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Abstract

Bacterial pathogens encode a wide variety of effectors and toxins that hijack host cell structure and function. Of particular importance are virulence factors that target actin cytoskeleton dynamics critical for cell shape, stability, motility, phagocytosis, and division. In addition, many bacteria target organelles of the general secretory pathway (e.g., the endoplasmic reticulum and the Golgi complex) and recycling pathways (e.g., the endolysosomal system) to establish and maintain an intracellular replicative niche. Recent research on the biochemistry and structural biology of bacterial effector proteins and toxins has begun to shed light on the molecular underpinnings of these host-pathogen interactions. This exciting work is revealing how pathogens gain control of the complex and dynamic host cellular environments, which impacts our understanding of microbial infectious disease, immunology, and human cell biology.

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2016-10-06
2024-03-29
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Literature Cited

  1. Aili M, Hallberg B, Wolf-Watz H, Rosqvist R. 2002. GAP activity of Yersinia YopE. Methods Enzymol. 358:359–70 [Google Scholar]
  2. Aktories K. 2011. Bacterial protein toxins that modify host regulatory GTPases. Nat. Rev. Microbiol. 9:487–98 [Google Scholar]
  3. Aktories K, Barmann M, Ohishi I, Tsuyama S, Jakobs KH, Habermann E. 1986. Botulinum C2 toxin ADP-ribosylates actin. Nature 322:390–92 [Google Scholar]
  4. Aktories K, Wegner A. 1989. ADP-ribosylation of actin by clostridial toxins. J. Cell Biol. 109:1385–87 [Google Scholar]
  5. Al-Younes HM, Brinkmann V, Meyer TF. 2004. Interaction of Chlamydia trachomatis serovar L2 with the host autophagic pathway. Infect. Immun. 72:4751–62 [Google Scholar]
  6. Alto NM, Weflen AW, Rardin MJ, Yarar D, Lazar CS. et al. 2007. The type III effector EspF coordinates membrane trafficking by the spatiotemporal activation of two eukaryotic signaling pathways. J. Cell Biol. 178:1265–78 [Google Scholar]
  7. Andor A, Trulzsch K, Essler M, Roggenkamp A, Wiedemann A. et al. 2001. YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell. Microbiol. 3:301–10 [Google Scholar]
  8. Avvaru BS, Pernier J, Carlier MF. 2015. Dimeric WH2 repeats of VopF sequester actin monomers into non-nucleating linear string conformations: an X-ray scattering study. J. Struct. Biol. 190:192–99 [Google Scholar]
  9. Bakowski MA, Braun V, Lam GY, Yeung T, Heo WD. et al. 2010. The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe 7:453–62 [Google Scholar]
  10. Benanti EL, Nguyen CM, Welch MD. 2015. Virulent Burkholderia species mimic host actin polymerases to drive actin-based motility. Cell 161:348–60 [Google Scholar]
  11. Beron W, Gutierrez MG, Rabinovitch M, Colombo MI. 2002. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect. Immun. 70:5816–21 [Google Scholar]
  12. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S. et al. 2000. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19:3235–49 [Google Scholar]
  13. Birmingham CL, Canadien V, Gouin E, Troy EB, Yoshimori T. et al. 2007. Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3:442–51 [Google Scholar]
  14. Birmingham CL, Jiang X, Ohlson MB, Miller SI, Brumell JH. 2005. Salmonella-induced filament formation is a dynamic phenotype induced by rapidly replicating Salmonella enterica serovar Typhimurium in epithelial cells. Infect. Immun. 73:1204–8 [Google Scholar]
  15. Boucrot E, Henry T, Borg JP, Gorvel JP, Meresse S. 2005. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308:1174–78 [Google Scholar]
  16. Brombacher E, Urwyler S, Ragaz C, Weber SS, Kami K. et al. 2009. Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate–binding effector protein of Legionella pneumophila. J. Biol. Chem. 284:4846–56 [Google Scholar]
