Necrotic Death of Rhodococcus equi-Infected Macrophages Is Regulated by Virulence-Associated Plasmids

Infection and Immunity

Volumn 72, Issue 2, 2004, Pages 853-862

  Lührmann, Anja ^a,b   Mauder, Norman ^b   Sydor, Tobias ^a   Fernandez Mora, Eugenia ^a,b   Schulze Luehrmann, Jan ^a   Takai, Shinji ^c   Haas, Albert ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c KITASATO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; ANTIBIOTIC AGENT; DNA; ETOPOSIDE; FORMALDEHYDE; GRAMICIDIN S; PHOSPHOLIPID; TETRACYCLINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BRONCHOPNEUMONIA; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; ELECTRON MICROSCOPY; GENE EXPRESSION; GRAM POSITIVE BACTERIUM; HEAT; HORSE DISEASE; MACROPHAGE; MOUSE; NECROSIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RHODOCOCCUS; RHODOCOCCUS EQUI; ULTRAVIOLET IRRADIATION; VAPA GENE; VAPB GENE;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; CULTURE MEDIA; MACROPHAGES; MICE; NECROSIS; PLASMIDS; RHODOCOCCUS EQUI; VIRULENCE; VIRULENCE FACTORS;

EID: 0842283067     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.2.853-862.2004     Document Type: Article

References (62)

