1932

Abstract

The ubiquitous proteins with FIC (filamentation induced by cyclic AMP) domains use a conserved enzymatic machinery to modulate the activity of various target proteins by posttranslational modification, typically AMPylation. Following intensive study of the general properties of FIC domain catalysis, diverse molecular activities and biological functions of these remarkably versatile proteins are now being revealed. Here, we review the biological diversity of FIC domain proteins and summarize the underlying structure-function relationships. The original and most abundant genuine bacterial FIC domain proteins are toxins that use diverse molecular activities to interfere with bacterial physiology in various, yet ill-defined, biological contexts. Host-targeted virulence factors have evolved repeatedly out of this pool by exaptation of the enzymatic FIC domain machinery for the manipulation of host cell signaling in favor of bacterial pathogens. The single human FIC domain protein HypE (FICD) has a specific function in the regulation of protein stress responses.

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2016-09-08
2024-04-21
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Literature Cited

  1. Aktories K. 1.  2015. Rho-modifying bacterial protein toxins. Pathog. Dis. 73:ftv091 [Google Scholar]
  2. Al-Khodor S, Price CT, Kalia A, Abu Kwaik Y. 2.  2010. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 18:132–39 [Google Scholar]
  3. Arbing MA, Handelman SK, Kuzin AP, Verdon G, Wang C. 3.  et al. 2010. Crystal structures of Phd-Doc, HigA, and YeeU establish multiple evolutionary links between microbial growth-regulating toxin-antitoxin systems. Structure 18:996–1010 [Google Scholar]
  4. Behnke J, Feige MJ, Hendershot LM. 4.  2015. BiP and its nucleotide exchange factors Grp170 and Sil1: mechanisms of action and biological functions. J. Mol. Biol. 427:1589–608 [Google Scholar]
  5. Broncel M, Serwa RA, Bunney TD, Katan M, Tate EW. 5.  2016. Global profiling of Huntington-associated protein E (HYPE)-mediated AMPylation through a chemical proteomic approach. Mol. Cell Proteom. 15:715–25 [Google Scholar]
  6. Bunney TD, Cole AR, Broncel M, Esposito D, Tate EW, Katan M. 6.  2014. Crystal structure of the human, FIC-domain containing protein HYPE and implications for its functions. Structure 22:1831–43 [Google Scholar]
  7. Campanacci V, Mukherjee S, Roy CR, Cherfils J. 7.  2013. Structure of the Legionella effector AnkX reveals the mechanism of phosphocholine transfer by the FIC domain. EMBO J. 32:1469–77 [Google Scholar]
  8. Casselli T, Lynch T, Southward CM, Jones BW, DeVinney R. 8.  2008. Vibrio parahaemolyticus inhibition of Rho family GTPase activation requires a functional chromosome I type III secretion system. Infect. Immun. 76:2202–11 [Google Scholar]
  9. Castro-Roa D, Garcia-Pino A, De Gieter S, van Nuland NA, Loris R, Zenkin N. 9.  2013. The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu. Nat. Chem. Biol. 9:811–17Shows that the Doc toxin is a kinase that phosphorylates EF-Tu. [Google Scholar]
  10. Chambers JE, Petrova K, Tomba G, Vendruscolo M, Ron D. 10.  2012. ADP ribosylation adapts an ER chaperone response to short-term fluctuations in unfolded protein load. J. Cell Biol. 198:371–85 [Google Scholar]
  11. Chan WT, Yeo CC, Sadowy E, Espinosa M. 11.  2014. Functional validation of putative toxin-antitoxin genes from the gram-positive pathogen Streptococcus pneumoniae: phd-doc is the fourth bona-fide operon. Front. Microbiol. 5:677 [Google Scholar]