  17. Buchwald G, Friebel A, Galan JE, Hardt WD, Wittinghofer A, Scheffzek K. 2002. Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J. 21:3286–95 [Google Scholar]
  18. Burdette DL, Seemann J, Orth K. 2009. Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis. Mol. Microbiol. 73:639–49 [Google Scholar]
  19. Burdette DL, Yarbrough ML, Orvedahl A, Gilpin CJ, Orth K. 2008. Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. PNAS 105:12497–502 [Google Scholar]
  20. Burnaevskiy N, Fox TG, Plymire DA, Ertelt JM, Weigele BA. et al. 2013. Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature 496:106–9 [Google Scholar]
  21. Burnaevskiy N, Peng T, Reddick LE, Hang HC, Alto NM. 2015. Myristoylome profiling reveals a concerted mechanism of ARF GTPase deacylation by the bacterial protease IpaJ. Mol. Cell 58:110–22 [Google Scholar]
  22. Case ED, Chong A, Wehrly TD, Hansen B, Child R. et al. 2014. The Francisella O-antigen mediates survival in the macrophage cytosol via autophagy avoidance. Cell. Microbiol. 16:862–77 [Google Scholar]
  23. Chang J, Myeni SK, Lin TL, Wu CC, Staiger CJ, Zhou D. 2007. SipC multimerization promotes actin nucleation and contributes to Salmonella-induced inflammation. Mol. Microbiol. 66:1548–56 [Google Scholar]
  24. Cherfils J, Zeghouf M. 2013. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol. Rev. 93:269–309 [Google Scholar]
  25. Choy A, Dancourt J, Mugo B, O'Connor TJ, Isberg RR. et al. 2012. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science 338:1072–76 [Google Scholar]
  26. Christen M, Coye LH, Hontz JS, LaRock DL, Pfuetzner RA. et al. 2009. Activation of a bacterial virulence protein by the GTPase RhoA. Sci. Signal. 2:ra71 [Google Scholar]
  27. Clements A, Smollett K, Lee SF, Hartland EL, Lowe M, Frankel G. 2011. EspG of enteropathogenic and enterohemorrhagic E. coli binds the Golgi matrix protein GM130 and disrupts the Golgi structure and function. Cell. Microbiol. 13:1429–39 [Google Scholar]
  28. Comerci DJ, Martinez-Lorenzo MJ, Sieira R, Gorvel JP, Ugalde RA. 2001. Essential role of the VirB machinery in the maturation of the Brucella abortus–containing vacuole. Cell. Microbiol. 3:159–68 [Google Scholar]
  29. Cordero CL, Kudryashov DS, Reisler E, Satchell KJ. 2006. The actin cross-linking domain of the Vibrio cholerae RTX toxin directly catalyzes the covalent cross-linking of actin. J. Biol. Chem. 281:32366–74 [Google Scholar]
  30. Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A. et al. 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13:343–59 [Google Scholar]
  31. de Figueiredo P, Ficht TA, Rice-Ficht A, Rossetti CA, Adams LG. 2015. Pathogenesis and immunobiology of brucellosis: review of Brucella-host interactions. Am. J. Pathol. 185:1505–17 [Google Scholar]
  32. Dean P. 2011. Functional domains and motifs of bacterial type III effector proteins and their roles in infection. FEMS Microbiol. Rev. 35:1100–25 [Google Scholar]
  33. Deiwick J, Salcedo SP, Boucrot E, Gilliland SM, Henry T. et al. 2006. The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect. Immun. 74:6965–72 [Google Scholar]
  34. Dobbs N, Burnaevskiy N, Chen D, Gonugunta VK, Alto NM, Yan N. 2015. STING activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe 18:157–68 [Google Scholar]
  35. Domingues L, Holden DW, Mota LJ. 2014. The Salmonella effector SteA contributes to the control of membrane dynamics of Salmonella-containing vacuoles. Infect. Immun. 82:2923–34 [Google Scholar]
  36. Donaldson JG, Jackson CL. 2011. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12:362–75 [Google Scholar]
  37. Dong N, Zhu Y, Lu Q, Hu L, Zheng Y, Shao F. 2012. Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150:1029–41 [Google Scholar]
  38. Dorn BR, Dunn WA Jr, Progulske-Fox A. 2001. Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect. Immun. 69:5698–708 [Google Scholar]
