细菌ADP-核糖基水解酶的结构基础与催化机理
作者:
基金项目:

国家自然科学基金(82225028,82172287,31900879,32171265);国家重点研发计划(2021YFC2301403)


Structural basis and catalytic mechanism of bacterial ADP-ribosyl hydrolases
Author:
  • 摘要
  • | |
  • 访问统计
  • |
  • 参考文献 [69]
  • | | | |
  • 文章评论
    摘要:

    ADP-核糖基化(adenosine diphosphate-ribosylation,ADPr)修饰是由ADP-核糖基转移酶(adenosine diphosphate-ribosyltransferases,ARTs)和ADP-核糖基水解酶(adenosine diphosphate-ribosylhydrolases,ARHs)共同催化的可逆化翻译后修饰,广泛地分布于真核生物和原核生物中。ARHs是一类能够逆转特定氨基酸残基或DNA、RNA特定位点/序列ADPr修饰的关键酶,通过调控细菌或宿主的生理代谢、信号传导和基因表达调控等关键生命过程,在细菌物种间/种内的竞争、应激反应和致病性中发挥重要作用。鉴于细菌ARHs相关研究领域近期取得了一定的进展,本综述从其分类、结构特点以及催化机制角度对其进行系统总结,以期为深入理解细菌ARHs的作用机理及其在细菌生命过程的重要生物学功能提供帮助。

    Abstract:

    Adenosine diphosphate-ribosylation (ADPr) is a reversible post-translational modification that is catalyzed by adenosine diphosphate-ribosyltransferases (ARTs) and adenosine diphosphate- ribosylhydrolases (ARHs), and it widely occurs in eukaryotes and prokaryotes. ARHs are a class of key enzymes that can reverse ADPr modification of specific amino acid residues or specific sites/sequences of DNA and RNA. They can regulate the physiological metabolism, signal transduction, gene expression, and other key life processes in bacteria or hosts, playing an important role in the inter/intraspecific competition, stress responses, and pathogenicity of bacteria. This article reviews the classification, structural characteristics, and catalytic mechanisms of bacterial ARHs, aiming to enrich our understanding about the catalytic mechanisms and biological functions of ARHs in bacterial life.

    参考文献
    [1] MIKOLČEVIĆ P, HLOUŠEK-KASUN A, AHEL I, MIKOČ A. ADP-ribosylation systems in bacteria and viruses[J]. Computational and Structural Biotechnology Journal, 2021, 19: 2366-2383.
    [2] SUSKIEWICZ MJ, PROKHOROVA E, RACK JGM, AHEL I. ADP-ribosylation from molecular mechanisms to therapeutic implications[J]. Cell, 2023, 186(21): 4475-4495.
    [3] ARAVIND L, ZHANG DP, de SOUZA RF, ANAND S, IYER LM. The natural history of ADP-ribosyltransferases and the ADP-ribosylation system[J]. Current Topics in Microbiology and Immunology, 2015, 384: 3-32.
    [4] RACK JGM, PALAZZO L, AHEL I. (ADP-ribosyl)hydrolases: structure, function, and biology[J]. Genes & Development, 2020, 34(5/6): 263-284.
    [5] ALVAREZ-GONZALEZ R, ALTHAUS FR. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents[J]. Mutation Research/DNA Repair, 1989, 218(2): 67-74.
    [6] RACK JGM, PERINA D, AHEL I. Macrodomains: structure, function, evolution, and catalytic activities[J]. Annual Review of Biochemistry, 2016, 85: 431-454.
    [7] BROCHU G, DUCHAINE C, THIBEAULT L, LAGUEUX J, SHAH GM, POIRIER GG. Mode of action of poly(ADP-ribose) glycohydrolase[J]. Biochimica et Biophysica Acta, 1994, 1219(2): 342-350.
