A Translocated Effector Required for Bartonella Dissemination from Derma to Blood Safeguards Migratory Host Cells from Damage by Co-translocated Effectors

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Okujava, Rusudan ^a   Guye, Patrick ^a,e   Lu, Yun Yueh ^a   Mistl, Claudia ^a   Polus, Florine ^a,f   Vayssier Taussat, Muriel ^b   Halin, Cornelia ^c   Rolink, Antonius G ^d   Dehio, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b CEMAGREF   (France)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BARTONELLA EFFECTOR PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL TRANSMISSION; BARTONELLA; BARTONELLA HENSELAE; CELL CULTURE; CELL DAMAGE; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE CARRIER; FEMALE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOFLUORESCENCE TEST; NONHUMAN; PARASITE MIGRATION; PHENOTYPE; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; TIME-LAPSE VIDEO MICROSCOPY; TYPE IV SECRETION SYSTEM; UMBILICAL VEIN ENDOTHELIAL CELL; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ZOONOSIS; ACTIN FILAMENT; ANIMAL; BACTERIAL SECRETION SYSTEM; BAGG ALBINO MOUSE; BARTONELLOSIS; BONE MARROW CELL; CELL MOTION; CYTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; WISTAR RAT;

ACTIN CYTOSKELETON; ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BARTONELLA; BARTONELLA INFECTIONS; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; CYTOPROTECTION; DENDRITIC CELLS; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VIRULENCE FACTORS;

EID: 84903472801     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004187     Document Type: Article

References (64)