  12. Chatterji M, Sengupta S, Nagaraja V. 12.  2003. Chromosomally encoded gyrase inhibitor GyrI protects Escherichia coli against DNA-damaging agents. Arch. Microbiol. 180:339–46 [Google Scholar]
  13. Chen C, Banga S, Mertens K, Weber MM, Gorbaslieva I. 13.  et al. 2010. Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. PNAS 107:21755–60 [Google Scholar]
  14. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL. 14.  2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–94 [Google Scholar]
  15. Cruz JW, Rothenbacher FP, Maehigashi T, Lane WS, Dunham CM, Woychik NA. 15.  2014. Doc toxin is a kinase that inactivates elongation factor Tu. J. Biol. Chem. 289:7788–98 [Google Scholar]
  16. Cruz JW, Woychik NA. 16.  2014. Teaching Fido new ModiFICation tricks. PLOS Pathog. 10:e1004349 [Google Scholar]
  17. Das D, Krishna SS, McMullan D, Miller MD, Xu Q. 17.  et al. 2009. Crystal structure of the Fic (Filamentation induced by cAMP) family protein SO4266 (gi|24375750) from Shewanella oneidensis MR-1 at 1.6 Å resolution. Proteins 75:264–71 [Google Scholar]
  18. Defeu Soufo HJ, Reimold C, Breddermann H, Mannherz HG, Graumann PL. 18.  2015. Translation elongation factor EF-Tu modulates filament formation of actin-like MreB protein in vitro. J. Mol. Biol. 427:1715–27 [Google Scholar]
  19. Deghorain M, Goeders N, Jové T, Melderen L. 19.  2013. Type II toxin-antitoxin loci: the ccdAB and parDE families. Prokaryotic Toxin-Antitoxins K Gerdes 45–67 Berlin: Springer [Google Scholar]
  20. Desveaux D, Singer AU, Wu AJ, McNulty BC, Musselwhite L. 20.  et al. 2007. Type III effector activation via nucleotide binding, phosphorylation, and host target interaction. PLOS Pathog. 3:e48 [Google Scholar]
  21. Dy RL, Richter C, Salmond GPC, Fineran PC. 21.  2014. Remarkable mechanisms in microbes to resist phage infections. Annu. Rev. Virol. 1:307–31 [Google Scholar]
  22. Engel P, Goepfert A, Stanger FV, Harms A, Schmidt A. 22.  et al. 2012. Adenylylation control by intra- or intermolecular active-site obstruction in Fic proteins. Nature 482:107–10Shows that bona fide AMPylating Fic proteins are regulated by a conserved mechanism of inhibition. [Google Scholar]
  23. Engel P, Salzburger W, Liesch M, Chang CC, Maruyama S. 23.  et al. 2011. Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella. PLOS Genet. 7:e1001296 [Google Scholar]
  24. Feng F, Yang F, Rong W, Wu X, Zhang J. 24.  et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–18 [Google Scholar]
  25. Finsel I, Hilbi H. 25.  2015. Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones. Cell Microbiol. 17:935–50 [Google Scholar]
  26. Frampton R, Aggio RB, Villas-Boas SG, Arcus VL, Cook GM. 26.  2012. Toxin-antitoxin systems of Mycobacterium smegmatis are essential for cell survival. J. Biol. Chem. 287:5340–56 [Google Scholar]
  27. Garcia-Pino A, Christensen-Dalsgaard M, Wyns L, Yarmolinsky M, Magnuson RD. 27.  et al. 2008. Doc of prophage P1 is inhibited by its antitoxin partner Phd through fold complementation. J. Biol. Chem. 283:30821–27 [Google Scholar]
  28. Garcia-Pino A, Zenkin N, Loris R. 28.  2014. The many faces of Fic: structural and functional aspects of Fic enzymes. Trends Biochem. Sci. 39:121–29 [Google Scholar]
  29. Gerdes K, Maisonneuve E. 29.  2012. Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol. 66:103–23 [Google Scholar]