    [8] TING SY, BOSCH DE, MANGIAMELI SM, RADEY MC, HUANG S, PARK YJ, KELLY KA, FILIP SK, GOO YA, ENG JK, ALLAIRE M, VEESLER D, WIGGINS PA, PETERSON SB, MOUGOUS JD. Bifunctional immunity proteins protect bacteria against FtsZ-targeting ADP-ribosylating toxins[J]. Cell, 2018, 175(5): 1380-1392.e14.
    [9] JANKEVICIUS G, ARIZA A, AHEL M, AHEL I. The toxin-antitoxin system DarTG catalyzes reversible ADP-ribosylation of DNA[J]. Molecular Cell, 2016, 64(6): 1109-1116.
    [10] ZHANG WC, WANG CL, SONG Y, SHAO C, ZHANG X, ZANG JY. Structural insights into the mechanism of Escherichia coli YmdB: a 2'-O-acetyl-ADP-ribose deacetylase[J]. Journal of Structural Biology, 2015, 192(3): 478-486.
    [11] APPEL CD, FELD GK, WALLACE BD, WILLIAMS RS. Structure of the sirtuin-linked macrodomain SAV0325 from Staphylococcus aureus[J]. Protein Science, 2016, 25(9): 1682-1691.
    [12] KARRAS GI, KUSTATSCHER G, BUHECHA HR, ALLEN MD, PUGIEUX C, SAIT F, BYCROFT M, LADURNER AG. The macro domain is an ADP-ribose binding module[J]. EMBO Journal, 2005, 24(11): 1911-1920.
    [13] FORST AH, KARLBERG T, HERZOG N, THORSELL AG, GROSS A, FEIJS KLH, VERHEUGD P, KURSULA P, NIJMEIJER B, KREMMER E, KLEINE H, LADURNER AG, SCHÜLER H, LÜSCHER B. Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains[J]. Structure, 2013, 21(3): 462-475.
    [14] RACK JGM, ZORZINI V, ZHU ZH, SCHULLER M, AHEL D, AHEL I. Viral macrodomains: a structural and evolutionary assessment of the pharmacological potential[J]. Open Biology, 2020, 10(11): 200237.
    [15] FU JQ, LI PW, GUAN HX, HUANG D, SONG L, OUYANG SY, LUO ZQ. Legionella pneumophila temporally regulates the activity of ADP/ATP translocases by reversible ADP-ribosylation[J]. mLife, 2022, 1(1): 51-65.
    [16] ZHANG ZR, FU JQ, RACK JGM, LI C, VOORNEVELD J, FILIPPOV DV, AHEL I, LUO ZQ, DAS C. Legionella metaeffector MavL reverses ubiquitin ADP-ribosylation via a conserved arginine-specific macrodomain[J]. Nature Communications, 2024, 15(1): 2452.
    [17] BERTHOLD CL, WANG H, NORDLUND S, HÖGBOM M. Mechanism of ADP-ribosylation removal revealed by the structure and ligand complexes of the dimanganese mono-ADP-ribosylhydrolase DraG[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(34): 14247-14252.
    [18] LI XD, HUERGO LF, GASPERINA A, PEDROSA FO, MERRICK M, WINKLER FK. Crystal structure of dinitrogenase reductase-activating glycohydrolase (DRAG) reveals conservation in the ADP-ribosylhydrolase fold and specific features in the ADP-ribose-binding pocket[J]. Journal of Molecular Biology, 2009, 390(4): 737-746.
    [19] LAMBRECHT MJ, BRICHACEK M, BARKAUSKAITE E, ARIZA A, AHEL I, HERGENROTHER PJ. Synthesis of dimeric ADP-ribose and its structure with human poly(ADP-ribose) glycohydrolase[J]. Journal of the American Chemical Society, 2015, 137(10): 3558-3564.
    [20] ZAPATA-PÉREZ R, GIL-ORTIZ F, MARTÍNEZ-MOÑINO AB, GARCÍA-SAURA AG, JUANHUIX J, SÁNCHEZ-FERRER Á. Structural and functional analysis of Oceanobacillus iheyensis macrodomain reveals a network of waters involved in substrate binding and catalysis[J]. Open Biology, 2017, 7(4): 160327.
