Shigella flexneri IpaH7.8 facilitates escape of virulent bacteria from the endocytic vacuoles of mouse and human macrophages

Infection and Immunity

Volumn 68, Issue 6, 2000, Pages 3608-3619

  Fernandez Prada, Carmen M ^a   Hoover, David L ^a   Tall, Ben D ^b   Hartman, Antoinette B ^a   Kopelowitz, June ^a   Venkatesan, Malabi M ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL VACUOLE; DELETION MUTANT; ENDOCYTOSIS; FACILITATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; SHIGELLA FLEXNERI; STRAIN DIFFERENCE; TISSUE CULTURE;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL DEATH; CHLOROQUINE; DNA FRAGMENTATION; ENDOCYTOSIS; EYE; GENTAMICINS; GUINEA PIGS; HUMANS; INTERLEUKIN-1; MACROPHAGES; MICE; MONOCYTES; SHIGELLA FLEXNERI; TUMOR NECROSIS FACTOR-ALPHA; VACUOLES;

EID: 0034110502     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.6.3608-3619.2000     Document Type: Article

References (46)

1. Bahrani, F. K., P. J. Sansonetti, and C. Parsot. 1997. Secretion of Ipa proteins by Shigella flexneri: inducer molecules and kinetics of activation. Infect. Immun. 65:4005-4010.
2. Boland, A., S. Havaux, and G. R. Cornelis. 1998. Heterogeneity of the Yersinia YopM protein. Microb. Pathog. 25:343-348.
3. Buchanan, S. G., and N. J. Gay. 1996. Structural and functional diversity in the leucine-rich repeat family of proteins. Prog. Biophys. Mol. Biol. 65:1-25.
4. Buysse, J. M., C. K. Stover, E. V. Oaks, M. M. Venkatesan, and D. J. Kopecko. 1987. Molecular cloning of invasion plasmid antigen (ipa) genes from Shigella flexneri: analysis of ipa gene products and genetic mapping. J. Bacteriol. 169:2561-2569.
5. Buysse, J. M., A. B. Hartman, N. Strockbine, and M. M. Venkatesan. 1995. Genetic polymorphism of the ipaH multicopy antigen gene in Shigella spps. and enteroinvasive Escherichia coli. Microb. Pathog. 19:335-349.
6. Cornelis, G. R., A. Boland, A. P. Boyd, C. Geuijen, M. Iriarte, C. Neyt, M. P. Sory, and I. Stainier. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62:1315-1352.
7. Fernandez-Prada, C. M. 1997. Characterization of the cytotoxic interaction between human monocyte-derived macrophages and Shigella flexneri strains. Ph.D. thesis. George Washington University, Washington, D.C.
8. Fernandez-Prada, C. M., D. L. Hoover, B. Tall, and M. M. Venkatesan. 1997. Human monocyte-derived macrophages infected with virulent Shigella flexneri in vitro undergo a rapid cytolytic event similar to oncosis but not apoptosis. Infect. Immun. 65:1486-1496.
9. Fernandez-Prada, C. M., D. L. Hoover, B. Tall, S. Elliott, J. Nataro, and M. M. Venkatesan. 1998. Hemolysin-positive enteroaggregative and cell-detaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and apoptosis of murine J774 cells. Infect. Immun. 66:3918-3924.
10. Freiberg, C., R. Fellay, A. Bairoch, W. J. Broughton, A. Rosenthal, and X. Perret. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394-401.
11. Hale, T. L. 1998. Bacillary dysentery, p. 479-493. In W. J. Hausler, Jr., and M. Sussman (ed.), Topley & Wilson's microbiology and microbial infection, vol. 3. Bacterial infections. Oxford University Press, London, England.
12. Hartman, A. B., M. M. Venkatesan, E. V. Oaks, and J. M. Buysse. 1990. Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Shigella flexneri. J. Bacteriol. 172:1905-1915.
13. Hartman, A. B., C. J. Powell, C. L. Schultz, E. V. Oaks, and K. H. Eckels. 1991. Small-animal model to measure efficacy and immunogenicity of Shigella vaccine strains. Infect. Immun. 59:4075-4083.
14. Heffron, S., G. R. Moe, V. Sieber, J. Mengaud, P. Cossart, J. Vitali, and F. Jurnak. 1998. Sequence profile of the parallel beta helix in the pectate lyase superfamily. J. Struct. Biol. 122:223-235.
15. Higley, S., and M. Way. 1997. Actin and cell pathogenesis. Curr. Opin. Cell Biol. 9:62-69. (Review.)
16. Hilbi, H., Y. Chen, K. Thirumalai, and A. Zychlinsky. 1997. The interleukin 1β-converting enzyme, caspase 1, is activated during Shigella flexneri-induced apoptosis in human monocyte-derived macrophages. Infect. Immun. 65:5165-5170.
17. Hocking, A. M., T. Shinomura, and D. J. McQuillan. 1998. Leucine-rich repeat glycoproteins of the extracellular matrix. Matrix Biol. 17:1-19.
18. Islam, D., B. Veress, P. K. Bardhan, A. A. Lindberg, and B. Christensson. 1997. In situ characterization of inflammatory responses in the rectal mucosae of patients with shigellosis. Infect. Immun. 65:739-749.
19. Jung, H. C., L. Eckmann, S. K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Investig. 95:55-65.
20. Kajava, A. V. 1998. Structural diversity of leucine-rich repeat proteins. Mol. Biol. 277:519-527.
