Tuberculosis. Front. Immunol. 2021, 12, 660916. [Google Scholar] [CrossRef] [PubMed]
- Siewe, N.; Friedman, A. Cancer therapy with immune checkpoint inhibitor and CSF-1 blockade: A mathematical model. J. Theor. Biol. 2023, 556, 111297. [Google Scholar] [CrossRef] [PubMed]
- Kasraie, S.; Werfel, T. Role of macrophages in the pathogenesis of atopic dermatitis. Mediat. Inflamm. 2013, 2013, 942375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, Y.; Hao, Y.; Gao, D.; Li, G.; Zhang, Z. Phenotype and function of macrophage polarization in monocrotaline-induced pulmonary arterial hypertension rat model. Physiol. Res. 2021, 70, 213–226. [Google Scholar] [CrossRef]
- Kumar, V.; Kumar, A.; Mir, K.U.I.; Yadav, V.; Chauhan, S.S. Pleiotropic role of PARP1: An overview. 3 Biotech. 2022, 12, 3. [Google Scholar] [CrossRef]
- Luscher, B.; Butepage, M.; Eckei, L.; Krieg, S.; Verheugd, P.; Shilton, B.H. ADP-Ribosylation, a Multifaceted Posttranslational Modification Involved in the Control of Cell Physiology in Health and Disease. Chem. Rev. 2018, 118, 1092–1136. [Google Scholar] [CrossRef]
- Dawicki-McKenna, J.M.; Langelier, M.F.; DeNizio, J.E.; Riccio, A.A.; Cao, C.D.; Karch, K.R.; McCauley, M.; Steffen, J.D.; Black, B.E.; Pascal, J.M. PARP-1 Activation Requires Local Unfolding of an Autoinhibitory Domain. Mol. Cell 2015, 60, 755–768. [Google Scholar] [CrossRef] [Green Version]
- Eustermann, S.; Wu, W.F.; Langelier, M.F.; Yang, J.C.; Easton, L.E.; Riccio, A.A.; Pascal, J.M.; Neuhaus, D. Structural Basis of Detection and Signaling of DNA Single-Strand Breaks by Human PARP-1. Mol. Cell 2015, 60, 742–754. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jumper, J.; Evans, R.; Pritzel, A.; Green, T.; Figurnov, M.; Ronneberger, O.; Tunyasuvunakool, K.; Bates, R.; Zidek, A.; Potapenko, A.; et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021, 596, 583–589. [Google Scholar] [CrossRef] [PubMed]
- Mendoza-Alvarez, H.; Alvarez-Gonzalez, R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J. Biol. Chem. 1993, 268, 22575–22580. [Google Scholar] [CrossRef] [PubMed]
- Pion, E.; Ullmann, G.M.; Ame, J.C.; Gerard, D.; de Murcia, G.; Bombarda, E. DNA-induced dimerization of poly(ADP-ribose) polymerase-1 triggers its activation. Biochemistry 2005, 44, 14670–14681. [Google Scholar] [CrossRef]
- Ali, A.A.E.; Timinszky, G.; Arribas-Bosacoma, R.; Kozlowski, M.; Hassa, P.O.; Hassler, M.; Ladurner, A.G.; Pearl, L.H.; Oliver, A.W. The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat. Struct. Mol. Biol. 2012, 19, 685–692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thomas, C.; Ji, Y.; Wu, C.; Datz, H.; Boyle, C.; MacLeod, B.; Patel, S.; Ampofo, M.; Currie, M.; Harbin, J.; et al. Hit and run versus long-term activation of PARP-1 by its different domains fine-tunes nuclear processes. Proc. Natl. Acad. Sci. USA 2019, 116, 9941–9946. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Langelier, M.F.; Planck, J.L.; Roy, S.; Pascal, J.M. Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: Structural and functional insights into DNA-dependent PARP-1 activity. J. Biol. Chem. 2011, 286, 10690–10701. [Google Scholar] [CrossRef] [Green Version]
- Thomas, C.J.; Kotova, E.; Andrake, M.; Adolf-Bryfogle, J.; Glaser, R.; Regnard, C.; Tulin, A.V. Kinase-mediated changes in nucleosome conformation trigger chromatin decondensation via poly(ADP-ribosyl)ation. Mol. Cell 2014, 53, 831–842. [Google Scholar] [CrossRef] [Green Version]
- Ioannidou, A.; Goulielmaki, E.; Garinis, G.A. DNA Damage: From Chronic Inflammation to Age-Related Deterioration. Front. Genet. 2016, 7, 187. [Google Scholar] [CrossRef] [Green Version]
