Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival

Microbial Pathogenesis

Volumn 52, Issue 6, 2012, Pages 367-374

  Rosales Reyes, Roberto ^a   Pérez López, Araceli ^a,c   Sánchez Gómez, Concepción ^d   Hernández Mote, Rosaura Ruth ^d   Castro Eguiluz, Denisse ^c   Ortiz Navarrete, Vianney ^c   Alpuche Aranda, Celia Mercedes ^a,b,e  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Instituto Nacional de Referencia Epidemiológica   (Mexico)

^c DEPARTAMENTO DE FÍSICA   (Mexico)

^d HOSPITAL INFANTIL DE MÉXICO FEDERICO GÓMEZ   (Mexico)

^e Instituto Nacional de Diagnostico y Referencia Epidemiologicos   (Mexico)

Author keywords

B cells; Macropinocytosis; Pyroptosis; Salmonella; SPI 1

Indexed keywords

ACTIN; INTERLEUKIN 1BETA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; CELL DEATH; CELL INVASION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HOST PATHOGEN INTERACTION; MICROTUBULE; MOUSE; NONHUMAN; PATHOGENICITY ISLAND; PHAGOSOME; PINOCYTOSIS; PRIORITY JOURNAL; SALMONELLA; SALMONELLOSIS;

ACTINS; ANIMALS; B-LYMPHOCYTES; BACTERIAL PROTEINS; CELLS, CULTURED; FEMALE; HOST-PATHOGEN INTERACTIONS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICROTUBULES; PHAGOSOMES; PINOCYTOSIS; SALMONELLA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); SALMONELLA;

EID: 84860340540     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2012.03.007     Document Type: Article

References (43)