  30. Goepfert A, Harms A, Schirmer T, Dehio C. 30.  2013. Type II toxin-antitoxin loci: the fic family. Prokaryotic Toxin-Antitoxins K Gerdes 177–87 Berlin: Springer [Google Scholar]
  31. Goepfert A, Stanger FV, Dehio C, Schirmer T. 31.  2013. Conserved inhibitory mechanism and competent ATP binding mode for adenylyltransferases with Fic fold. PLOS One 8:e64901 [Google Scholar]
  32. Goody PR, Heller K, Oesterlin LK, Muller MP, Itzen A, Goody RS. 32.  2012. Reversible phosphocholination of Rab proteins by Legionella pneumophila effector proteins. EMBO J. 31:1774–84 [Google Scholar]
  33. Goulard C, Langrand S, Carniel E, Chauvaux S. 33.  2010. The Yersinia pestis chromosome encodes active addiction toxins. J. Bacteriol. 192:3669–77 [Google Scholar]
  34. Ham H, Woolery AR, Tracy C, Stenesen D, Kramer H, Orth K. 34.  2014. Unfolded protein response-regulated Drosophila Fic (dFic) reversibly AMPylates BiP during endoplasmic reticulum homeostasis. J. Biol. Chem. 289:36059 [Google Scholar]
  35. Harms A, Dehio C. 35.  2012. Intruders below the radar: molecular pathogenesis of Bartonella spp. Clin. Microbiol. Rev. 25:42–78 [Google Scholar]
  36. Harms A, Stanger FV, Scheu PD, de Jong IG, Goepfert A. 36.  et al. 2015. Adenylylation of gyrase and topo IV by FicT toxins disrupts bacterial DNA topology. Cell Rep. 12:1497–507Reports class I FIC domain proteins as FicT toxins that AMPylate gyrase and topo IV. [Google Scholar]
  37. Hayes F, Kedzierska B. 37.  2014. Regulating toxin-antitoxin expression: controlled detonation of intracellular molecular timebombs. Toxins 6:337–58 [Google Scholar]
  38. Helaine S, Cheverton AM, Watson KG, Faure LM, Matthews SA, Holden DW. 38.  2014. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343:204–8 [Google Scholar]
  39. Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G. 39.  et al. 2009. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLOS Biol. 7:e96 [Google Scholar]
  40. Innes RW. 40.  2011. Activation of plant Nod-like receptors: How indirect can it be?. Cell Host Microbe 9:87–89 [Google Scholar]
  41. Itzen A, Blankenfeldt W, Goody RS. 41.  2011. Adenylylation: renaissance of a forgotten post-translational modification. Trends Biochem. Sci. 36:221–28 [Google Scholar]
  42. Kawamukai M, Matsuda H, Fujii W, Nishida T, Izumoto Y. 42.  et al. 1988. Cloning of the fic-1 gene involved in cell filamentation induced by cyclic AMP and construction of a delta fic Escherichia coli strain. J. Bacteriol. 170:3864–69 [Google Scholar]
  43. Kawamukai M, Matsuda H, Fujii W, Utsumi R, Komano T. 43.  1989. Nucleotide sequences of fic and fic-1 genes involved in cell filamentation induced by cyclic AMP in Escherichia coli. J. Bacteriol. 171:4525–29 [Google Scholar]
  44. Khater S, Mohanty D. 44.  2015. Deciphering the molecular basis of functional divergence in AMPylating enzymes by molecular dynamics simulations and structure guided phylogeny. Biochemistry 54:5209–24 [Google Scholar]
  45. Khater S, Mohanty D. 45.  2015. In silico identification of AMPylating enzymes and study of their divergent evolution. Sci. Rep. 5:10804 [Google Scholar]
  46. Kinch LN, Yarbrough ML, Orth K, Grishin NV. 46.  2009. Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLOS One 4:e5818Established that the Fido domain is formed by AvrB and Doc homologs together with Fic proteins sensu stricto. [Google Scholar]