21. Kiener, P., P. M. Davis, G. C. Starling, C. Mehlin, S. J. Klebanoff, J. A. Ledbetter, and W. C. Liles. 1997. Differential induction of apoptosis by Fas-Fas ligand interactions in human monocytes and macrophages. J. Exp. Med. 185:1511-1516.
22. Kim, J. M., L. Eckman, T. C. Savidge, D. C. Lowe, T. Witthoft, and M. F. Kagnoff. 1998. Apoptosis of human intestinal epithelial cells after bacterial invasion. J. Clin. Investig. 102:1815-1823.
23. Lecuit, M., H. Ohayon, L. Braun, J. Mengaud, and P. Cossart. 1997. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect. Immun. 12:5309-5319.
24. Lindgren, S. W., and F. Heffron. 1997. To sting or be stung: bacteria-induced apoptosis. Trends Microbiol. 5:263-264.
25. Makino, S., C. Sasakawa, K. Kamata, T. Kurata, and M. Yoshikawa. 1986. A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in Shigella flexneri 2a. Cell 46:551-555.
26. Mandic-Mulec, I., J. Weiss, and A. Zychlinsky. 1997. Shigella flexneri is trapped in polymorphonuclear leukocyte vacuoles and efficiently killed. Infect. Immun. 65:110-115.
27. Mangan, D. F., and S. M. Wahl. 1991. Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines. J. Immunol. 147:3408-3412.
28. Mangan, D. F., S. E. Mergenhagen, and S. M. Wahl. 1993. Apoptosis in human monocytes: possible role in chronic inflammatory diseases. J. Periodontol. 64:461-466.
29. Menard, R., M. C. Prevost, P. Gounon, P. Sansonetti, and C. Dehio. 1996. The secreted 1pa complex of Shigella flexneri promotes entry into mammalian cells. Proc. Natl. Acad. Sci. USA 93:1254-1258.
30. Nonaka, T., A. Kuwae, C. Sasakawa, and S. Imajoh-Ohmi. 1999. Shigella flexneri YSH6000 induces two types of cell death, apoptosis and oncosis, in the differentiated human monoblastic cell line U937. FEMS Microbiol. Lett. 174:89-95.
31. Perdomo, O. J., J. M. Cavaillon, M. Huerre, H. Ohayon, P. Gounon, and P. J. Sansonetti. 1994. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J. Exp. Med. 180:1307-1319.
32. Perera, L. P., and T. A. Waldmann. 1998. Activation of human monocytes induces differential resistance to apoptosis with rapid down regulation of caspase-8/FLICE. Proc. Natl. Acad. Sci. USA 95:14308-14313.
33. Raqib, R., A. Ljungdahl, A. A. Lindberg, B. Wretlind, U. Anderson, and J. Anderson. 1996. Dissociation between cytokine mRNA expression and protein production in shigellosis. Eur. J. Immunol. 26:1130-1138.
34. Roshak, A. K., K. M. Anderson, S. D. Holmes, Z. Jonak, B. Bolognese, J. Terrett, and L. A. Marshall. 1999. Anti-human RP105 sera induces lymphocyte proliferation. J. Leukoc. Biol. 65:43-49.
35. Sansonetti, P. J., J. Arondel, J. M. Cavaillon, and M. Huerre. 1995. Role of interleukin-1 in the pathogenesis of experimental shigellosis. J. Clin. Investig. 96:884-892.
36. Sasakawa, C., K. Komatsu, T. Tobe, T. Suzuki, and M. Yoshikawa. 1993. Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a. J. Bacteriol. 175:2334-2346.
37. Schwan, W. R., and D. J. Kopecko. 1997. Uptake of pathogenic intracellular bacteria into human and murine macrophages downregulates the eukaryotic 26S protease complex ATPase gene. Infect. Immun. 65:4754-4760.
38. Sharma, A., H. T. Sojar, I. Glurich, K. Honma, H. K. Kuramitsu, and R. Genco. 1998. Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. Infect. Immun. 66:5703-5710.
39. Um, H. D., J. M. Orenstein, and S. M. Wahl. 1996. Fas mediates apoptosis in human monocytes by a reactive oxygen intermediate dependent pathway. Immunology 156:3469-3477.
40. Venkatesan, M. M., J. M. Buysse, and A. B. Hartman. 1991. Sequence variation in two ipaH genes of Shigella flexneri 5 and homology to the LRG-like family of proteins. Mol. Microbiol. 5:2435-2445.
41. Venkatesan, M. M., J. M. Buysse, and D. J. Kopecko. 1988. Characterization of invasion plasmid antigen genes (ipaBCD) from Shigella flexneri. Proc. Natl. Acad. Sci. USA 85:9317-9321.
42. Venkatesan, M. M., J. M. Buysse, and E. V. Oaks. 1992. Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of spa locus. J. Bacteriol. 174:1990-2001.
43. Watarai, M., S. Funato, and C. Sasakawa. 1996. Interaction of Ipa proteins of Shigella flexneri with α 5β1 integrin promotes entry of the bacteria into mammalian cells. J. Exp. Med. 183:991-999.
44. Zhang, C., Y. Xu, J. Gu, and S. F. Schlossman. 1998. A cell surface receptor defined by a mAb mediates a unique type of cell death similar to oncosis. Proc. Natl. Acad. Sci. USA 95:6290-6295.
45. Zychlinsky, A., B. Kenny, R. Menard, M. C. Prevost, I. B. Holland, and P. J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11:619-627.
46. Zychlinsky, A., K. Thirumalai, J. Arondel, J. R. Cantey, A. O. Aliprantis, and P. J. Sansonetti. 1996. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64:5357-5365.