  39. Dortet L, Mostowy S, Samba-Louaka A, Gouin E, Nahori MA. et al. 2011. Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLOS Pathog. 7:e1002168 [Google Scholar]
  40. Druar C, Yu F, Barnes JL, Okinaka RT, Chantratita N. et al. 2008. Evaluating Burkholderia pseudomallei Bip proteins as vaccines and Bip antibodies as detection agents. FEMS Immunol. Med. Microbiol. 52:78–87 [Google Scholar]
  41. Elliott SJ, Krejany EO, Mellies JL, Robins-Browne RM, Sasakawa C, Kaper JB. 2001. EspG, a novel type III system–secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect. Immun. 69:4027–33 [Google Scholar]
  42. Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S. et al. 1997. Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387:729–33 [Google Scholar]
  43. Fleiszig SM, Wiener-Kronish JP, Miyazaki H, Vallas V, Mostov KE. et al. 1997. Pseudomonas aeruginosa–mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 65:579–86 [Google Scholar]
  44. Friebel A, Ilchmann H, Aepfelbacher M, Ehrbar K, Machleidt W, Hardt WD. 2001. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J. Biol. Chem. 276:34035–40 [Google Scholar]
  45. Fu Y, Galan JE. 1999. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401:293–97 [Google Scholar]
  46. Fullner KJ, Mekalanos JJ. 2000. In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J. 19:5315–23 [Google Scholar]
  47. Galkin VE, Orlova A, VanLoock MS, Zhou D, Galan JE, Egelman EH. 2002. The bacterial protein SipA polymerizes G-actin and mimics muscle nebulin. Nat. Struct. Biol. 9:518–21 [Google Scholar]
  48. Ghigo E, Colombo MI, Heinzen RA. 2012. The Coxiella burnetii parasitophorous vacuole. Adv. Exp. Med. Biol. 984:141–69 [Google Scholar]
  49. Glotfelty LG, Hecht GA. 2012. Enteropathogenic E. coli effectors EspG1/G2 disrupt tight junctions: new roles and mechanisms. Ann. N. Y. Acad. Sci. 1258:149–58 [Google Scholar]
  50. Goldberg MB, Theriot JA. 1995. Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. PNAS 92:6572–76 [Google Scholar]
  51. Goody PR, Heller K, Oesterlin LK, Muller MP, Itzen A, Goody RS. 2012. Reversible phosphocholination of Rab proteins by Legionella pneumophila effector proteins. EMBO J. 31:1774–84 [Google Scholar]
  52. Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W. et al. 2005. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell. Microbiol. 7:981–93 [Google Scholar]
  53. Haglund CM, Choe JE, Skau CT, Kovar DR, Welch MD. 2010. Rickettsia Sca2 is a bacterial formin-like mediator of actin-based motility. Nat. Cell Biol. 12:1057–63 [Google Scholar]
  54. Han S, Craig JA, Putnam CD, Carozzi NB, Tainer JA. 1999. Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex. Nat. Struct. Biol. 6:932–36 [Google Scholar]
  55. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815–26 [Google Scholar]
  56. Hayes CS, Aoki SK, Low DA. 2010. Bacterial contact–dependent delivery systems. Annu. Rev. Genet. 44:71–90 [Google Scholar]
  57. Hayward RD, Koronakis V. 1999. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18:4926–34 [Google Scholar]
  58. Heisler DB, Kudryashova E, Grinevich DO, Suarez C, Winkelman JD. et al. 2015. ACD toxin–produced actin oligomers poison formin-controlled actin polymerization. Science 349:535–39 [Google Scholar]
  59. Henry T, Couillault C, Rockenfeller P, Boucrot E, Dumont A. et al. 2006. The Salmonella effector protein PipB2 is a linker for kinesin-1. PNAS 103:13497–502 [Google Scholar]
  60. Higa N, Toma C, Koizumi Y, Nakasone N, Nohara T. et al. 2013. Vibrio parahaemolyticus effector proteins suppress inflammasome activation by interfering with host autophagy signaling. PLOS Pathog. 9:e1003142 [Google Scholar]
  61. Hiyoshi H, Kodama T, Saito K, Gotoh K, Matsuda S. et al. 2011. VopV, an F-actin-binding type III secretion effector, is required for Vibrio parahaemolyticus–induced enterotoxicity. Cell Host Microbe 10:401–9 [Google Scholar]