- Bauer, M.; Goldstein, M.; Christmann, M.; Becker, H.; Heylmann, D.; Kaina, B. Human monocytes are severely impaired in base and DNA double-strand break repair that renders them vulnerable to oxidative stress. Proc. Natl. Acad. Sci. USA 2011, 108, 21105–21110. [Google Scholar] [CrossRef]
- Dharwal, V.; Naura, A.S. PARP-1 inhibition ameliorates elastase induced lung inflammation and emphysema in mice. Biochem. Pharmacol. 2018, 150, 24–34. [Google Scholar] [CrossRef]
- Dharwal, V.; Sandhir, R.; Naura, A.S. PARP-1 inhibition provides protection against elastase-induced emphysema by mitigating the expression of matrix metalloproteinases. Mol. Cell Biochem. 2019, 457, 41–49. [Google Scholar] [CrossRef]
- Kunze, F.A.; Bauer, M.; Komuczki, J.; Lanzinger, M.; Gunasekera, K.; Hopp, A.K.; Lehmann, M.; Becher, B.; Muller, A.; Hottiger, M.O. ARTD1 in Myeloid Cells Controls the IL-12/18-IFN-gamma Axis in a Model of Sterile Sepsis, Chronic Bacterial Infection, and Cancer. J. Immunol. 2019, 202, 1406–1416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Durkacz, B.W.; Omidiji, O.; Gray, D.A.; Shall, S. (ADP-ribose)n participates in DNA excision repair. Nature 1980, 283, 593–596. [Google Scholar] [CrossRef]
- Singla, S.; Kumar, V.; Jena, G. 3-aminobenzamide protects against colitis associated diabetes mellitus in male BALB/c mice: Role of PARP-1, NLRP3, SIRT-1, AMPK. Biochimie 2023, 211, 96–109. [Google Scholar] [CrossRef] [PubMed]
- Kovacs, D.; Vantus, V.B.; Vamos, E.; Kalman, N.; Schicho, R.; Gallyas, F.; Radnai, B. Olaparib: A Clinically Applied PARP Inhibitor Protects from Experimental Crohn’s Disease and Maintains Barrier Integrity by Improving Bioenergetics through Rescuing Glycolysis in Colonic Epithelial Cells. Oxid. Med. Cell. Longev. 2021, 2021, 7308897. [Google Scholar] [CrossRef] [PubMed]
- Gupte, R.; Nandu, T.; Kraus, W.L. Nuclear ADP-ribosylation drives IFNgamma-dependent STAT1alpha enhancer formation in macrophages. Nat. Commun. 2021, 12, 3931. [Google Scholar] [CrossRef] [PubMed]
- Gerner, R.R.; Klepsch, V.; Macheiner, S.; Arnhard, K.; Adolph, T.E.; Grander, C.; Wieser, V.; Pfister, A.; Moser, P.; Hermann-Kleiter, N.; et al. NAD metabolism fuels human and mouse intestinal inflammation. Gut 2018, 67, 1813–1823. [Google Scholar] [CrossRef] [Green Version]
- Mercurio, L.; Morelli, M.; Scarponi, C.; Scaglione, G.L.; Pallotta, S.; Avitabile, D.; Albanesi, C.; Madonna, S. Enhanced NAMPT-Mediated NAD Salvage Pathway Contributes to Psoriasis Pathogenesis by Amplifying Epithelial Auto-Inflammatory Circuits. Int. J. Mol. Sci. 2021, 22, 6860. [Google Scholar] [CrossRef]
- Arroyo, A.B.; Bernal-Carrion, M.; Canton-Sandoval, J.; Cabas, I.; Corbalan-Velez, R.; Martinez-Menchon, T.; Ferri, B.; Cayuela, M.L.; Garcia-Moreno, D.; Mulero, V. NAMPT and PARylation Are Involved in the Pathogenesis of Atopic Dermatitis. Int. J. Mol. Sci. 2023, 24, 7992. [Google Scholar] [CrossRef]
- Soldani, C.; Scovassi, A.I. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: An update. Apoptosis 2002, 7, 321–328. [Google Scholar] [CrossRef]
- Yang, Y.; Jiang, G.; Zhang, P.; Fan, J. Programmed cell death and its role in inflammation. Mil. Med. Res. 2015, 2, 12. [Google Scholar] [CrossRef] [Green Version]
- Huang, P.; Chen, G.; Jin, W.; Mao, K.; Wan, H.; He, Y. Molecular Mechanisms of Parthanatos and Its Role in Diverse Diseases. Int. J. Mol. Sci. 2022, 23, 7292. [Google Scholar] [CrossRef]
- Andrabi, S.A.; Dawson, T.M.; Dawson, V.L. Mitochondrial and nuclear cross talk in cell death: Parthanatos. Ann. N. Y Acad. Sci. 2008, 1147, 233–241. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Wang, C.; Tian, Y.; Zhang, F.; Xu, W.; Li, X.; Shu, Z.; Wang, Y.; Huang, K.; Huang, D. Inhibition of Poly(ADP-Ribose) Polymerase-1 Protects Chronic Alcoholic Liver Injury. Am. J. Pathol. 2016, 186, 3117–3130. [Google Scholar] [CrossRef] [Green Version]