  47. Komano T, Utsumi R, Kawamukai M. 47.  1991. Functional analysis of the fic gene involved in regulation of cell division. Res. Microbiol. 142:269–77 [Google Scholar]
  48. Lee CC, Wood MD, Ng K, Andersen CB, Liu Y. 48.  et al. 2004. Crystal structure of the type III effector AvrB from Pseudomonas syringae. Structure 12:487–94 [Google Scholar]
  49. Lee D, Bourdais G, Yu G, Robatzek S, Coaker G. 49.  2015. Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H+-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27:2042–56 [Google Scholar]
  50. Lehnherr H, Maguin E, Jafri S, Yarmolinsky MB. 50.  1993. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 233:414–28 [Google Scholar]
  51. Lewallen DM, Sreelatha A, Dharmarajan V, Madoux F, Chase P. 51.  et al. 2014. Inhibiting AMPylation: a novel screen to identify the first small molecule inhibitors of protein AMPylation. ACS Chem. Biol. 9:433–42 [Google Scholar]
  52. Liu J, Elmore JM, Lin ZJ, Coaker G. 52.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46 [Google Scholar]
  53. Liu M, Zhang Y, Inouye M, Woychik NA. 53.  2008. Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit. PNAS 105:5885–90 [Google Scholar]
  54. Lobato-Marquez D, Moreno-Cordoba I, Figueroa V, Diaz-Orejas R, Garcia-del Portillo F. 54.  2015. Distinct type I and type II toxin-antitoxin modules control Salmonella lifestyle inside eukaryotic cells. Sci. Rep. 5:9374 [Google Scholar]
  55. Lu C, Nakayasu ES, Zhang LQ, Luo ZQ. 55.  2016. Identification of Fic-1 as an enzyme that inhibits bacterial DNA replication by AMPylating GyrB, promoting filament formation. Sci. Signal 9:ra11 [Google Scholar]
  56. Luong P, Kinch LN, Brautigam CA, Grishin NV, Tomchick DR, Orth K. 56.  2010. Kinetic and structural insights into the mechanism of AMPylation by VopS Fic domain. J. Biol. Chem. 285:20155–63 [Google Scholar]
  57. Makarova KS, Wolf YI, Koonin EV. 57.  2009. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4:19 [Google Scholar]
  58. Mattoo S, Durrant E, Chen MJ, Xiao J, Lazar CS. 58.  et al. 2011. Comparative analysis of Histophilus somni immunoglobulin-binding protein A (IbpA) with other fic domain-containing enzymes reveals differences in substrate and nucleotide specificities. J. Biol. Chem. 286:32834–42 [Google Scholar]
  59. Merrell DS, Falkow S. 59.  2004. Frontal and stealth attack strategies in microbial pathogenesis. Nature 430:250–56 [Google Scholar]
  60. Mishra S, Bhagavat R, Chandra N, Vijayarangan N, Rajeswari H, Ajitkumar P. 60.  2012. Cloning, expression, purification, and biochemical characterisation of the FIC motif containing protein of Mycobacterium tuberculosis. Protein Expr. Purif. 86:58–67 [Google Scholar]
  61. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S. 61.  et al. 2015. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43:D213–21 [Google Scholar]
  62. Mukherjee S, Liu X, Arasaki K, McDonough J, Galan JE, Roy CR. 62.  2011. Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 477:103–6Shows that the FIC domain of Legionella AnkX catalyzes target protein phosphocholination. [Google Scholar]
  63. Newton HJ, Kohler LJ, McDonough JA, Temoche-Diaz M, Crabill E. 63.  et al. 2014. A screen of Coxiella burnetii mutants reveals important roles for Dot/Icm effectors and host autophagy in vacuole biogenesis. PLOS Pathog. 10:e1004286 [Google Scholar]
