SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells

Traffic

Volumn 4, Issue 1, 2003, Pages 36-48

  Brumell, John H ^a   Kujat Choy, Sonya ^a   Brown, Nat F ^a   Vallance, Bruce A ^a   Knodler, Leigh A ^a   Finlay, B Brett ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Endosome; Lysosome; Microbial pathogenesis; SopD; Type III secretion

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN SOPD2; RAB PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL SALMONELLOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; GENE DISRUPTION; GENETIC CONSERVATION; HELA CELL; HOST CELL; HUMAN; HUMAN CELL; LETHAL DOSE; LYSOSOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; SURVIVAL TIME;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TIME FACTORS; TRANSPORT VESICLES;

EID: 0038782812     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0854.2003.40106.x     Document Type: Article

References (69)

1. Jones BD, Falkow S. Salmonellosis. host immune responses and bacterial virulence determinants. Annu Rev Immunol 1996;14:533-561.
2. Tsolis RM, Kingsley RA, Townsend SM, Ficht TA, Adams LG, Baumler AJ. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 1999;473: 261-274.
3. Richter-Dahlfors A, Buchan AMJ, Finlay BB. Murine salmonellosis studied by confocal microscopy. Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 1997;186:569-580.
4. Salcedo SP, Noursadeghi M, Cohen J, Holden DW. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol 2001;3:587-597.
5. Duclos S, Desjardins M. Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2000;2:365-377.
6. Brumell JH, Perrin AJ, Goosney DL, Finlay BB. Microbial pathogenesis: new niches for Salmonella. Curr Biol 2002;12:R15-R17.
7. Holden DW. Trafficking of the Salmonella vacuole in macrophages. Traffic 2002;3:161-169.
8. Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC, Mastroeni P, Fang FC. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxicase. Science 2000;287:1655-1658.
9. Vazquez-Torres A, Fantuzzi G, Edwards CK, 3rd, Dinarello CA, Fang FC. Defective localization of the NADPH phagocyte oxidase to Salmonella-containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages. Proc Natl Acad Sci USA 2001;98:2561-2565.
10. Garcia-del Portillo F, Finlay BB. Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 1995:129:81-97.
11. Meresse S, Steele-Mortimer O, Finlay BB, Gorvel JP. The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 1999;18:4394-4403.
12. Steele-Mortimer OM, Méresse S, Gorvel J-P, Toh B-H, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1999:1:33-51.
13. Baldeon ME, Ceresa BP, Casanova JE. Expression of constitutively active Rab5 uncouples maturation of the Salmonella-containing vacuole from intracellular replication. Cell Microbiol 2001;3:473-486.
14. Brumell JH, Tang P, Mills SD, Finlay BB. Characterization of Salmonella-induced filaments (Sifs) reveals a delayed interaction between Salmonella-containing vacuoles and late endocytic compartments. Traffic 2001;2:643-653.
15. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB. Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci USA 1993;90:10544-10548.
16. Stein MA, Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol 1996;20:151-164.
17. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2000;2:145-156.
18. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, Hedges S, Wallis TS. A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 1997;25:903-912.
19. Jones MA, Wood MW, Mullan PB, Watson PR, Wallis TS, Galyov EE. Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 1998;66:5799-5804.
20. Wallis TS, Wood M, Watson P, Paulin S, Jones M, Galyov E. Sips, Sops, and SPIs but not stn influence Salmonella enteropathogenesis. Adv Exp Med Biol 1999;473:275-280.
21. Watson PR, Galyov EE, Paulin SM, Jones PW, Wallis TS. Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect Immun 1998;66:1432-1438.
22. Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, Galyov EE. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 1998;29:883-891.
23. Galan JE, Curtiss RD. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 1989;86:6383-6387.
24. Galan JE, Zhou D. Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci USA 2000;97:8754-8761.
25. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, Finlay BB. The invasion-associated type III secretion system of Salmonella enterica serovar typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol 2002;4:43-54.
26. Cirillo DM, Valdivia RH, Monack DM, Falkow S. Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival [In Process Citation]. Mol Microbiol 1998:30:175-188.
27. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW. Simultaneous identification of bacterial virulence genes by negative selection. Science 1995;269:400-403.
28. Hensel M, Shea JE, Raupach B, Monack D, Falkow S, Gleeson C, Kubo T, Holden DW. Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol Microbiol 1997;24:155-167.
29. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, Vazquez-Torres A, Glesson C, Fang FC, Holden DW. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages [In Process Citation]. Mol Microbiol 1998:30:163-174.
30. Ochman H, Soncini FC, Solomon F, Groisman EA. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 1996;93:7800-7804.
31. Pfeifer CG, Marcus SL, Steele-Mortimer O, Knodler LA, Finlay BB. Salmonella typhimurium virulence genes are induced upon bacterial invasion into phagocytic and nonphagocytic cells. Infect Immun 1999;67:5690-5698.