- Cohen-Armon, M. The Modified Phenanthridine PJ34 Unveils an Exclusive Cell-Death Mechanism in Human Cancer Cells. Cancers 2020, 12, 1628. [Google Scholar] [CrossRef] [PubMed]
- Erener, S.; Petrilli, V.; Kassner, I.; Minotti, R.; Castillo, R.; Santoro, R.; Hassa, P.O.; Tschopp, J.; Hottiger, M.O. Inflammasome-activated caspase 7 cleaves PARP1 to enhance the expression of a subset of NF-kappaB target genes. Mol. Cell 2012, 46, 200–211. [Google Scholar] [CrossRef] [Green Version]
- Martinez-Morcillo, F.J.; Canton-Sandoval, J.; Martinez-Navarro, F.J.; Cabas, I.; Martinez-Vicente, I.; Armistead, J.; Hatzold, J.; Lopez-Munoz, A.; Martinez-Menchon, T.; Corbalan-Velez, R.; et al. NAMPT-derived NAD+ fuels PARP1 to promote skin inflammation through parthanatos cell death. PLoS Biol. 2021, 19, e3001455. [Google Scholar] [CrossRef] [PubMed]
- Lopez, M.; Tanowitz, H.B.; Garg, N.J. Pathogenesis of Chronic Chagas Disease: Macrophages, Mitochondria, and Oxidative Stress. Curr. Clin. Microbiol. Rep. 2018, 5, 45–54. [Google Scholar] [CrossRef]
- Bonney, K.M.; Luthringer, D.J.; Kim, S.A.; Garg, N.J.; Engman, D.M. Pathology and Pathogenesis of Chagas Heart Disease. Annu. Rev. Pathol. 2019, 14, 421–447. [Google Scholar] [CrossRef]
- Ba, X.; Gupta, S.; Davidson, M.; Garg, N.J. Trypanosoma cruzi induces the reactive oxygen species-PARP-1-RelA pathway for up-regulation of cytokine expression in cardiomyocytes. J. Biol. Chem. 2010, 285, 11596–11606. [Google Scholar] [CrossRef] [Green Version]
- Wen, J.J.; Yin, Y.W.; Garg, N.J. PARP1 depletion improves mitochondrial and heart function in Chagas disease: Effects on POLG dependent mtDNA maintenance. PLoS Pathog. 2018, 14, e1007065. [Google Scholar] [CrossRef] [Green Version]
- Florentino, P.T.V.; Vitorino, F.N.L.; Mendes, D.; da Cunha, J.P.C.; Menck, C.F.M. Trypanosoma cruzi infection changes the chromatin proteome profile of infected human cells. J. Proteomics 2023, 272, 104773. [Google Scholar] [CrossRef] [PubMed]
- Florentino, P.T.V.; Mendes, D.; Vitorino, F.N.L.; Martins, D.J.; Cunha, J.P.C.; Mortara, R.A.; Menck, C.F.M. DNA damage and oxidative stress in human cells infected by Trypanosoma cruzi. PLoS Pathog. 2021, 17, e1009502. [Google Scholar] [CrossRef]
- Choudhuri, S.; Garg, N.J. PARP1-cGAS-NF-kappaB pathway of proinflammatory macrophage activation by extracellular vesicles released during Trypanosoma cruzi infection and Chagas disease. PLoS Pathog. 2020, 16, e1008474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Macaluso, G.; Grippi, F.; Di Bella, S.; Blanda, V.; Gucciardi, F.; Torina, A.; Guercio, A.; Cannella, V. A Review on the Immunological Response against Trypanosoma cruzi. Pathogens 2023, 12, 282. [Google Scholar] [CrossRef] [PubMed]
- von Lukowicz, T.; Hassa, P.O.; Lohmann, C.; Boren, J.; Braunersreuther, V.; Mach, F.; Odermatt, B.; Gersbach, M.; Camici, G.G.; Stahli, B.E.; et al. PARP1 is required for adhesion molecule expression in atherogenesis. Cardiovasc. Res. 2008, 78, 158–166. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, W. Bidirectional regulation role of PARP-1 in high glucose-induced endothelial injury. Exp. Cell Res. 2022, 421, 113400. [Google Scholar] [CrossRef]
- Wei, L.; Yang, C.; Li, K.Q.; Zhong, C.L.; Sun, Z.Y. 3-Aminobenzamide protects against cerebral artery injury and inflammation in rats with intracranial aneurysms. Pharmazie 2019, 74, 142–146. [Google Scholar] [CrossRef]