    [21] MOURE VR, COSTA FF, CRUZ LM, PEDROSA FO, SOUZA EM, LI XD, WINKLER F, HUERGO LF. Regulation of nitrogenase by reversible mono-ADP-ribosylation[J]. Current Topics in Microbiology and Immunology, 2015, 384: 89-106.
    [22] BENTLEY SD, CHATER KF, CERDEÑO-TÁRRAGA AM, CHALLIS GL, THOMSON NR, JAMES KD, HARRIS DE, QUAIL MA, KIESER H, HARPER D, BATEMAN A, BROWN S, CHANDRA G, CHEN CW, COLLINS M, CRONIN A, FRASER A, GOBLE A, HIDALGO J, HORNSBY T, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2)[J]. Nature, 2002, 417(6885): 141-147.
    [23] MUNNUR D, BARTLETT E, MIKOLČEVIĆ P, KIRBY IT, RACK JGM, MIKOČ A, COHEN MS, AHEL I. Reversible ADP-ribosylation of RNA[J]. Nucleic Acids Research, 2019, 47(11): 5658-5669.
    [24] AGNEW T, MUNNUR D, CRAWFORD K, PALAZZO L, MIKOČ A, AHEL I. MacroD1 is a promiscuous ADP-ribosyl hydrolase localized to mitochondria[J]. Frontiers in Microbiology, 2018, 9: 20.
    [25] SLADE D, DUNSTAN MS, 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[J]. Nature, 2011, 477(7366): 616-620.
    [26] CHO CC, CHIEN CY, CHIU YC, LIN MH, HSU CH. Structural and biochemical evidence supporting poly ADP-ribosylation in the bacterium Deinococcus radiodurans[J]. Nature Communications, 2019, 10(1): 1491.
    [27] GARCÍA-SAURA AG, ZAPATA-PÉREZ R, HIDALGO JF, CABANES J, GIL-ORTIZ F, SÁNCHEZ-FERRER Á. An uncharacterized FMAG_01619 protein from Fusobacterium mortiferum ATCC 9817 demonstrates that some bacterial macrodomains can also act as poly-ADP-ribosylhydrolases[J]. Scientific Reports, 2019, 9(1): 3230.
    [28] DEEP A, SINGH L, KAUR J, VELUSAMY M, BHARDWAJ P, SINGH R, THAKUR KG. Structural insights into DarT toxin neutralization by cognate DarG antitoxin: ssDNA mimicry by DarG C-terminal domain keeps the DarT toxin inhibited[J]. Structure, 2023, 31(7): 780-789.e4.
    [29] LeROUX M, SRIKANT S, TEODORO GIC, ZHANG T, LITTLEHALE ML, DORON S, BADIEE M, LEUNG AKL, SOREK R, LAUB MT. The DarTG toxin-antitoxin system provides phage defence by ADP-ribosylating viral DNA[J]. Nature Microbiology, 2022, 7(7): 1028-1040.
    [30] JOHANNESMAN A, CARLSON NA, LeROUX M. Phages carry orphan antitoxin-like enzymes to neutralize the DarTG1 toxin-antitoxin defense system[J]. bioRxiv, 2024: 2024.07.11.602962.
    [31] LALIĆ J, POSAVEC MARJANOVIĆ M, PALAZZO L, PERINA D, SABLJIĆ I, ŽAJA R, COLBY T, PLEŠE B, HALASZ M, JANKEVICIUS G, BUCCA G, AHEL M, MATIĆ I, ĆETKOVIĆ H, LUIĆ M, MIKOČ A, AHEL I. Disruption of macrodomain protein SCO6735 increases antibiotic production in Streptomyces coelicolor[J]. Journal of Biological Chemistry, 2016, 291(44): 23175-23187.
    [32] FU JQ, ZHOU MW, GRITSENKO MA, NAKAYASU ES, SONG L, LUO ZQ. Legionella pneumophila modulates host energy metabolism by ADP-ribosylation of ADP/ATP translocases[J]. eLife, 2022, 11: e73611.