32. Shea JE, Hensel M, Gleason C, Holden DW. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Aced Sci USA 1996;93:2593-2597.
33. Shea JE, Beuzon CR, Gleason C, Mundy R, Holden DW. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 1999;67:213-219.
34. Beuzon CR, Banks G, Deiwick J, Hensel M, Holden DW. pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol Microbiol 1999;33:806-816.
35. Hansen-Wester I, Stecher B, Hensel M. Type III secretion of Salmonella enterica serovar typhimurium translocated effectors and SseFG. Infect Immun 2002;70:1403-1409.
36. Nikolaus T, Deiwick J, Rappl C, Freeman JA, Schroder W, Miller SI, Hensel M. SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J Bacteriol 2001;183:6036-6045.
37. Miao EA, Scherer CA, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ, Miller SI. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 1999;34:850-864.
38. Miao EA, Miller SI. A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc Natl Acad Sci USA 2000;97:7539-7544.
39. Brumell JH, Goosney DL, Finlay BB. SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 2002;3:407-415.
40. Brumell JH, Rosenberger CM, Gotto GT, Marcus SL, Finlay BB. SifA permits survival and replication of Salmonella typhimurium in murine macrophages. Cell Microbiol 2001;3:75-84.
41. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, Waterman SR, Ryder TA, Boucrot E, Holden DW. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 2000;19:3235-3249.
42. Knodler LA, Celli J, Hardt WD, Vallance BA, Yip C, Finlay BB. Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol Microbiol 2002;43:1089-1103.
43. Brumell JH, Marcus SL, Finlay BB. N-terminal conservation of putative type III secreted effectors of Salmonella typhimurium. Mol Micro 2000;36:773-774.
44. Guy RL, Gonias LA, Stein MA. Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region. Mol Microbiol 2000;37:1417-1435.
45. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Da F, Hou S, Layman D, Leonard S, Nguyen C, Scott K. Complete genome sequence of Salmonella enterica serovar typhimurium LT2. Nature 2001;413:852-856.
46. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia H, Baker S, Basham D, Brooks K, Chillingworth T. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001;413:848-852.
47. Worley MJ, Ching KH, Heffron F. Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 2000;36:749-761.
48. Groisman EA. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 2001;183:1835-1842.
49. Eichelberg K, Galan JE. Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1) - encoded transcriptional activators InvF and hilA. Infect Immun 1999:67:4099-4105.
50. Bajaj V, Lucas RL, Hwang C, Lee CA. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 1996;22:703-714.
51. Darwin KH, Miller VL. The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes. Mol Microbiol 2000;35:949-960.
52. Deiwick J, Nikolaus T, Erdogan S, Hensel M. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 1999;31:1759-73.
53. Martinez-Lorenzo MJ, Meresse S, de Chastellier C, Gorvel JP. Unusual intracellular trafficking of Salmonella typhimurium in human melanoma cells. Cell Microbiol 2001;3:407-416.
54. Rosenberger C, Finlay BB. Macrophages inhibit Salmonella typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J Biol Chem 2002;277:18753-18762.
55. Gauthier A, de Grado M, Finlay BB. Mechanical fractionation reveals structural requirements for enteropathogenic Escherichia coli Tir insertion into host membranes. Infect Immun 2000;68:4344-4348.
56. Somsel Rodman J, Wandinger-Ness A. Rab GTPases coordinate endocytosis. J Cell Sci 2000;113:183-192.
57. Feng Y, Press B, Wandinger-Ness A. Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 1995;131:1435-1452.
58. Feng Y, Press B, Chen W, Zimmerman J, Wandinger-Ness A. Expression and properties of Rab7 in endosome function. Meth Enzymol 2001;329:175-187.
59. Press B, Feng Y, Hoflack B, Wandinger-Ness A. Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J Cell Biol 1998;140:1075-1089.
60. Garvis SG, Beuzon CR, Holden DW. A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol 2001;3:731-744.
61. Ruiz-Albert JYUXJ, Beuzon CR, Blakey AN, Galyov EE, Holden DW. Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 2002; 44:645-661.
62. Bispham J, Tripathi BN, Watson PR, Wallis TS. Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect Immun 2001;69:367-377.
63. Tsolis RM, Adams LG, Ficht TA, Baumler AJ. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 1999:67:4879-4885.
64. Fields PI, Groisman EA, Heffron FA Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 1989;243:1059-1062.
65. Edwards RA, Keller LH, Schifferli DM. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 1998;207:149-157.
66. Miller VL, Mekalanos JJ. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 1988:170:2575-2583.
67. Celli J, Trieu-Cuot P. Circularization of Tn916 is required for expression of the transposon-encoded transfer functions: characterization of long tetracycline-inducible transcripts reading through the attachment site. Mol Microbiol 1998;28:103-117.
68. Carlsson SR, Roth J, Piller F, Fukuda M. Isolation and characterization of human lysosomal membrane glycoproteins, h-Lamp-1 and h-Lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan. J Biol Chem 1988;263:18911-18919.
69. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 1998;392:193-197.