1. Monack DM, Mueller A, Falkow S, (2004) Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2: 747-765.
2. Lee KS, Kalantzis A, Jackson CB, O'Connor L, Murata-Kamiya N, et al. (2012) Helicobacter pylori CagA triggers expression of the bactericidal lectin REG3gamma via gastric STAT3 activation. PLoS One 7: e30786.
3. Kido M, Watanabe N, Aoki N, Iwamoto S, Nishiura H, et al. (2011) Dual roles of CagA protein in Helicobacterpylori-induced chronic gastritis in mice. Biochem Biophys Res Commun 412: 266-272.
4. Schroeder GN, Hilbi H, (2008) Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev 21: 134-156.
5. Diacovich L, Gorvel JP, (2010) Bacterial manipulation of innate immunity to promote infection. Nat Rev Microbiol 8: 117-128.
6. Shames SR, Finlay BB, (2012) Bacterial effector interplay: a new way to view effector function. Trends Microbiol 20: 214-219.
7. Chomel BB, Boulouis HJ, Maruyama S, Breitschwerdt EB, (2006) Bartonella spp. in pets and effect on human health. Emerg Infect Dis 12: 389-394.
8. Boulouis HJ, Chang CC, Henn JB, Kasten RW, Chomel BB, (2005) Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet Res 36: 383-410.
9. Chomel BB, Boulouis HJ, Breitschwerdt EB, Kasten RW, Vayssier-Taussat M, et al. (2009) Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 40: 29.
10. Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR, (2010) Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care (San Antonio) 20: 8-30.
11. Dehio C, (2004) Molecular and cellular basis of bartonella pathogenesis. Annu Rev Microbiol 58: 365-390.
12. Foil L, Andress E, Freeland RL, Roy AF, Rutledge R, et al. (1998) Experimental infection of domestic cats with Bartonella henselae by inoculation of Ctenocephalides felis (Siphonaptera: Pulicidae) feces. J Med Entomol 35: 625-628.
13. Raoult D, Aboudharam G, Crubezy E, Larrouy G, Ludes B, et al. (2000) Molecular identification by "suicide PCR" of Yersinia pestis as the agent of medieval black death. Proc Natl Acad Sci U S A 97: 12800-12803.
14. Schulein R, Seubert A, Gille C, Lanz C, Hansmann Y, et al. (2001) Invasion and persistent intracellular colonization of erythrocytes. A unique parasitic strategy of the emerging pathogen Bartonella. J Exp Med 193: 1077-1086.
15. Engel P, Salzburger W, Liesch M, Chang CC, Maruyama S, 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.
16. Seubert A, Hiestand R, de la Cruz F, Dehio C, (2003) A bacterial conjugation machinery recruited for pathogenesis. Mol Microbiol 49: 1253-1266.
17. Schulein R, Dehio C, (2002) The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol Microbiol 46: 1053-1067.
18. Dehio C, (2008) Infection-associated type IV secretion systems of Bartonella and their diverse roles in host cell interaction. Cell Microbiol 10: 1591-1598.
19. Vayssier-Taussat M, Le Rhun D, Deng HK, Biville F, Cescau S, et al. (2010) The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 6: e1000946.
20. Nystedt B, Frank AC, Thollesson M, Andersson SG, (2008) Diversifying selection and concerted evolution of a type IV secretion system in Bartonella. Mol Biol Evol 25: 287-300.
21. Schulein R, Guye P, Rhomberg TA, Schmid MC, Schroder G, et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 102: 856-861.
22. Selbach M, Paul FE, Brandt S, Guye P, Daumke O, et al. (2009) Host cell interactome of tyrosine-phosphorylated bacterial proteins. Cell Host Microbe 5: 397-403.
23. Schmid MC, Schulein R, Dehio M, Denecker G, Carena I, et al. (2004) The VirB type IV secretion system of Bartonella henselae mediates invasion, proinflammatory activation and antiapoptotic protection of endothelial cells. Mol Microbiol 52: 81-92.
24. Rhomberg TA, Truttmann MC, Guye P, Ellner Y, Dehio C, (2009) A translocated protein of Bartonella henselae interferes with endocytic uptake of individual bacteria and triggers uptake of large bacterial aggregates via the invasome. Cell Microbiol 11: 927-945.
25. Schmid MC, Scheidegger F, Dehio M, Balmelle-Devaux N, Schulein R, et al. (2006) A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog 2: e115.
26. Dehio C, Meyer M, Berger J, Schwarz H, Lanz C, (1997) Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 110 (Pt 18) (): 2141-2154.
27. Truttmann MC, Rhomberg TA, Dehio C, (2011) Combined action of the type IV secretion effector proteins BepC and BepF promotes invasome formation of Bartonella henselae on endothelial and epithelial cells. Cell Microbiol 13: 284-299.
28. Iwanicki MP, Vomastek T, Tilghman RW, Martin KH, Banerjee J, et al. (2008) FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J Cell Sci 121: 895-905.
29. Rid R, Schiefermeier N, Grigoriev I, Small JV, Kaverina I, (2005) The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil Cytoskeleton 61: 161-171.
30. Worthylake RA, Lemoine S, Watson JM, Burridge K, (2001) RhoA is required for monocyte tail retraction during transendothelial migration. J Cell Biol 154: 147-160.
31. Heasman SJ, Carlin LM, Cox S, Ng T, Ridley AJ, (2010) Coordinated RhoA signaling at the leading edge and uropod is required for T cell transendothelial migration. J Cell Biol 190: 553-563.