    [33] KUBORI T, LEE J, KIM H, YAMAZAKI K, NISHIKAWA M, KITAO T, OH BH, NAGAI H. Reversible modification of mitochondrial ADP/ATP translocases by paired Legionella effector proteins[J]. Proceedings of the National Academy of Sciences of the United States of America, 2022, 119(23): e2122872119.
    [34] AKTURK A, WASILKO DJ, WU XC, LIU Y, ZHANG Y, QIU JZ, LUO ZQ, REITER KH, BRZOVIC PS, KLEVIT RE, MAO YX. Mechanism of phosphoribosyl-ubiquitination mediated by a single Legionella effector[J]. Nature, 2018, 557(7707): 729-733.
    [35] FU JQ, LI SY, GUAN HX, LI C, ZHAO YB, CHEN TT, XIAN W, ZHANG ZR, LIU Y, GUAN QT, WANG JT, LU QH, KANG LN, ZHENG SR, LI JY, CAO SJ, DAS C, LIU XY, SONG L, OUYANG SY, LUO ZQ. Legionella maintains host cell ubiquitin homeostasis by effectors with unique catalytic mechanisms[J]. Nature Communications, 2024, 15(1): 5953.
    [36] SLADE D, DUNSTAN MS, 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[J]. Nature, 2011, 477(7366): 616-620.
    [37] WANG ZZ, GAGNÉ JP, POIRIER GG, XU WQ. Crystallographic and biochemical analysis of the mouse poly(ADP-ribose) glycohydrolase[J]. PLoS One, 2014, 9(1): e86010.
    [38] BARKAUSKAITE E, BRASSINGTON A, TAN ES, WARWICKER J, DUNSTAN MS, BANOS B, LAFITE P, AHEL M, MITCHISON TJ, AHEL I, LEYS D. Visualization of poly(ADP-ribose) bound to PARG reveals inherent balance between exo- and endo-glycohydrolase activities[J]. Nature Communications, 2013, 4: 2164.
    [39] SCHULLER M, BUTLER RE, ARIZA A, TROMANS-COIA C, JANKEVICIUS G, CLARIDGE TDW, KENDALL SL, GOH S, STEWART GR, AHEL I. Molecular basis for DarT ADP-ribosylation of a DNA base[J]. Nature, 2021, 596(7873): 597-602.
    [40] SCHULLER M, RAGGIASCHI R, MIKOLCEVIC P, RACK JGM, ARIZA A, ZHANG YG, LEDERMANN R, TANG C, MIKOC A, AHEL I. Molecular basis for the reversible ADP-ribosylation of guanosine bases[J]. Molecular Cell, 2023, 83(13): 2303-2315.e6.
    [41] ROSENTHAL F, FEIJS KLH, FRUGIER E, BONALLI M, FORST AH, IMHOF R, WINKLER HC, FISCHER D, CAFLISCH A, HASSA PO, LÜSCHER B, HOTTIGER MO. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases[J]. Nature Structural & Molecular Biology, 2013, 20(4): 502-507.
    [42] JANKEVICIUS G, HASSLER M, GOLIA B, RYBIN V, ZACHARIAS M, TIMINSZKY G, LADURNER AG. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation[J]. Nature Structural & Molecular Biology, 2013, 20(4): 508-514.
    [43] FEHR AR, CHANNAPPANAVAR R, JANKEVICIUS G, FETT C, ZHAO JC, ATHMER J, MEYERHOLZ DK, AHEL I, PERLMAN S. The conserved coronavirus macrodomain promotes virulence and suppresses the innate immune response during severe acute respiratory syndrome coronavirus infection[J]. mBio, 2016, 7(6): e01721-16.
    [44] LI CQ, DEBING Y, JANKEVICIUS G, NEYTS J, AHEL I, COUTARD B, CANARD B. Viral macro domains reverse protein ADP-ribosylation[J]. Journal of Virology, 2016, 90(19): 8478-8486.