- Daugherty, M.D.; Young, J.M.; Kerns, J.A.; Malik, H.S. Rapid evolution of PARP genes suggests a broad role for ADP-ribosylation in host-virus conflicts. PLoS Genet. 2014, 10, e1004403. [Google Scholar] [CrossRef] [Green Version]
- Iwata, H.; Goettsch, C.; Sharma, A.; Ricchiuto, P.; Goh, W.W.; Halu, A.; Yamada, I.; Yoshida, H.; Hara, T.; Wei, M.; et al. PARP9 and PARP14 cross-regulate macrophage activation via STAT1 ADP-ribosylation. Nat. Commun. 2016, 7, 12849. [Google Scholar] [CrossRef] [Green Version]
- Higashi, H.; Maejima, T.; Lee, L.H.; Yamazaki, Y.; Hottiger, M.O.; Singh, S.A.; Aikawa, M. A Study into the ADP-Ribosylome of IFN-gamma-Stimulated THP-1 Human Macrophage-like Cells Identifies ARTD8/PARP14 and ARTD9/PARP9 ADP-Ribosylation. J. Proteome Res. 2019, 18, 1607–1622. [Google Scholar] [CrossRef] [Green Version]
- Jin, U.H.; Cheng, Y.; Park, H.; Davidson, L.A.; Callaway, E.S.; Chapkin, R.S.; Jayaraman, A.; Asante, A.; Allred, C.; Weaver, E.A.; et al. Short Chain Fatty Acids Enhance Aryl Hydrocarbon (Ah) Responsiveness in Mouse Colonocytes and Caco-2 Human Colon Cancer Cells. Sci. Rep. 2017, 7, 10163. [Google Scholar] [CrossRef] [Green Version]
- Szanto, M.; Gupte, R.; Kraus, W.L.; Pacher, P.; Bai, P. PARPs in lipid metabolism and related diseases. Prog. Lipid Res. 2021, 84, 101117. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.C.; Hsiao, C.C.; Chen, T.W.; Wu, C.C.; Chao, T.Y.; Leung, S.Y.; Eng, H.L.; Lee, C.P.; Wang, T.Y.; Lin, M.C. Whole Genome DNA Methylation Analysis of Active Pulmonary Tuberculosis Disease Identifies Novel Epigenotypes: PARP9/miR-505/RASGRP4/GNG12 Gene Methylation and Clinical Phenotypes. Int. J. Mol. Sci. 2020, 21, 3180. [Google Scholar] [CrossRef] [PubMed]
- Thirunavukkarasu, S.; Ahmed, M.; Rosa, B.A.; Boothby, M.; Cho, S.H.; Rangel-Moreno, J.; Mbandi, S.K.; Schreiber, V.; Gupta, A.; Zuniga, J.; et al. Poly(ADP-ribose) polymerase 9 mediates early protection against Mycobacterium tuberculosis infection by regulating type I IFN production. J. Clin. Investig. 2023, 133, e158630. [Google Scholar] [CrossRef] [PubMed]
- Xing, J.; Zhang, A.; Du, Y.; Fang, M.; Minze, L.J.; Liu, Y.J.; Li, X.C.; Zhang, Z. Identification of poly(ADP-ribose) polymerase 9 (PARP9) as a noncanonical sensor for RNA virus in dendritic cells. Nat. Commun. 2021, 12, 2681. [Google Scholar] [CrossRef]
- Han, J.; Chen, C.; Wang, C.; Qin, N.; Huang, M.; Ma, Z.; Zhu, M.; Dai, J.; Jiang, Y.; Ma, H.; et al. Transcriptome-wide association study for persistent hepatitis B virus infection and related hepatocellular carcinoma. Liver Int. 2020, 40, 2117–2127. [Google Scholar] [CrossRef]
- Liang, T.J. Hepatitis B: The virus and disease. Hepatology 2009, 49, S13–S21. [Google Scholar] [CrossRef] [Green Version]
- Eckei, L.; Krieg, S.; Butepage, M.; Lehmann, A.; Gross, A.; Lippok, B.; Grimm, A.R.; Kummerer, B.M.; Rossetti, G.; Luscher, B.; et al. The conserved macrodomains of the non-structural proteins of Chikungunya virus and other pathogenic positive strand RNA viruses function as mono-ADP-ribosylhydrolases. Sci. Rep. 2017, 7, 41746. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez, G.J.; Ramirez-Mejia, J.M.; Urcuqui-Inchima, S. Transcriptional and post-transcriptional mechanisms that regulate the genetic program in Zika virus-infected macrophages. Int. J. Biochem. Cell Biol. 2022, 153, 106312. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, M.B.; Johns, M.; Cao, J.; Liu, Y.; Yu, S.C.; Hyde, G.D.; Laffan, M.A.; Marchese, F.P.; Cho, S.H.; Clark, A.R.; et al. PARP-14 combines with tristetraprolin in the selective posttranscriptional control of macrophage tissue factor expression. Blood 2014, 124, 3646–3655. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mehrotra, P.; Riley, J.P.; Patel, R.; Li, F.; Voss, L.; Goenka, S. PARP-14 functions as a transcriptional switch for Stat6-dependent gene activation. J. Biol. Chem. 2011, 286, 1767–1776. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holbourn, K.P.; Shone, C.C.; Acharya, K.R. A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J. 2006, 273, 4579–4593. [Google Scholar] [CrossRef]