  62. Hoffman GR, Nassar N, Cerione RA. 2000. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100:345–56 [Google Scholar]
  63. Horenkamp FA, Mukherjee S, Alix E, Schauder CM, Hubber AM. et al. 2014. Legionella pneumophila subversion of host vesicular transport by SidC effector proteins. Traffic 15:488–99 [Google Scholar]
  64. Hsu F, Luo X, Qiu J, Teng YB, Jin J. et al. 2014. The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling. PNAS 111:10538–43 [Google Scholar]
  65. Huang J, Birmingham CL, Shahnazari S, Shiu J, Zheng YT. et al. 2011. Antibacterial autophagy occurs at PI3P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7:17–26 [Google Scholar]
  66. Hutagalung AH, Novick PJ. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91:119–49 [Google Scholar]
  67. Juris SJ, Rudolph AE, Huddler D, Orth K, Dixon JE. 2000. A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. PNAS 97:9431–36 [Google Scholar]
  68. Just I, Selzer J, Jung M, van Damme J, Vandekerckhove J, Aktories K. 1995. Rho-ADP-ribosylating exoenzyme from Bacillus cereus. Purification, characterization, and identification of the NAD-binding site. Biochemistry 34:334–40 [Google Scholar]
  69. Kahn RA. 2009. Toward a model for Arf GTPases as regulators of traffic at the Golgi. FEBS Lett. 583:3872–79 [Google Scholar]
  70. Kaniga K, Trollinger D, Galan JE. 1995a. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J. Bacteriol. 177:7078–85 [Google Scholar]
  71. Kaniga K, Tucker S, Trollinger D, Galan JE. 1995b. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J. Bacteriol. 177:3965–71 [Google Scholar]
  72. Keestra AM, Baumler AJ. 2014. Detection of enteric pathogens by the nodosome. Trends Immunol. 35:123–30 [Google Scholar]
  73. Keestra AM, Winter MG, Auburger JJ, Frassle SP, Xavier MN. et al. 2013. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 496:233–37 [Google Scholar]
  74. Kim KH, An DR, Song J, Yoon JY, Kim HS. et al. 2012. Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7. PNAS 109:7729–34 [Google Scholar]
  75. Kingdon HS, Shapiro BM, Stadtman ER. 1967. Regulation of glutamine synthetase. 8. ATP: glutamine synthetase adenylyltransferase, an enzyme that catalyzes alterations in the regulatory properties of glutamine synthetase. PNAS 58:1703–10 [Google Scholar]
  76. Knodler LA, Steele-Mortimer O. 2005. The Salmonella effector PipB2 affects late endosome/lysosome distribution to mediate Sif extension. Mol. Biol. Cell 16:4108–23 [Google Scholar]
  77. Krieger V, Liebl D, Zhang Y, Rajashekar R, Chlanda P. et al. 2014. Reorganization of the endosomal system in Salmonella-infected cells: the ultrastructure of Salmonella-induced tubular compartments. PLOS Pathog. 10:e1004374 [Google Scholar]
  78. Kubori T, Galan JE. 2003. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115:333–42 [Google Scholar]
  79. Kuhle V, Abrahams GL, Hensel M. 2006. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2–dependent manner. Traffic 7:716–30 [Google Scholar]
  80. Lang AE, Schmidt G, Schlosser A, Hey TD, Larrinua IM. et al. 2010. Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 327:1139–42 [Google Scholar]
  81. Lerena MC, Colombo MI. 2011. Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system. Cell. Microbiol. 13:814–35 [Google Scholar]
  82. Lin W, Fullner KJ, Clayton R, Sexton JA, Rogers MB. et al. 1999. Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. PNAS 96:1071–76 [Google Scholar]
  83. Liverman AD, Cheng HC, Trosky JE, Leung DW, Yarbrough ML. et al. 2007. Arp2/3-independent assembly of actin by Vibrio type III effector VopL. PNAS 104:17117–22 [Google Scholar]
  84. Loisel TP, Boujemaa R, Pantaloni D, Carlier MF. 1999. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401:613–16 [Google Scholar]
  85. Lossi NS, Rolhion N, Magee AI, Boyle C, Holden DW. 2008. The Salmonella SPI-2 effector SseJ exhibits eukaryotic activator-dependent phospholipase A and glycerophospholipid: cholesterol acyltransferase activity. Microbiology 154:2680–88 [Google Scholar]