    [45] LEI J, KUSOV Y, HILGENFELD R. Nsp3 of coronaviruses: structures and functions of a large multi-domain protein[J]. Antiviral Research, 2018, 149: 58-74.
    [46] RACK JGM, MORRA R, BARKAUSKAITE E, KRAEHENBUEHL R, ARIZA A, QU Y, ORTMAYER M, LEIDECKER O, CAMERON DR, MATIC I, PELEG AY, LEYS D, TRAVEN A, AHEL I. Identification of a class of protein ADP-ribosylating sirtuins in microbial pathogens[J]. Molecular Cell, 2015, 59(2): 309-320.
    [47] CHEN DW, VOLLMAR M, ROSSI MN, PHILLIPS C, KRAEHENBUEHL R, SLADE D, MEHROTRA PV, von DELFT F, CROSTHWAITE SK, GILEADI O, DENU JM, AHEL I. Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases[J]. Journal of Biological Chemistry, 2011, 286(15): 13261-13271.
    [48] KIM T, LEE J, KIM KS. Escherichia coli YmdB regulates biofilm formation independently of its role as an RNase III modulator[J]. BMC Microbiology, 2013, 13: 266.
    [49] FONTANA P, BONFIGLIO JJ, PALAZZO L, BARTLETT E, MATIC I, AHEL I. Serine ADP-ribosylation reversal by the hydrolase ARH3[J]. eLife, 2017, 6: e28533.
    [50] PERINA D, MIKOČ A, AHEL J, ĆETKOVIĆ H, ŽAJA R, AHEL I. Distribution of protein poly(ADP-ribosyl)ation systems across all domains of life[J]. DNA Repair, 2014, 23: 4-16.
    [51] TUCKER JA, BENNETT N, BRASSINGTON C, DURANT ST, HASSALL G, HOLDGATE G, McALISTER M, TRUMAN C, WATSON M. Structures of the human poly(ADP-ribose) glycohydrolase catalytic domain confirm catalytic mechanism and explain inhibition by ADP-HPD derivatives[J]. PLoS One, 2012, 7(12): e50889.
    [52] VILCHEZ LARREA SC, SCHLESINGER M, KEVORKIAN ML, FLAWIÁ MM, ALONSO GD, FERNÁNDEZ VILLAMIL SH. Host cell poly(ADP-ribose) glycohydrolase is crucial for Trypanosoma cruzi infection cycle[J]. PLoS One, 2013, 8(6): e67356.
    [53] FENG BM, LIU CL, de OLIVEIRA MVV, INTORNE AC, LI B, BABILONIA K, de SOUZA FILHO GA, SHAN LB, HE P. Protein poly(ADP-ribosyl)ation regulates Arabidopsis immune gene expression and defense responses[J]. PLoS Genetics, 2015, 11(1): e1004936.
    [54] LIU YQ, ZHOU JZ, OMELCHENKO MV, BELIAEV AS, VENKATESWARAN A, STAIR J, WU LY, THOMPSON DK, XU D, ROGOZIN IB, GAIDAMAKOVA EK, ZHAI M, MAKAROVA KS, KOONIN EV, DALY MJ. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(7): 4191-4196.
    [55] AHEL D, HOREJSÍ Z, WIECHENS N, POLO SE, GARCIA-WILSON E, AHEL I, FLYNN H, SKEHEL M, WEST SC, JACKSON SP, OWEN-HUGHES T, BOULTON SJ. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1[J]. Science, 2009, 325(5945): 1240-1243.
    [56] AHEL I, VUJAKLIJA D, MIKOČ A, GAMULIN V. Transcriptional analysis of the recA gene in Streptomyces rimosus: identification of the new type of promoter[J]. FEMS Microbiology Letters, 2002, 209(1): 129-133.
    [57] GAMULIN V, CETKOVIC H, AHEL I. Identification of a promoter motif regulating the major DNA damage response mechanism of Mycobacterium tuberculosis[J]. FEMS Microbiology Letters, 2004, 238(1): 57-63.