- Atasheva, S.; Frolova, E.I.; Frolov, I. Interferon-stimulated poly(ADP-Ribose) polymerases are potent inhibitors of cellular translation and virus replication. J. Virol. 2014, 88, 2116–2130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.; Mao, D.; Roswit, W.T.; Jin, X.; Patel, A.C.; Patel, D.A.; Agapov, E.; Wang, Z.; Tidwell, R.M.; Atkinson, J.J.; et al. PARP9-DTX3L ubiquitin ligase targets host histone H2BJ and viral 3C protease to enhance interferon signaling and control viral infection. Nat. Immunol. 2015, 16, 1215–1227. [Google Scholar] [CrossRef] [PubMed]
- Gagne, J.P.; Isabelle, M.; Lo, K.S.; Bourassa, S.; Hendzel, M.J.; Dawson, V.L.; Dawson, T.M.; Poirier, G.G. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 2008, 36, 6959–6976. [Google Scholar] [CrossRef] [Green Version]
- Catara, G.; Grimaldi, G.; Schembri, L.; Spano, D.; Turacchio, G.; Lo Monte, M.; Beccari, A.R.; Valente, C.; Corda, D. PARP1-produced poly-ADP-ribose causes the PARP12 translocation to stress granules and impairment of Golgi complex functions. Sci. Rep. 2017, 7, 14035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Isabelle, M.; Gagne, J.P.; Gallouzi, I.E.; Poirier, G.G. Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation. J. Cell Sci. 2012, 125, 4555–4566. [Google Scholar] [CrossRef] [Green Version]
- Leung, A.; Todorova, T.; Ando, Y.; Chang, P. Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol. 2012, 9, 542–548. [Google Scholar] [CrossRef] [Green Version]
- Karras, G.I.; Kustatscher, G.; Buhecha, H.R.; Allen, M.D.; Pugieux, C.; Sait, F.; Bycroft, M.; Ladurner, A.G. The macro domain is an ADP-ribose binding module. EMBO J. 2005, 24, 1911–1920. [Google Scholar] [CrossRef] [Green Version]
- Egloff, M.P.; Malet, H.; Putics, A.; Heinonen, M.; Dutartre, H.; Frangeul, A.; Gruez, A.; Campanacci, V.; Cambillau, C.; Ziebuhr, J.; et al. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J. Virol. 2006, 80, 8493–8502. [Google Scholar] [CrossRef] [Green Version]
- Eriksson, K.K.; Cervantes-Barragan, L.; Ludewig, B.; Thiel, V. Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1’’-phosphatase, a viral function conserved in the alpha-like supergroup. J. Virol. 2008, 82, 12325–12334. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuri, T.; Eriksson, K.K.; Putics, A.; Zust, R.; Snijder, E.J.; Davidson, A.D.; Siddell, S.G.; Thiel, V.; Ziebuhr, J.; Weber, F. The ADP-ribose-1’’-monophosphatase domains of severe acute respiratory syndrome coronavirus and human coronavirus 229E mediate resistance to antiviral interferon responses. J. Gen. Virol. 2011, 92, 1899–1905. [Google Scholar] [CrossRef] [PubMed]
- Fehr, A.R.; Athmer, J.; Channappanavar, R.; Phillips, J.M.; Meyerholz, D.K.; Perlman, S. The nsp3 macrodomain promotes virulence in mice with coronavirus-induced encephalitis. J. Virol. 2015, 89, 1523–1536. [Google Scholar] [CrossRef] [Green Version]
- Voth, L.S.; O’Connor, J.J.; Kerr, C.M.; Doerger, E.; Schwarting, N.; Sperstad, P.; Johnson, D.K.; Fehr, A.R. Unique Mutations in the Murine Hepatitis Virus Macrodomain Differentially Attenuate Virus Replication, Indicating Multiple Roles for the Macrodomain in Coronavirus Replication. J. Virol. 2021, 95, e0076621. [Google Scholar] [CrossRef]
