Salmonella-induced macrophage death: Multiple mechanisms, different outcomes

Cellular Microbiology

Volumn 6, Issue 11, 2004, Pages 1019-1025

  Hueffer, Karsten ^a   Galán, Jorge E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN CDC42; RAC1 PROTEIN; RAF PROTEIN; TOLL LIKE RECEPTOR;

APOPTOSIS; BACTERIAL VIRULENCE; CELL INTERACTION; CELL SURVIVAL; CELL TYPE; CELLULAR IMMUNITY; HOST PATHOGEN INTERACTION; HOST RESISTANCE; INFECTION RESISTANCE; MACROPHAGE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA ENTERICA; SALMONELLOSIS; SHORT SURVEY;

ANIMALS; APOPTOSIS; CELL LINE; HUMANS; MACROPHAGES; MICE; SALMONELLA ENTERICA;

SALMONELLA; SALMONELLA ENTERICA;

EID: 6344277362     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2004.00451.x     Document Type: Short Survey

References (62)

1. Boise, L., and Collins, C. (2001) Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol 9: 64-67.
2. Brennan, M., and Cookson, B. (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
3. Browne, S.H., Lesnick, M.L., and Guiney, D.G. (2002) Genetic requirements for salmonella-induced cytopathology in human monocyte-derived macrophages. Infect Immun 70: 7126-7135.
4. Bursch, W., Ellinger, A., Gerner, C., Frohwein, U., and Schulte-Hermann, R. (2000) Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 926: 1-12.
5. Chen, L.M., Kaniga, K., and Galán, J.E. (1996a) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
6. Chen, Y., Smith, M.R., Thirumalai, K., and Zychlinsky, A. (1996b) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
7. Cohen, I., Castedo, M., and Kroemer, G. (2002) Tantalizing Thanatos: unexpected links in death pathways. Trends Cell Biol 12: 293-295.
8. Collazo, C., and Galán, J.E. (1997) The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol 24: 747-756.
9. Cookson, B.T., and Brennan, M.A. (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9: 113-114.
10. De Geyter, C., Wattiez, R., Sansonetti, P., Falmagne, P., Ruysschaert, J.M., Parsot, C., and Cabiaux, V. (2000) Characterization of the interaction of IpaB and IpaD, proteins required for entry of Shigella flexneri into epithelial cells, with a lipid membrane. Eur J Biochem 267: 5769-5776.
11. Forsberg, M., Blomgran, R., Lerm, M., Sarndahl, E., Sebti, S.M., Hamilton, A. et al. (2003) Differential effects of invasion by and phagocytosis of Salmonella typhimurium on apoptosis in human macrophages: potential role of Rho-GTPases and Akt. J Leukoc Biol 74: 620-629.
12. Galán, J.E. (1999) Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr Op Microbiol 2: 46-50.
13. Galán, J.E. (2001) Salmonella interaction with host cells: type III Secretion at Work. Annu Rev Cell Dev Biol 17: 53-86.
14. Galán, J.E. (2002) The cell biology of microbial infections: coming of age. J Cell Biol 158: 387-388.
15. Galán, J.E., and Zhou, D. (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci USA 97: 8754-8761.
16. Gotoh, H., Okada, N., Kim, Y.G., Shiraishi, K., Hirami, N., Haneda, T. et al. (2003) Extracellular secretion of the virulence plasmid-encoded ADP-ribosyltransferase SpvB in Salmonella. Microb Pathog 34: 227-238.
17. Gozuacik, D., and Kimchi, A. (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23: 2891-2906.
18. Guilloteau, L.A., Wallis, T.S., Gautier, A.V., MacIntyre, S., Platt, D.J., and Lax, A.J. (1996) The Salmonella virulence plasmid enhances Salmonella-induced lysis of macrophages and influences inflammatory responses. Infect Immun 64: 3385-3393.
19. Hales, K., and Fuller, M. (1997) Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90: 121-129.
20. Hayward, R., McGhie, E., and Koronakis, V. (2000) Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion. Mol Microbiol 37: 727-739.
21. Hensel, M. (2000) Salmonella pathogenicity island 2. Mol Microbiol 36: 1015-1023.
22. Hernandez, L.D., Pypaert, M., Flavell, R.A., and Galan, J.E. (2003) A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 163: 1123-1131.
23. Hersh, D., Monack, D., Smith, M., Ghori, N., Falkow, S., and Zychlinsky, A. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96: 2396-23401.
24. Hsu, L.C., Park, J.M., Zhang, K., Luo, J.L., Maeda, S., Kaufman, R.J. et al. (2004) The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428: 341-345.
25. Hume, P.J., McGhie, E.J., Hayward, R.D., and Koronakis, V. (2003) The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol Microbiol 49: 425-439.
26. Inohara, N., and Nunez, G. (2003) NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 3: 371-382.
27. Jarvelainen, H.A., Galmiche, A., and Zychlinsky, A. (2003) Caspase-1 activation by Salmonella. Trends Cell Biol 13 204-209.
28. Jesenberger, V., Procyk, K.J., Yuan, J., Reipert, S., and Baccarini, M. (2000) Salmonella-induced caspase-2 activation in macrophages: a novel mechanism in pathogen-mediated apoptosis. J Exp Med 192: 1035-1046.
29. Jesenberger, V., Procyk, K.J., Ruth, J., Schreiber, M., Theussl, H.C., Wagner, E.F., and Baccarini, M. (2001) Protective role of Raf-1 in Salmonella-induced macrophage apoptosis. J Exp Med 193: 353-364.
30. Knodler, L.A., and Finlay, B.B. (2001) Salmonella and apoptosis: to live or let die? Microbes Infect 3: 1321-1326.