  86. Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J. Cell Biol. 127:107–15 [Google Scholar]
  87. Machner MP, Isberg RR. 2007. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318:974–77 [Google Scholar]
  88. Madasu Y, Suarez C, Kast DJ, Kovar DR, Dominguez R. 2013. Rickettsia Sca2 has evolved formin-like activity through a different molecular mechanism. PNAS 110:E2677–86 [Google Scholar]
  89. McEwan DG, Popovic D, Gubas A, Terawaki S, Suzuki H. et al. 2015a. PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Mol. Cell 57:39–54 [Google Scholar]
  90. McEwan DG, Richter B, Claudi B, Wigge C, Wild P. et al. 2015b. PLEKHM1 regulates Salmonella-containing vacuole biogenesis and infection. Cell Host Microbe 17:58–71 [Google Scholar]
  91. McGhie EJ, Hayward RD, Koronakis V. 2001. Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J. 20:2131–39 [Google Scholar]
  92. McGhie EJ, Hayward RD, Koronakis V. 2004. Control of actin turnover by a Salmonella invasion protein. Mol. Cell 13:497–510 [Google Scholar]
  93. McGourty K, Thurston TL, Matthews SA, Pinaud L, Mota LJ, Holden DW. 2012. Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function. Science 338:963–67 [Google Scholar]
  94. Mesquita FS, Thomas M, Sachse M, Santos AJ, Figueira R, Holden DW. 2012. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLOS Pathog. 8:e1002743 [Google Scholar]
  95. Miki T, Akiba K, Iguchi M, Danbara H, Okada N. 2011. The Chromobacterium violaceum type III effector CopE, a guanine nucleotide exchange factor for Rac1 and Cdc42, is involved in bacterial invasion of epithelial cells and pathogenesis. Mol. Microbiol. 80:1186–203 [Google Scholar]
  96. Mohr C, Koch G, Just I, Aktories K. 1992. ADP-ribosylation by Clostridium botulinum C3 exoenzyme increases steady-state GTPase activities of recombinant rhoA and rhoB proteins. FEBS Lett. 297:95–99 [Google Scholar]
  97. Mostowy S, Bonazzi M, Hamon MA, Tham TN, Mallet A. et al. 2010. Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8:433–44 [Google Scholar]
  98. Mukhopadhyay S, Linstedt AD. 2013. Retrograde trafficking of AB5 toxins: mechanisms to therapeutics. J. Mol. Med. 91:1131–41 [Google Scholar]
  99. Muller MP, Peters H, Blumer J, Blankenfeldt W, Goody RS, Itzen A. 2010. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 329:946–49 [Google Scholar]
  100. Myeni SK, Zhou D. 2010. The C terminus of SipC binds and bundles F-actin to promote Salmonella invasion. J. Biol. Chem. 285:13357–63 [Google Scholar]
  101. Nagahama M, Ohkubo A, Oda M, Kobayashi K, Amimoto K. et al. 2011. Clostridium perfringens TpeL glycosylates the Rac and Ras subfamily proteins. Infect. Immun. 79:905–10 [Google Scholar]
  102. Namgoong S, Boczkowska M, Glista MJ, Winkelman JD, Rebowski G. et al. 2011. Mechanism of actin filament nucleation by Vibrio VopL and implications for tandem W domain nucleation. Nat. Struct. Mol. Biol. 18:1060–67 [Google Scholar]
  103. Nawabi P, Catron DM, Haldar K. 2008. Esterification of cholesterol by a type III secretion effector during intracellular Salmonella infection. Mol. Microbiol. 68:173–85 [Google Scholar]
  104. Neunuebel MR, Chen Y, Gaspar AH, Backlund PS Jr., Yergey A, Machner MP. 2011. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science 333:453–56 [Google Scholar]
  105. Neves D, Job V, Dortet L, Cossart P, Dessen A. 2013. Structure of internalin InlK from the human pathogen Listeria monocytogenes. J. Mol. Biol. 425:4520–29 [Google Scholar]
  106. Newton HJ, Kohler LJ, McDonough JA, Temoche-Diaz M, Crabill E. 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]
  107. Nishimura M, Fujii T, Hiyoshi H, Makino F, Inoue H. et al. 2015. A repeat unit of Vibrio diarrheal T3S effector subverts cytoskeletal actin homeostasis via binding to interstrand region of actin filaments. Sci. Rep. 5:10870 [Google Scholar]