- Grunewald, M.E.; Chen, Y.; Kuny, C.; Maejima, T.; Lease, R.; Ferraris, D.; Aikawa, M.; Sullivan, C.S.; Perlman, S.; Fehr, A.R. The coronavirus macrodomain is required to prevent PARP-mediated inhibition of virus replication and enhancement of IFN expression. PLoS Pathog. 2019, 15, e1007756. [Google Scholar] [CrossRef] [Green Version]
- Fehr, A.R.; Channappanavar, R.; Jankevicius, G.; Fett, C.; Zhao, J.; Athmer, J.; Meyerholz, D.K.; Ahel, I.; Perlman, S. The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection. mBio 2016, 7, e01721-16. [Google Scholar] [CrossRef] [Green Version]
- Hoch, N.C. Host ADP-ribosylation and the SARS-CoV-2 macrodomain. Biochem. Soc. Trans. 2021, 49, 1711–1721. [Google Scholar] [CrossRef]
- Cantini, F.; Banci, L.; Altincekic, N.; Bains, J.K.; Dhamotharan, K.; Fuks, C.; Furtig, B.; Gande, S.L.; Hargittay, B.; Hengesbach, M.; et al. (1)H, (13)C, and (15)N backbone chemical shift assignments of the apo and the ADP-ribose bound forms of the macrodomain of SARS-CoV-2 non-structural protein 3b. Biomol. NMR Assign. 2020, 14, 339–346. [Google Scholar] [CrossRef]
- Michalska, K.; Kim, Y.; Jedrzejczak, R.; Maltseva, N.I.; Stols, L.; Endres, M.; Joachimiak, A. Crystal structures of SARS-CoV-2 ADP-ribose phosphatase: From the apo form to ligand complexes. IUCrJ 2020, 7, 814–824. [Google Scholar] [CrossRef] [PubMed]
- Lin, M.H.; Chang, S.C.; Chiu, Y.C.; Jiang, B.C.; Wu, T.H.; Hsu, C.H. Structural, Biophysical, and Biochemical Elucidation of the SARS-CoV-2 Nonstructural Protein 3 Macro Domain. ACS Infect. Dis. 2020, 6, 2970–2978. [Google Scholar] [CrossRef]
- Correy, G.J.; Kneller, D.W.; Phillips, G.; Pant, S.; Russi, S.; Cohen, A.E.; Meigs, G.; Holton, J.M.; Gahbauer, S.; Thompson, M.C.; et al. The mechanisms of catalysis and ligand binding for the SARS-CoV-2 NSP3 macrodomain from neutron and x-ray diffraction at room temperature. Sci. Adv. 2022, 8, eabo5083. [Google Scholar] [CrossRef]
- Schuller, M.; Correy, G.J.; Gahbauer, S.; Fearon, D.; Wu, T.; Diaz, R.E.; Young, I.D.; Carvalho Martins, L.; Smith, D.H.; Schulze-Gahmen, U.; et al. Fragment binding to the Nsp3 macrodomain of SARS-CoV-2 identified through crystallographic screening and computational docking. Sci. Adv. 2021, 7, eabf8711. [Google Scholar] [CrossRef]
- Claverie, J.M. A Putative Role of de-Mono-ADP-Ribosylation of STAT1 by the SARS-CoV-2 Nsp3 Protein in the Cytokine Storm Syndrome of COVID-19. Viruses 2020, 12, 646. [Google Scholar] [CrossRef] [PubMed]
- Alhammad, Y.M.O.; Kashipathy, M.M.; Roy, A.; Gagne, J.P.; McDonald, P.; Gao, P.; Nonfoux, L.; Battaile, K.P.; Johnson, D.K.; Holmstrom, E.D.; et al. The SARS-CoV-2 Conserved Macrodomain Is a Mono-ADP-Ribosylhydrolase. J. Virol. 2021, 95, 10–1128. [Google Scholar] [CrossRef]
- Brosey, C.A.; Houl, J.H.; Katsonis, P.; Balapiti-Modarage, L.P.F.; Bommagani, S.; Arvai, A.; Moiani, D.; Bacolla, A.; Link, T.; Warden, L.S.; et al. Targeting SARS-CoV-2 Nsp3 macrodomain structure with insights from human poly(ADP-ribose) glycohydrolase (PARG) structures with inhibitors. Prog. Biophys. Mol. Biol. 2021, 163, 171–186. [Google Scholar] [CrossRef] [PubMed]
- Chea, C.; Lee, D.Y.; Kato, J.; Ishiwata-Endo, H.; Moss, J. Macrodomain Mac1 of SARS-CoV-2 Nonstructural Protein 3 Hydrolyzes Diverse ADP-ribosylated Substrates. bioRxiv 2023. [Google Scholar] [CrossRef]
- Russo, L.C.; Tomasin, R.; Matos, I.A.; Manucci, A.C.; Sowa, S.T.; Dale, K.; Caldecott, K.W.; Lehtio, L.; Schechtman, D.; Meotti, F.C.; et al. The SARS-CoV-2 Nsp3 macrodomain reverses PARP9/DTX3L-dependent ADP-ribosylation induced by interferon signaling. J. Biol. Chem. 2021, 297, 101041. [Google Scholar] [CrossRef]
- Alhammad, Y.M.; Parthasarathy, S.; Ghimire, R.; O’Connor, J.J.; Kerr, C.M.; Pfannenstiel, J.J.; Chanda, D.; Miller, C.A.; Unckless, R.L.; Zuniga, S.; et al. SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in mice. bioRxiv 2023. [Google Scholar] [CrossRef]