    [58] SBERRO H, LEAVITT A, KIRO R, KOH E, PELEG Y, QIMRON U, SOREK R. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning[J]. Molecular Cell, 2013, 50(1): 136-148.
    [59] YAMAGUCHI Y, PARK JH, INOUYE M. Toxin-antitoxin systems in bacteria and archaea[J]. Annual Review of Genetics, 2011, 45: 61-79.
    [60] SHARIFI R, MORRA R, APPEL CD, TALLIS M, CHIOZA B, JANKEVICIUS G, SIMPSON MA, MATIC I, OZKAN E, GOLIA B, SCHELLENBERG MJ, WESTON R, WILLIAMS JG, ROSSI MN, GALEHDARI H, KRAHN J, WAN A, TREMBATH RC, CROSBY AH, AHEL D, et al. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease[J]. The EMBO Journal, 2013, 32(9): 1225-1237.
    [61] LAWARÉE E, JANKEVICIUS G, COOPER C, AHEL I, UPHOFF S, TANG CM. DNA ADP-ribosylation stalls replication and is reversed by RecF-mediated homologous recombination and nucleotide excision repair[J]. Cell Reports, 2020, 30(5): 1373-1384.e4.
    [62] ZAVERI A, WANG RJ, BOTELLA L, SHARMA R, ZHU LN, WALLACH JB, SONG NM, JANSEN RS, RHEE KY, EHRT S, SCHNAPPINGER D. Depletion of the DarG antitoxin in Mycobacterium tuberculosis triggers the DNA-damage response and leads to cell death[J]. Molecular Microbiology, 2020, 114(4): 641-652.
    [63] BHOGARAJU S, KALAYIL S, LIU YB, BONN F, COLBY T, MATIC I, DIKIC I. Phosphoribosylation of ubiquitin promotes serine ubiquitination and impairs conventional ubiquitination[J]. Cell, 2016, 167(6): 1636-1649.e13.
    [64] HUERGO LF, CHUBATSU LS, SOUZA EM, PEDROSA FO, STEFFENS MBR, MERRICK M. Interactions between PII proteins and the nitrogenase regulatory enzymes DraT and DraG in Azospirillum brasilense[J]. FEBS Letters, 2006, 580(22): 5232-5236.
    [65] BOCK FJ, CHANG P. New directions in poly(ADP-ribose) polymerase biology[J]. The FEBS Journal, 2016, 283(22): 4017-4031.
    [66] GUPTE R, LIU ZY, KRAUS WL. PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes[J]. Genes & Development, 2017, 31(2): 101-126.
    [67] RECHKUNOVA NI, MALTSEVA EA, LAVRIK OI. Post-translational modifications of nucleotide excision repair proteins and their role in the DNA repair[J]. Biochemistry Biokhimiia, 2019, 84(9): 1008-1020.
    [68] HOCH NC, POLO LM. ADP-ribosylation: from molecular mechanisms to human disease[J]. Genetics and Molecular Biology, 2019, 43(1 suppl 1): e20190075.
    [69] RAJAWAT J, SHUKLA N, MISHRA DP. Therapeutic targeting of poly(ADP-ribose) polymerase-1(PARP1) in cancer: current developments, therapeutic strategies, and future opportunities[J]. Medicinal Research Reviews, 2017, 37(6): 1461-1491.
    相似文献
    引证文献
    网友评论
    网友评论
    分享到微博
    发 布
引用本文

焦引弟,张路豪,欧阳松应,关洪鑫. 细菌ADP-核糖基水解酶的结构基础与催化机理[J]. 微生物学报, 2025, 65(1): 38-51

复制
分享
文章指标
  • 点击次数:110
  • 下载次数: 144
  • HTML阅读次数: 126
  • 引用次数: 0
历史
  • 收稿日期:2024-08-19
  • 在线发布日期: 2025-01-04
  • 出版日期: 2025-01-04
文章二维码