  64. Palanivelu DV, Goepfert A, Meury M, Guye P, Dehio C, Schirmer T. 64.  2010. Fic domain catalyzed adenylylation: insight provided by the structural analysis of the type IV secretion system effector BepA. Protein Sci. 20:492–99 [Google Scholar]
  65. Pan X, Luhrmann A, Satoh A, Laskowski-Arce MA, Roy CR. 65.  2008. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651–54 [Google Scholar]
  66. Pieles K, Glatter T, Harms A, Schmidt A, Dehio C. 66.  2014. An experimental strategy for the identification of AMPylation targets from complex protein samples. Proteomics 14:1048–52 [Google Scholar]
  67. Preissler S, Rato C, Chen R, Antrobus R, Ding S. 67.  et al. 2015. AMPylation matches BiP activity to client protein load in the endoplasmic reticulum. eLife 4:e12621Shows that HypE AMPylates the ER chaperone BiP to adjust its activity to client load. [Google Scholar]
  68. Rahman M, Ham H, Liu X, Sugiura Y, Orth K, Kramer H. 68.  2012. Visual neurotransmission in Drosophila requires expression of Fic in glial capitate projections. Nat. Neurosci. 15:871–75Demonstrates a function of the Drosophila HypE homolog in eyesight in vivo. [Google Scholar]
  69. Roy CR, Cherfils J. 69.  2015. Structure and function of Fic proteins. Nat. Rev. Microbiol. 13:631–40 [Google Scholar]
  70. Roy CR, Mukherjee S. 70.  2009. Bacterial FIC proteins AMP up infection. Sci. Signal 2:pe14 [Google Scholar]
  71. Russell AR, Ashfield T, Innes RW. 71.  2015. Pseudomonas syringae effector AvrPphB suppresses AvrB-induced activation of RPM1 but not AvrRpm1-induced activation. Mol. Plant Microbe Interact. 28:727–35 [Google Scholar]
  72. Sanyal A, Chen AJ, Nakayasu ES, Lazar CS, Zbornik EA. 72.  et al. 2015. A novel link between Fic (filamentation induced by cAMP)-mediated adenylylation/AMPylation and the unfolded protein response. J. Biol. Chem. 290:8482–99 [Google Scholar]
  73. Schulein R, Guye P, Rhomberg TA, Schmid MC, Schroder G. 73.  et al. 2005. A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. PNAS 102:856–61 [Google Scholar]
  74. Siamer S, Dehio C. 74.  2015. New insights into the role of Bartonella effector proteins in pathogenesis. Curr. Opin. Microbiol. 23:80–85 [Google Scholar]
  75. Stanger FV, Burmann BM, Harms A, Aragao H, Mazur A. 75.  et al. 2016. Intrinsic regulation of FIC-domain AMP-transferases by oligomerization and automodification. PNAS 113:E529–37 [Google Scholar]
  76. Tan Y, Arnold RJ, Luo ZQ. 76.  2011. Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination. PNAS 108:21212–17 [Google Scholar]
  77. Tran PV, Bannor TA, Doktor SZ, Nichols BP. 77.  1990. Chromosomal organization and expression of Escherichia coli pabA. J. Bacteriol. 172:397–410 [Google Scholar]
  78. Truttmann MC, Wu Q, Stiegeler S, Duarte JN, Ingram J, Ploegh HL. 78.  2015. HypE-specific nanobodies as tools to modulate HypE-mediated target AMPylation. J. Biol. Chem. 290:9087–100 [Google Scholar]
  79. Utsumi R, Kawamukai M, Obata K, Morita J, Himeno M, Komano T. 79.  1983. Identification of a membrane protein induced concurrently with cell filamentation by cyclic AMP in an Escherichia coli K-12 fic mutant. J. Bacteriol. 155:398–401 [Google Scholar]
  80. Utsumi R, Kusafuka S, Nakayama T, Tanaka K, Takayanagi Y. 80.  et al. 1993. Stationary phase-specific expression of the fic gene in Escherichia coli K-12 is controlled by the rpoS gene product (σ38). FEMS Microbiol. Lett. 113:273–78 [Google Scholar]
  81. Utsumi R, Nakamoto Y, Kawamukai M, Himeno M, Komano T. 81.  1982. Involvement of cyclic AMP and its receptor protein in filamentation of an Escherichia coli fic mutant. J. Bacteriol. 151:807–12Introduces the term filamentation induced by cAMP. [Google Scholar]