- Cohen, M.S. Interplay between compartmentalized NAD(+) synthesis and consumption: A focus on the PARP family. Genes. Dev. 2020, 34, 254–262. [Google Scholar] [CrossRef] [PubMed]
- Gupte, R.; Liu, Z.; Kraus, W.L. PARPs and ADP-ribosylation: Recent advances linking molecular functions to biological outcomes. Genes. Dev. 2017, 31, 101–126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dantoft, W.; Robertson, K.A.; Watkins, W.J.; Strobl, B.; Ghazal, P. Metabolic Regulators Nampt and Sirt6 Serially Participate in the Macrophage Interferon Antiviral Cascade. Front. Microbiol. 2019, 10, 355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Habeichi, N.J.; Tannous, C.; Yabluchanskiy, A.; Altara, R.; Mericskay, M.; Booz, G.W.; Zouein, F.A. Insights into the modulation of the interferon response and NAD(+) in the context of COVID-19. Int. Rev. Immunol. 2022, 41, 464–474. [Google Scholar] [CrossRef] [PubMed]
- Block, T.; Kuo, J. Rationale for Nicotinamide Adenine Dinucleotide (NAD+) Metabolome Disruption as a Pathogenic Mechanism of Post-Acute COVID-19 Syndrome. Clin. Pathol. 2022, 15, 2632010X221106986. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Deng, Y.; Pang, H.; Ma, T.; Ye, Q.; Chen, Q.; Chen, H.; Hu, Z.; Qin, C.F.; Xu, Z. Treatment of SARS-CoV-2-induced pneumonia with NAD(+) and NMN in two mouse models. Cell Discov. 2022, 8, 38. [Google Scholar] [CrossRef]
- Zhai, L.H.; Chen, K.F.; Hao, B.B.; Tan, M.J. Proteomic characterization of post-translational modifications in drug discovery. Acta Pharmacol. Sin. 2022, 43, 3112–3129. [Google Scholar] [CrossRef]
- Gehrig, P.M.; Nowak, K.; Panse, C.; Leutert, M.; Grossmann, J.; Schlapbach, R.; Hottiger, M.O. Gas-Phase Fragmentation of ADP-Ribosylated Peptides: Arginine-Specific Side-Chain Losses and Their Implication in Database Searches. J. Am. Soc. Mass. Spectrom. 2021, 32, 157–168. [Google Scholar] [CrossRef]
- Zee, B.M.; Garcia, B.A. Electron transfer dissociation facilitates sequencing of adenosine diphosphate-ribosylated peptides. Anal. Chem. 2010, 82, 28–31. [Google Scholar] [CrossRef]
- Rosenthal, F.; Nanni, P.; Barkow-Oesterreicher, S.; Hottiger, M.O. Optimization of LTQ-Orbitrap Mass Spectrometer Parameters for the Identification of ADP-Ribosylation Sites. J. Proteome Res. 2015, 14, 4072–4079. [Google Scholar] [CrossRef]
- Singh, S.A.; Kuraoka, S.; Pestana, D.V.S.; Nasir, W.; Delanghe, B.; Aikawa, M. The RiboMaP Spectral Annotation Method Applied to Various ADP-Ribosylome Studies Including INF-gamma-Stimulated Human Cells and Mouse Tissues. Front. Cardiovasc. Med. 2022, 9, 851351. [Google Scholar] [CrossRef]
- Anagho, H.A.; Elsborg, J.D.; Hendriks, I.A.; Buch-Larsen, S.C.; Nielsen, M.L. Characterizing ADP-Ribosylation Sites Using Af1521 Enrichment Coupled to ETD-Based Mass Spectrometry. Methods Mol. Biol. 2023, 2609, 251–270. [Google Scholar] [CrossRef]
- Buch-Larsen, S.C.; Hendriks, I.A.; Lodge, J.M.; Rykaer, M.; Furtwangler, B.; Shishkova, E.; Westphall, M.S.; Coon, J.J.; Nielsen, M.L. Mapping Physiological ADP-Ribosylation Using Activated Ion Electron Transfer Dissociation. Cell Rep. 2020, 32, 108176. [Google Scholar] [CrossRef] [PubMed]
- Hendriks, I.A.; Larsen, S.C.; Nielsen, M.L. An Advanced Strategy for Comprehensive Profiling of ADP-ribosylation Sites Using Mass Spectrometry-based Proteomics. Mol. Cell Proteom. 2019, 18, 1010–1026. [Google Scholar] [CrossRef] [PubMed]
- Daniels, C.M.; Ong, S.E.; Leung, A.K.L. ADP-Ribosylated Peptide Enrichment and Site Identification: The Phosphodiesterase-Based Method. Methods Mol. Biol. 2017, 1608, 79–93. [Google Scholar] [CrossRef] [Green Version]