1. Haraga A., Ohlson M.B., Miller S.I. Salmonellae interplay with host cells. Nat Rev Microbiol 2008, 6:53-66.
2. Francis C.L., Ryan T.A., Jones B.D., Smith S.J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 1993, 364:639-642.
3. Jones B.D., Paterson H.F., Hall A., Falkow S. Salmonella typhimurium induces membrane ruffling by a growth factor-receptor-independent mechanism. Proc Natl Acad Sci U S A 1993, 90:10390-10394.
4. Mills S.D., Finlay B.B. Comparison of Salmonella typhi and Salmonella typhimurium invasion, intracellular growth and localization in cultured human epithelial cells. Microb Pathog 1994, 17:409-423.
5. Jepson M.A., Clark M.A. The role of M cells in Salmonella infection. Microbes Infect 2001, 3:1183-1190.
6. Alpuche-Aranda C.M., Berthiaume E.P., Mock B., Swanson J.A., Miller S.I. Spacious phagosome formation within mouse macrophages correlates with Salmonella serotype pathogenicity and host susceptibility. Infect Immun 1995, 63:4456-4462.
7. Alpuche-Aranda C.M., Racoosin E.L., Swanson J.A., Miller S.I. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med 1994, 179:601-608.
8. Steele-Mortimer O. The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 2008, 11:38-45.
9. Vazquez-Torres A., Xu Y., Jones-Carson J., Holden D.W., Lucia S.M., Dinauer M.C., et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 2000, 287:1655-1658.
10. Chakravortty D., Hansen-Wester I., Hensel M. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 2002, 195:1155-1166.
11. Groisman E.A., Chiao E., Lipps C.J., Heffron F. Salmonella typhimurium PhoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci U S A 1989, 86:7077-7081.
12. Miller S.I., Kukral A.M., Mekalanos J.J. A two-component regulatory system (PhoP PhoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 1989, 86:5054-5058.
13. Monack D.M., Mueller A., Falkow S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol 2004, 2:747-765.
14. Monack D.M., Navarre W.W., Falkow S. Salmonella-induced macrophage death: the role of caspase-1 in death and inflammation. Microbes Infect 2001, 3:1201-1212.
15. Miller S.I., Mekalanos J.J. Constitutive expression of the PhoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 1990, 172:2485-2490.
16. Monack D.M., Hersh D., Ghori N., Bouley D., Zychlinsky A., Falkow S. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 2000, 192:249-258.
17. Monack D.M., Raupach B., Hromockyj A.E., Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci U S A 1996, 93:9833-9838.
18. Fink S.L., Cookson B.T. Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 2007, 9:2562-2570.
19. Rosales-Reyes R., Alpuche-Aranda C., Ramirez-Aguilar Mde L., Castro-Eguiluz A.D., Ortiz-Navarrete V. Survival of Salmonella enterica serovar Typhimurium within late endosomal-lysosomal compartments of B lymphocytes is associated with the inability to use the vacuolar alternative major histocompatibility complex class I antigen-processing pathway. Infect Immun 2005, 73:3937-3944.
20. Castro-Eguiluz D., Pelayo R., Rosales-Garcia V., Rosales-Reyes R., Alpuche-Aranda C., Ortiz-Navarrete V. B cell precursors are targets for Salmonella infection. Microb Pathog 2009, 47:52-56.
21. Rodriguez-Pinto D. B cells as antigen presenting cells. Cell Immunol 2005, 238:67-75.
22. Vidard L., Kovacsovics-Bankowski M., Kraeft S.K., Chen L.B., Benacerraf B., Rock K.L. Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J Immunol 1996, 156:2809-2818.
23. Verjans G.M., Ringrose J.H., van Alphen L., Feltkamp T.E., Kusters J.G. Entrance and survival of Salmonella typhimurium and Yersinia enterocolitica within human B- and T-cell lines. Infect Immun 1994, 62:2229-2235.
24. Racoosin E.L., Swanson J.A. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci 1992, 102(Pt 4):867-880.
25. Darwin K.H., Miller V.L. InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in Salmonella typhimurium. J Bacteriol 1999, 181:4949-4954.
26. Marlovits T.C., Kubori T., Lara-Tejero M., Thomas D., Unger V.M., Galan J.E. Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 2006, 441:637-640.
27. Brennan M.A., Cookson B.T. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 2000, 38:31-40.
28. Guiney D.G. The role of host cell death in Salmonella infections. Curr Top Microbiol Immunol 2005, 289:131-150.
29. Geddes K., Cruz F., Heffron F. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog 2007, 3:e196.
30. Souwer Y., Griekspoor A., Jorritsma T., de Wit J., Janssen H., Neefjes J., et al. B cell receptor-mediated internalization of salmonella: a novel pathway for autonomous B cell activation and antibody production. J Immunol 2009, 182:7473-7481.
31. Sztein M.B., Tanner M.K., Polotsky Y., Orenstein J.M., Levine M.M. Cytotoxic T lymphocytes after oral immunization with attenuated vaccine strains of Salmonella typhi in humans. J Immunol 1995, 155:3987-3993.
32. Ugrinovic S., Menager N., Goh N., Mastroeni P. Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun 2003, 71:6808-6819.
33. Yrlid U., Svensson M., Hakansson A., Chambers B.J., Ljunggren H.G., Wick M.J. In vivo activation of dendritic cells and T cells during Salmonella enterica serovar Typhimurium infection. Infect Immun 2001, 69:5726-5735.
34. Kim K.J., Kanellopoulos-Langevin C., Merwin R.M., Sachs D.H., Asofsky R. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J Immunol 1979, 122:549-554.
35. Patel J.C., Galan J.E. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr Opin Microbiol 2005, 8:10-15.
36. Bueno S.M., Wozniak A., Leiva E.D., Riquelme S.A., Carreno L.J., Hardt W.D., et al. Salmonella pathogenicity island 1 differentially modulates bacterial entry to dendritic and non-phagocytic cells. Immunology 2010, 130:273-287.
37. Cooper K.G., Winfree S., Malik-Kale P., Jolly C., Ireland R., Knodler L.A., et al. Activation of Akt by the bacterial inositol phosphatase, SopB, is wortmannin insensitive. PLoS One 2011, 6:e22260.
38. Bergsbaken T., Fink S.L., Cookson B.T. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009, 7:99-109.
39. Chen L.M., Kaniga K., Galan J.E. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 1996, 21:1101-1115.
40. McElroy D.S., Ashley T.J., D'Orazio S.E. Lymphocytes serve as a reservoir for Listeria monocytogenes growth during infection of mice. Microb Pathog 2009, 46:214-221.
41. Lombardi G., del Gallo F., Vismara D., Piccolella E., de Martino C., Garzelli C., et al. Epstein-Barr virus-transformed B cells process and present Mycobacterium tuberculosis particulate antigens to T-cell clones. Cell Immunol 1987, 107:281-292.
42. Krocova Z., Hartlova A., Souckova D., Zivna L., Kroca M., Rudolf E., et al. Interaction of B cells with intracellular pathogen Francisella tularensis. Microb Pathog 2008, 45:79-85.
43. Miao E.A., Brittnacher M., Haraga A., Jeng R.L., Welch M.D., Miller S.I. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol Microbiol 2003, 48:401-415.