  108. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. 2005. Escape of intracellular Shigella from autophagy. Science 307:727–31 [Google Scholar]
  109. Ohlson MB, Huang Z, Alto NM, Blanc MP, Dixon JE. et al. 2008. Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 4:434–46 [Google Scholar]
  110. Okada R, Zhou X, Hiyoshi H, Matsuda S, Chen X. et al. 2014. The Vibrio parahaemolyticus effector VopC mediates Cdc42-dependent invasion of cultured cells but is not required for pathogenicity in an animal model of infection. Cell. Microbiol. 16:938–47 [Google Scholar]
  111. Orchard RC, Kittisopikul M, Altschuler SJ, Wu LF, Suel GM, Alto NM. 2012. Identification of F-actin as the dynamic hub in a microbial-induced GTPase polarity circuit. Cell 148:803–15 [Google Scholar]
  112. Otomo T, Tomchick DR, Otomo C, Panchal SC, Machius M, Rosen MK. 2005. Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 433:488–94 [Google Scholar]
  113. Otto H, Tezcan-Merdol D, Girisch R, Haag F, Rhen M, Koch-Nolte F. 2000. The spvB gene-product of the Salmonella enterica virulence plasmid is a mono(ADP-ribosyl)transferase. Mol. Microbiol. 37:1106–15 [Google Scholar]
  114. Pollard TD, Blanchoin L, Mullins RD. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29:545–76 [Google Scholar]
  115. Popoff MR, Rubin EJ, Gill DM, Boquet P. 1988. Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect. Immun. 56:2299–306 [Google Scholar]
  116. Prashar A, Terebiznik MR. 2015. Legionella pneumophila: homeward bound away from the phagosome. Curr. Opin. Microbiol. 23:86–93 [Google Scholar]
  117. Prehna G, Ivanov MI, Bliska JB, Stebbins CE. 2006. Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126:869–80 [Google Scholar]
  118. Pujol C, Klein KA, Romanov GA, Palmer LE, Cirota C. et al. 2009. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect. Immun. 77:2251–61 [Google Scholar]
  119. Raju D, Hussey S, Ang M, Terebiznik MR, Sibony M. et al. 2012. Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans. Gastroenterology 142:1160–71 [Google Scholar]
  120. Reed SC, Lamason RL, Risca VI, Abernathy E, Welch MD. 2014. Rickettsia actin-based motility occurs in distinct phases mediated by different actin nucleators. Curr. Biol. 24:98–103 [Google Scholar]
  121. Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T. et al. 1999. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97:221–31 [Google Scholar]
  122. Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI. 2007. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell. Microbiol. 9:891–909 [Google Scholar]
  123. Roy CR, Cherfils J. 2015. Structure and function of Fic proteins. Nat. Rev. Microbiol. 13:631–40 [Google Scholar]
  124. Rudolph MG, Weise C, Mirold S, Hillenbrand B, Bader B. et al. 1999. Biochemical analysis of SopE from Salmonella typhimurium, a highly efficient guanosine nucleotide exchange factor for RhoGTPases. J. Biol. Chem. 274:30501–9 [Google Scholar]
  125. Ruiz-Albert J, Yu XJ, Beuzon CR, Blakey AN, Galyov EE, Holden DW. 2002. Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol. Microbiol. 44:645–61 [Google Scholar]
  126. Salcedo SP, Holden DW. 2003. SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J. 22:5003–14 [Google Scholar]
  127. Sallee NA, Rivera GM, Dueber JE, Vasilescu D, Mullins RD. et al. 2008. The pathogen protein EspFU hijacks actin polymerization using mimicry and multivalency. Nature 454:1005–8 [Google Scholar]
  128. Scheffzek K, Stephan I, Jensen ON, Illenberger D, Gierschik P. 2000. The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nat. Struct. Biol. 7:122–26 [Google Scholar]
  129. Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K. 1997. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387:725–29 [Google Scholar]
  130. Schroeder N, Henry T, de Chastellier C, Zhao W, Guilhon AA. et al. 2010. The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles. PLOS Pathog. 6:e1001002 [Google Scholar]