- Nowak, K.; Rosenthal, F.; Karlberg, T.; Butepage, M.; Thorsell, A.G.; Dreier, B.; Grossmann, J.; Sobek, J.; Imhof, R.; Luscher, B.; et al. Engineering Af1521 improves ADP-ribose binding and identification of ADP-ribosylated proteins. Nat. Commun. 2020, 11, 5199. [Google Scholar] [CrossRef] [PubMed]
- Vivelo, C.A.; Wat, R.; Agrawal, C.; Tee, H.Y.; Leung, A.K. ADPriboDB: The database of ADP-ribosylated proteins. Nucleic Acids Res. 2017, 45, D204–D209. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ayyappan, V.; Wat, R.; Barber, C.; Vivelo, C.A.; Gauch, K.; Visanpattanasin, P.; Cook, G.; Sazeides, C.; Leung, A.K.L. ADPriboDB 2.0: An updated database of ADP-ribosylated proteins. Nucleic Acids Res. 2021, 49, D261–D265. [Google Scholar] [CrossRef] [PubMed]
- Kuraoka, S.; Higashi, H.; Yanagihara, Y.; Sonawane, A.R.; Mukai, S.; Mlynarchik, A.K.; Whelan, M.C.; Hottiger, M.O.; Nasir, W.; Delanghe, B.; et al. A Novel Spectral Annotation Strategy Streamlines Reporting of Mono-ADP-ribosylated Peptides Derived from Mouse Liver and Spleen in Response to IFN-gamma. Mol. Cell Proteomics 2022, 21, 100153. [Google Scholar] [CrossRef]
- Collier, R.J.; Cole, H.A. Diphtheria toxin subunit active in vitro. Science 1969, 164, 1179–1181. [Google Scholar] [CrossRef]
- Hebert, A.S.; Prasad, S.; Belford, M.W.; Bailey, D.J.; McAlister, G.C.; Abbatiello, S.E.; Huguet, R.; Wouters, E.R.; Dunyach, J.J.; Brademan, D.R.; et al. Comprehensive Single-Shot Proteomics with FAIMS on a Hybrid Orbitrap Mass Spectrometer. Anal. Chem. 2018, 90, 9529–9537. [Google Scholar] [CrossRef]
Enzyme | Activity | Disease/Biological Process(s) |
---|---|---|
PARP1/ARTD1 | PARylation, MARylation, or non-catalytic activity | Emphysema/Chronic lung inflammation [49,50] H. pylori infection [51] Colitis/Inflammatory bowel diseases [53,54,56] Psoriasis [57,66] Atopic dermatitis [58] Alcoholic liver injury [63] Chagas heart disease [69,70,71,72] |
PARP7/ARTD14 | MARylation | SARS-CoV-2 infection [23] Colitis/Inflammatory bowel diseases [53,54,56] |
PARP9/ARTD9 | MARylation | Pulmonary tuberculosis [83,84] RNA-viruses infections [85,86] Atherosclerosis/arterial inflammation [79,80] SARS-CoV-2 infection [117] |
PARP10/ARTD10 | MARylation | SARS-CoV-2 infection [23] Arboviruses infections [88] |
PARP12/ARTD12 | MARylation | Assembly and maintenance of stress granules [15] SARS-CoV-2 infection [23] |
PARP13/ARTD13 | Non-catalytic activity | Assembly and maintenance of stress granules [15] |
PARP14/ARTD8 | MARylation | Atopic dermatitis (Clinical Trial No.: NCT05215808) SARS-CoV-2 infection [23] Atherosclerosis/arterial inflammation [79,80,90,91] Arboviruses infections [88,89] |
PARP15/ARTD7 | MARylation | Assembly and maintenance of stress granules [15] Arboviruses infections [88] |
PARG | Hydrolysis (PAR) | Assembly and maintenance of stress granules [15,98] |
Macrodomain 1 (nsp3) | Hydrolysis (MAR) | SARS-CoV-2 infection [114,117,118] |
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Santinelli-Pestana, D.V.; Aikawa, E.; Singh, S.A.; Aikawa, M. PARPs and ADP-Ribosylation in Chronic Inflammation: A Focus on Macrophages. Pathogens 2023, 12, 964. https://doi.org/10.3390/pathogens12070964
Santinelli-Pestana DV, Aikawa E, Singh SA, Aikawa M. PARPs and ADP-Ribosylation in Chronic Inflammation: A Focus on Macrophages. Pathogens. 2023; 12(7):964. https://doi.org/10.3390/pathogens12070964
Chicago/Turabian StyleSantinelli-Pestana, Diego V., Elena Aikawa, Sasha A. Singh, and Masanori Aikawa. 2023. "PARPs and ADP-Ribosylation in Chronic Inflammation: A Focus on Macrophages" Pathogens 12, no. 7: 964. https://doi.org/10.3390/pathogens12070964