  82. Utsumi R, Tanabe H, Nakamoto Y, Kawamukai M, Sakai H. 82.  et al. 1981. Inhibitory effect of adenosine 3′,5′-phosphate on cell division of Escherichia coli K-12 mutant derivatives. J. Bacteriol. 147:1105–9 [Google Scholar]
  83. van Schaik EJ, Chen C, Mertens K, Weber MM, Samuel JE. 83.  2013. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nat. Rev. Microbiol. 11:561–73 [Google Scholar]
  84. Voorhees RM, Ramakrishnan V. 84.  2013. Structural basis of the translational elongation cycle. Annu. Rev. Biochem. 82:203–36 [Google Scholar]
  85. Vos SM, Lyubimov AY, Hershey DM, Schoeffler AJ, Sengupta S. 85.  et al. 2014. Direct control of type IIA topoisomerase activity by a chromosomally encoded regulatory protein. Genes Dev 28:1485–97 [Google Scholar]
  86. Vos SM, Tretter EM, Schmidt BH, Berger JM. 86.  2011. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell. Biol. 12:827–41 [Google Scholar]
  87. Wang G, Roux B, Feng F, Guy E, Li L. 87.  et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–95 [Google Scholar]
  88. Welner D, Dedic E, van Leeuwen HC, Kuijper E, Bjerrum MJ. 88.  et al. 2014. Protein expression, characterization, crystallization and preliminary X-ray crystallographic analysis of a Fic protein from Clostridium difficile. Acta Crystallogr. F Struct. Biol. Commun. F70:827–31 [Google Scholar]
  89. Woolery AR, Luong P, Broberg CA, Orth K. 89.  2010. AMPylation: Something old is new again. Front. Microbiol. 1:113 [Google Scholar]
  90. Woolery AR, Yu X, LaBaer J, Orth K. 90.  2014. AMPylation of Rho GTPases subverts multiple host signaling processes. J. Biol. Chem. 289:32977–88 [Google Scholar]
  91. Worby CA, Mattoo S, Kruger RP, Corbeil LB, Koller A. 91.  et al. 2009. The Fic domain: regulation of cell signaling by adenylylation. Mol. Cell 34:93–103 [Google Scholar]
  92. Xiao J, Worby CA, Mattoo S, Sankaran B, Dixon JE. 92.  2010. Structural basis of Fic-mediated adenylylation. Nat. Struct. Mol. Biol. 17:1004–10First and only report of a structure of a FIC domain enzyme in complex with its target protein. [Google Scholar]
  93. Xu H, Yang J, Gao W, Li L, Li P. 93.  et al. 2014. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513:237–41 [Google Scholar]
  94. Yamaguchi Y, Park JH, Inouye M. 94.  2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45:61–79 [Google Scholar]
  95. Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K. 95.  2009. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323:269–72First report of AMPylation as enzymatic activity of Fic proteins (with Worby et al.; 91). [Google Scholar]
  96. Yu X, Woolery AR, Luong P, Hao YH, Grammel M. 96.  et al. 2014. Copper-catalyzed azide-alkyne cycloaddition (click chemistry)-based detection of global pathogen-host AMPylation on self-assembled human protein microarrays. Mol. Cell Proteom. 13:3164–76 [Google Scholar]
  97. Zekarias B, Mattoo S, Worby C, Lehmann J, Rosenbusch RF, Corbeil LB. 97.  2010. Histophilus somni IbpA DR2/Fic in virulence and immunoprotection at the natural host alveolar epithelial barrier. Infect. Immun. 78:1850–58 [Google Scholar]
  98. Zhou Z, Wu Y, Yang Y, Du M, Zhang X. 98.  et al. 2015. An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion. Plant Cell 27:2032–41 [Google Scholar]
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