  131. Schroeder N, Mota LJ, Meresse S. 2011. Salmonella-induced tubular networks. Trends Microbiol. 19:268–77 [Google Scholar]
  132. Schuerch DW, Wilson-Kubalek EM, Tweten RK. 2005. Molecular basis of listeriolysin O pH dependence. PNAS 102:12537–42 [Google Scholar]
  133. Sehr P, Joseph G, Genth H, Just I, Pick E, Aktories K. 1998. Glucosylation and ADP ribosylation of Rho proteins: effects on nucleotide binding, GTPase activity, and effector coupling. Biochemistry 37:5296–304 [Google Scholar]
  134. Selyunin AS, Reddick LE, Weigele BA, Alto NM. 2014. Selective protection of an ARF1-GTP signaling axis by a bacterial scaffold induces bidirectional trafficking arrest. Cell Rep. 6:878–91 [Google Scholar]
  135. Selyunin AS, Sutton SE, Weigele BA, Reddick LE, Orchard RC. et al. 2011. The assembly of a GTPase-kinase signalling complex by a bacterial catalytic scaffold. Nature 469:107–11 [Google Scholar]
  136. Shahnazari S, Namolovan A, Mogridge J, Kim PK, Brumell JH. 2011. Bacterial toxins can inhibit host cell autophagy through cAMP generation. Autophagy 7:957–65 [Google Scholar]
  137. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575–88 [Google Scholar]
  138. Shin DM, Jeon BY, Lee HM, Jin HS, Yuk JM. et al. 2010. Mycobacterium tuberculosis Eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLOS Pathog. 6:e1001230 [Google Scholar]
  139. Simpson LL, Stiles BG, Zepeda H, Wilkins TD. 1989. Production by Clostridium spiroforme of an iotalike toxin that possesses mono(ADP-ribosyl)transferase activity: identification of a novel class of ADP-ribosyltransferases. Infect. Immun. 57:255–61 [Google Scholar]
  140. Spiering D, Hodgson L. 2011. Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh. Migr. 5:170–80 [Google Scholar]
  141. Sreelatha A, Bennett TL, Zheng H, Jiang QX, Orth K, Starai VJ. 2013. Vibrio effector protein, VopQ, forms a lysosomal gated channel that disrupts host ion homeostasis and autophagic flux. PNAS 110:11559–64 [Google Scholar]
  142. Stamm LM, Morisaki JH, Gao LY, Jeng RL, McDonald KL. et al. 2003. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J. Exp. Med. 198:1361–68 [Google Scholar]
  143. Starr T, Child R, Wehrly TD, Hansen B, Hwang S. et al. 2012. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11:33–45 [Google Scholar]
  144. Stebbins CE, Galan JE. 2000. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6:1449–60 [Google Scholar]
  145. Stender S, Friebel A, Linder S, Rohde M, Mirold S, Hardt WD. 2000. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36:1206–21 [Google Scholar]
  146. Stevens MP, Friebel A, Taylor LA, Wood MW, Brown PJ. et al. 2003. A Burkholderia pseudomallei type III secreted protein, BopE, facilitates bacterial invasion of epithelial cells and exhibits guanine nucleotide exchange factor activity. J. Bacteriol. 185:4992–96 [Google Scholar]
  147. Stiles BG, Wilkins TD. 1986. Clostridium perfringens iota toxin: synergism between two proteins. Toxicon 24:767–73 [Google Scholar]
  148. Sundin C, Henriksson ML, Hallberg B, Forsberg A, Frithz-Lindsten E. 2001. Exoenzyme T of Pseudomonas aeruginosa elicits cytotoxicity without interfering with Ras signal transduction. Cell. Microbiol. 3:237–46 [Google Scholar]
  149. Tan Y, Arnold RJ, Luo ZQ. 2011. Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination. PNAS 108:21212–17 [Google Scholar]
  150. Tan Y, Luo ZQ. 2011. Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 475:506–9 [Google Scholar]
  151. Tattoli I, Sorbara MT, Yang C, Tooze SA, Philpott DJ, Girardin SE. 2013. Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBO J. 32:3066–78 [Google Scholar]
  152. Tattoli I, Travassos LH, Carneiro LA, Magalhaes JG, Girardin SE. 2007. The Nodosome: Nod1 and Nod2 control bacterial infections and inflammation. Semin. Immunopathol. 29:289–301 [Google Scholar]