31. Kobayashi, K., Inohara, N., Hernandez, L.D., Galán, J.E., Nunez, G., Janeway, C.A. et al. (2002) RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416: 194-199.
32. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S., and Flavell, R.A. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267: 2000-2003.
33. Kurita, A., Gotoh, H., Eguchi, M., Okada, N., Matsuura, S., Matsui, H. et al. (2003) Intracellular expression of the Salmonella plasmid virulence protein, SpvB, causes apoptotic cell death in eukaryotic cells. Microb Pathog 35: 43-48.
34. Lemasters, J. (1999) V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol 276: G1-G6.
35. Lesnick, M.L., Reiner, N.E., Fierer, J., and Guiney, D.G. (2001) The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol Microbiol 39: 1464-1470.
36. Libby, S.J., Adams, L.G., Ficht, T.A., Allen, C., Whitford, H.A., Buchmeier, N.A. et al. (1997) The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host. Infect Immun 65: 1786-1792.
37. Lindgren, S.W., Stojiljkovic, I., and Heffron, F. (1996) Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA 93: 4197-4201.
38. Lindgren, S.W., and Heffron, F. (1997) To sting or be stung: bacteria-induced apoptosis. Trends Microbiol 5: 263-264.
39. Lockshin, R.A., and Zakeri, Z. (2002) Caspase-independent cell deaths. Curr Opin Cell Biol 14: 727-733.
40. Lundberg, U., Vinatzer, U., Berdnik, D., von Gabain, A., and Baccarini, M. (1999) Growth phase-regulated induction of Salmonella induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J Bacteriol 181: 3433-3437.
41. McGhie, E., Hume, P., Hayward, R., Torres, J., and K. (2002) Topology of the Salmonella invasion protein SipB in a model bilayer. Mol Microbiol 44: 1309-1312.
42. Monack, D.M., Raupach, B., Hromockyj, A.E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
43. Monack, D.M., Hersh, D., Ghori, N., Bouley, D., Zychlinsky, A., and Falkow, S. (2000) Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 192: 249-258.
44. Monack, D.M., Detweiler, C.S., and Falkow, S. (2001a) Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol 3: 825-837.
45. Monack, D.M., Navarre, W.W., and Falkow, S. (2001b) Salmonella-induced macrophage death: the role of caspase-1 in death and inflammation. Microbes Infect 3: 1201-1212.
46. Navarre, W.W., and Zychlinsky, A. (2000) Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell Microbiol 2: 265-273.
47. Rojo, M., Legros, F., Chateau, D., and Lombes, A. (2002) Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J Cell Sci 115: 1663-1674.
48. Rosenberger, C.M., and Finlay, B.B. (2003) Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 4: 385-396.
49. Santos, R.L., Tsolis, R.M., Baumler, A.J., Smith, R., and 3rd and Adams, L.G. (2001) Salmonella enterica serovar typhimurium induces cell death in bovine monocyte-derived macrophages by early sipB-dependent and delayed sipB-independent mechanisms. Infect Immun 69: 2293-2301.
50. Schwartz, L., Smith, S., Jones, M., and Osborne, B. (1993) Do all programmed cell deaths occur via apoptosis? Proc Natl Acad Sci USA 90: 980-984.
51. Shea, J.E., Beuzon, C.R., Gleeson, C., Mundy, R., and Holden, D.W. (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infection Immunity 67: 213-219.
52. Skoudy, A., Mounier, J., Aruffo, A., Ohayon, H., Gounon, P., Sansonetti, P., and Tran Van Nhieu, G. (2000) CD44 binds to the Shigella IpaB protein and participates in bacterial invasion of epithelial cells. Cell Microbiol 2: 19-33.
53. Stehlik, C., Lee, S.H., Dorfleutner, A., Stassinopoulos, A., Sagara, J., and Reed, J.C. (2003) Apoptosis-associated speck-like protein containing a caspase recruitment domain is a regulator of procaspase-1 activation. J Immunol 171: 6154-6163.
54. van der Velden, A.W., Lindgren, S.W., Worley, M.J., and Heffron, F. (2000) Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium. Infect Immun 68: 5702-5709.
55. Watarai, M., Funato, S., and Sasakawa, C. (1996) Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med 183: 991-999.
56. Waterman, S.R., and Holden, D.W. (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
57. Watson, P., Gautier, A., Paulin, S., Bland, A., Jones, P., and Wallis, T. (2000) Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect Immun 68: 3744-3747.
58. Xue, L., Fletcher, G., and Tolkovsky, A. (1999) Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol Cell Neurosci 14: 180-198.
59. Yoo, N.J., Park, W.S., Kim, S.Y., Reed, J.C., Son, S.G., Lee, J.Y., and Lee, S.H. (2002a) Nod1, a CARD protein, enhances pro-interleukin-1beta processing through the interaction with pro-caspase-1. Biochem Biophys Res Commun 299: 652-658.
60. Yoo, N.J., Park, W.S., Kim, S.Y., Reed, J.C., Son, S.G., Lee, J.Y., and Lee, S.H. (2002b) Nod1, a CARD protein, enhances pro-interleukin-1beta processing through the interaction with pro-caspase-1. Biochem Biophys Res Commun 299: 652-658.
61. Yuan, J., Lipinski, M., and Degterev, A. (2003) Diversity in the mechanisms of neuronal cell death. Neuron 40: 401-413.
62. Zhang, W.H., Wang, X., Narayanan, M., Zhang, Y., Huo, C., Reed, J.C., and Friedlander, R.M. (2003) Fundamental role of the Rip2/caspase-1 pathway in hypoxia and ischemia-induced neuronal cell death. Proc Natl Acad Sci USA 100: 16012-16017.