32. Fan H, Hall P, Santos LL, Gregory JL, Fingerle-Rowson G, et al. (2011) Macrophage migration inhibitory factor and CD74 regulate macrophage chemotactic responses via MAPK and Rho GTPase. J Immunol 186: 4915-4924.
33. Kim MJ, Kim S, Kim Y, Jin EJ, Sonn JK, (2012) Inhibition of RhoA but not ROCK induces chondrogenesis of chick limb mesenchymal cells. Biochem Biophys Res Commun 418: 500-505.
34. Aktories K, Wilde C, Vogelsgesang M, (2004) Rho-modifying C3-like ADP-ribosyltransferases. Rev Physiol Biochem Pharmacol 152: 1-22.
35. Groeger G, Nobes CD, (2007) Co-operative Cdc42 and Rho signalling mediates ephrinB-triggered endothelial cell retraction. Biochem J 404: 23-29.
36. Marignac G, Barrat F, Chomel B, Vayssier-Taussat M, Gandoin C, et al. (2010) Murine model for Bartonella birtlesii infection: New aspects. Comp Immunol Microbiol Infect Dis 33: 95-107.
37. Savina A, Amigorena S, (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 219: 143-156.
38. Shortman K, Naik SH, (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7: 19-30.
39. Skinner JA, Pilione MR, Shen H, Harvill ET, Yuk MH, (2005) Bordetella type III secretion modulates dendritic cell migration resulting in immunosuppression and bacterial persistence. J Immunol 175: 4647-4652.
40. Zlokarnik G, Negulescu PA, Knapp TE, Mere L, Burres N, et al. (1998) Quantitation of transcription and clonal selection of single living cells with beta-lactamase as reporter. Science 279: 84-88.
41. Shields JD, Fleury ME, Yong C, Tomei AA, Randolph GJ, et al. (2007) Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11: 526-538.
42. Edelman GM, Gally JA, (2001) Degeneracy and complexity in biological systems. Proc Natl Acad Sci U S A 98: 13763-13768.
43. Larsen M, Tremblay ML, Yamada KM, (2003) Phosphatases in cell-matrix adhesion and migration. Nat Rev Mol Cell Biol 4: 700-711.
44. Lamalice L, Le Boeuf F, Huot J, (2007) Endothelial cell migration during angiogenesis. Circ Res 100: 782-794.
45. Insall RH, Machesky LM, (2009) Actin dynamics at the leading edge: from simple machinery to complex networks. Dev Cell 17: 310-322.
46. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G, (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305: 1782-1786.
47. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B, (2003) Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116: 4605-4613.
48. Wood W, Martin P, (2002) Structures in focus-filopodia. Int J Biochem Cell Biol 34: 726-730.
49. Miao L, Vanderlinde O, Stewart M, Roberts TM, (2003) Retraction in amoeboid cell motility powered by cytoskeletal dynamics. Science 302: 1405-1407.
50. Jermy A, (2011) Bacterial pathogenesis: legionella effector under friendly fire. Nat Rev Microbiol 9: 80.
51. Chaturvedi LS, Marsh HM, Basson MD, (2011) Role of RhoA and its effectors ROCK and mDia1 in the modulation of deformation-induced FAK, ERK, p38, and MLC motogenic signals in human Caco-2 intestinal epithelial cells. Am J Physiol Cell Physiol 301: C1224-1238.
52. Narumiya S, Tanji M, Ishizaki T, (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 28: 65-76.
53. Kubori T, Galan JE, (2003) Temporal regulation of salmonella virulence effector function by proteasome-dependent protein degradation. Cell 115: 333-342.
54. Ingmundson A, Delprato A, Lambright DG, Roy CR, (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
55. Saenz HL, Engel P, Stoeckli MC, Lanz C, Raddatz G, et al. (2007) Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat Genet 39: 1469-1476.
56. Koesling J, Aebischer T, Falch C, Schulein R, Dehio C, (2001) Cutting edge: antibody-mediated cessation of hemotropic infection by the intraerythrocytic mouse pathogen Bartonella grahamii. J Immunol 167: 11-14.
57. Lopez-Bravo M, Ardavin C, (2008) In vivo induction of immune responses to pathogens by conventional dendritic cells. Immunity 29: 343-351.
58. Randolph GJ, Ochando J, Partida-Sanchez S, (2008) Migration of dendritic cell subsets and their precursors. Annu Rev Immunol 26: 293-316.
59. Alvarez D, Vollmann EH, von Andrian UH, (2008) Mechanisms and consequences of dendritic cell migration. Immunity 29: 325-342.
60. Gorvel JP, (2008) Brucella: a Mr "Hide" converted into Dr Jekyll. Microbes Infect 10: 1010-1013.
61. Salcedo SP, Marchesini MI, Lelouard H, Fugier E, Jolly G, et al. (2008) Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog 4: e21.
62. Dehio M, Knorre A, Lanz C, Dehio C, (1998) Construction of versatile high-level expression vectors for Bartonella henselae and the use of green fluorescent protein as a new expression marker. Gene 215: 223-229.
63. Brasel K, De Smedt T, Smith JL, Maliszewski CR, (2000) Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 96: 3029-3039.
64. Vigl B, Aebischer D, Nitschke M, Iolyeva M, Rothlin T, et al. (2011) Tissue inflammation modulates gene expression of lymphatic endothelial cells and dendritic cell migration in a stimulus-dependent manner. Blood 118: 205-215.