  153. Thomas M, Mesquita FS, Holden DW. 2012. The DUB-ious lack of ALIS in Salmonella infection: A Salmonella deubiquitinase regulates the autophagy of protein aggregates. Autophagy 8:1824–26 [Google Scholar]
  154. Van Engelenburg SB, Palmer AE. 2008. Quantification of real-time Salmonella effector type III secretion kinetics reveals differential secretion rates for SopE2 and SptP. Chem. Biol. 15:619–28 [Google Scholar]
  155. van Schaik EJ, Chen C, Mertens K, Weber MM, Samuel JE. 2013. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nat. Rev. Microbiol. 11:561–73 [Google Scholar]
  156. Vazquez CL, Colombo MI. 2010. Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ. 17:421–38 [Google Scholar]
  157. von Eichel–Streiber C, Boquet P, Sauerborn M, Thelestam M. 1996. Large clostridial cytotoxins—a family of glycosyltransferases modifying small GTP-binding proteins. Trends Microbiol. 4:375–82 [Google Scholar]
  158. Welch MD, Iwamatsu A, Mitchison TJ. 1997. Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385:265–69 [Google Scholar]
  159. Wilde C, Chhatwal GS, Schmalzing G, Aktories K, Just I. 2001. A novel C3-like ADP-ribosyltransferase from Staphylococcus aureus modifying RhoE and Rnd3. J. Biol. Chem. 276:9537–42 [Google Scholar]
  160. Winchell CG, Graham JG, Kurten RC, Voth DE. 2014. Coxiella burnetii type IV secretion-dependent recruitment of macrophage autophagosomes. Infect. Immun. 82:2229–38 [Google Scholar]
  161. Winnen B, Schlumberger MC, Sturm A, Schupbach K, Siebenmann S. et al. 2008. Hierarchical effector protein transport by the Salmonella Typhimurium SPI-1 type III secretion system. PLOS ONE 3:e2178 [Google Scholar]
  162. Xu H, Yang J, Gao W, Li L, Li P. et al. 2014. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513:237–41 [Google Scholar]
  163. Yang J, Zhang Z, Roe SM, Marshall CJ, Barford D. 2009. Activation of Rho GTPases by DOCK exchange factors is mediated by a nucleotide sensor. Science 325:1398–402 [Google Scholar]
  164. Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K. 2009. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323:269–72 [Google Scholar]
  165. Yasir M, Pachikara ND, Bao X, Pan Z, Fan H. 2011. Regulation of chlamydial infection by host autophagy and vacuolar ATPase-bearing organelles. Infect. Immun. 794019–28 [Google Scholar]
  166. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M. et al. 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11:1233–40 [Google Scholar]
  167. Yu B, Cheng HC, Brautigam CA, Tomchick DR, Rosen MK. 2011. Mechanism of actin filament nucleation by the bacterial effector VopL. Nat. Struct. Mol. Biol. 18:1068–74 [Google Scholar]
  168. Yu B, Martins IR, Li P, Amarasinghe GK, Umetani J. et al. 2010. Structural and energetic mechanisms of cooperative autoinhibition and activation of Vav1. Cell 140:246–56 [Google Scholar]
  169. Yu Y, Fang L, Zhang Y, Sheng H, Fang W. 2015. VgrG2 of type VI secretion system 2 of Vibrio parahaemolyticus induces autophagy in macrophages. Front. Microbiol. 6:168 [Google Scholar]
  170. Zahm JA, Padrick SB, Chen Z, Pak CW, Yunus AA. et al. 2013. The bacterial effector VopL organizes actin into filament-like structures. Cell 155:423–34 [Google Scholar]
  171. Zekarias B, Mattoo S, Worby C, Lehmann J, Rosenbusch RF, Corbeil LB. 2010. Histophilus somni IbpA DR2/Fic in virulence and immunoprotection at the natural host alveolar epithelial barrier. Infect. Immun. 78:1850–58 [Google Scholar]
  172. Zhou D, Mooseker MS, Galan JE. 1999. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283:2092–95 [Google Scholar]
  173. Zhou X, Konkel ME, Call DR. 2010. Vp1659 is a Vibrio parahaemolyticus type III secretion system 1 protein that contributes to translocation of effector proteins needed to induce cytolysis, autophagy, and disruption of actin structure in HeLa cells. J. Bacteriol. 192:3491–502 [Google Scholar]
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