1. Balcewicz-Sablinska, M. K., J. Keane, H. Kornfeld, and H. G. Remold. 1998. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-alpha. J. Immunol. 161:2636-2641.
2. Bantel, H., B. Sinha, W. Domschke, G. Peters, K. Schulze-Osthoff, and R. U. Jänicke. 2001. α-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J. Cell Biol. 155:637-648.
3. Barros, L. F., T. Hermosilla, and J. Castron. 2001. Necrotic volume increase and the early physiology of necrosis. Comp. Biochem. Physiol. 130:401-409.
4. Barry, C. E., III, R. E. Lee, K. Mdluli, A. E. Sampson, B. G. Schroeder, R. A. Slayden, and Y. Yuan. 1998. Mycolic acids: structure, biosynthesis and physiological functions. Prog. Lipid Res. 37:143-179.
5. Benoit, S., S. Taouji, A. Benachour, and A. Hartke. 2000. Resistance of Rhodococcus equi to acid pH. Int. J. Food Microbiol. 55:295-298.
6. Boise, L. H., and C. M. Collins. 2001. Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol. 9:64-67.
7. Byrne, B. A., J. F. Prescott, G. H. Palmer, S. Takai, V. M. Nicholson, D. C. Alperin, and S. A. Hines. 2001. Virulence plasmid of Rhodococcus equi contains inducible gene family encoding secreted proteins. Infect. Immun. 69:650-656.
8. Cornish, N., and J. A. Washington. 1999. Rhodococcus equi infections: clinical features and laboratory diagnosis. Curr. Clin. Top. Infect. Dis. 19:198-215.
9. Darrah, P. A., M. K. Hondalus, Q. Chen, H. Ischiropoulos, and D. M. Mosser. 2000. Cooperation between reactive oxygen and nitrogen intermediates in killing of Rhodococcus equi by activated macrophages. Infect. Immun. 68:3587-3593.
10. De La Pena-Moctezuma, A., J. F. Prescott, and M. Goodfellow. 1996. Attempts to find phenotypic markers of the virulence plasmid of Rhodococcus equi. Can. J. Vet. Res. 60:29-33.
11. Detrick-Hooks, B., T. Borsos, and H. J. Rapp. 1975. Quantitative comparison of techniques used to measure complement-mediated cytotoxicity of nucleated cells. J. Immunol. 114:287-290.
12. Dobos, K. M., E. A. Spotts, F. D. Quinn, and C. H. King. 2000. Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by membrane permeabilization. Infect. Immun. 68:6300-6310.
13. Fiani, M. L., J. Beitz, D. Turvy, J. S. Blum, and P. D. Stahl. 1998. Regulation of mannose receptor synthesis and turnover in mouse J774 macrophages. J. Leukoc. Biol. 64:85-91.
14. Francois, M., V. Le Cabec, M. A. Dupont, P. J. Sansonetti, and I. Maridonneau-Parini. 2000. Induction of necrosis in human neutrophils by Shigella flexneri requires type III secretion, IpaB and IpaC invasion, and actin polymerization. Infect. Immun. 68:1289-1296.
15. Fuhrmann, C., I. Soedarmanto, and C. Lämmler. 1997. Studies on the rod-coccus life cycle of Rhodococcus equi. Zentralbl. Veterinärmed. B. 44: 287-294.
16. George, K. M., D. Chatterjee, G. Gunawardana, D. Welty, J. Hayman, R. Lee, and P. L. Small. 1999. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854-857.
17. Giguere, S., and J. F. Prescott. 1998. Cytokine induction in murine macrophages infected with virulent and avirulent Rhodococcus equi. Infect. Immun. 66:1848-1854.
18. Giguere, S., M. K. Hondalus, J. A. Yager, P. Darrah, D. M. Mosser, and J. F. Prescott. 1999. Role of the 85-kilobase plasmid and plasmid-encoded virulence-associated protein A in intracellular survival and virulence of Rhodococcus equi. Infect. Immun. 67:3548-3557.
19. Gotoh, K., M. Mitsuyama, S. Imaizumi, I. Kawamura, and I. Yano. 1991. Mycolic acid-containing glycolipids as a possible virulence factor for Rhodococcus equi in mice. Microbiol. Immunol. 35:175-185.
20. Hietala, S. K., and A. A. Ardans. 1987. Interaction of Rhodococcus equi with phagocytic cells from R. equi-exposed and non-exposed foals. Vet. Microbiol. 14:307-320.
21. Hilbi, H., J. E. Moss, D. Hersh, Y. Chen, J. Arondel, S. Banerjee, R. A. Flavell, J. Yuan, P. J. Sansonetti, and A. Zychlinsky. 1998. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 49:32895-32900.
22. Hilbi, H., R. J. Puro, and A. Zychlinsky. 2000. Tripeptidyl peptidase II promotes maturation of caspase-1 in Shigella flexneri-induced macrophage apoptosis. Infect. Immun. 68:5502-5508.
23. + T lymphocytes. Clin. Diagn. Lab. Immunol. 10:208-215.
24. Hondalus, M. K. 1997. Pathogenesis and virulence of Rhodococcus equi. Vet. Microbiol. 56:257-268.
25. Hondalus, M. K., and D. M. Mosser. 1994. Survival and replication of Rhodococcus equi in macrophages. Infect. Immun. 62:4167-4175.
26. Hotz, M. A., J. Gong, F. Traganos, and Z. Darzynkiewicz. 1994. Flow cytometric detection of apoptosis: comparison of the assays of in situ DNA degradation and chromatin changes. Cytometry 15:237-244.
27. Keane, J., M. K. Balcewicz-Sablinska, H. G. Remold, G. L. Chupp, B. B. Meek, M. J. Fenton, and H. Kornfeld. 1997. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect. Immun. 65:298-304.
28. Keane, J., H. G. Remold, and H. Kornfeld. 2000. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J. Immunol. 164:2016-2020.
29. Kedlaya, I., M. B. Ing, and S. S. Wong. 2001. Rhodococcus equi infections in immunocompetent hosts: case report and review. Clin. Infect. Dis. 32:E39-E46.
30. Konkel, M. E., and P. F. Mixter. 2000. Flow cytometric detection of host cell apoptosis induced by bacterial infection. Methods Cell Sci. 22:209-215.
31. Lee, D., S.A. Long, J. L. Adams, G. Chan, K. S. Vaidya, T. A. Francis, K. Kikly, J. D. Winkler, C. M. Sung, C. Debouck, S. Richardson, M. A. Levy, W. E. DeWolf, Jr., P. M. Keller, T. Tomaszek, M. S. Head, M. D. Ryan, R. C. Haltiwanger, P. H. Liang, C. A. Janson, P. J. McDevitt, K. Johanson, N. O. Concha, W. Chan, S. S. Abdel-Meguid, A. M. Badger, M. W. Lark, D. P. Nadeau, L. J. Suva, M. Gowen, and M. E. Nuttall. 2000. Potent and selective nonpeptide inhibitors of caspases 3 and 7 inhibit apoptosis and maintain cell functionality. J. Biol. Chem. 275:16007-16014.
32. Lührmann, A., K. Streker, A. Schüttfort, J. J. D. Daniels, and A. Haas. 2001. Afipia felis resides in a macrophage compartment that is disconnected from the endocytic pathway. Proc. Natl. Acad. Sci. USA 98:7271-7276.
33. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146:3-15.
34. Mosser, D. M., and M. K. Hondalus. 1996. Rhodococcus equi: an emerging opportunistic pathogen. Trends Microbiol. 4:29-33.
35. Navarre, W. W., and A. Zychlinsky. 2000. Pathogen-induced apoptosis of macrophages: a common end for different pathogenic strategies. Cell. Microbiol. 2:265-273.
36. Nicholson, V. M., and J. F. Prescott. 1997. Restriction enzyme analysis of the virulence plasmids of VapA-positive Rhodococcus equi strains isolated from humans and horses. J. Clin. Microbiol. 35:738-740.
37. Nordmann, P., N. Zinzendorf, M. Keller, I. Lair, E. Ronco, and M. Guenounou. 1994. Interaction of virulent and non-virulent Rhodococcus equi human isolates with phagocytes, fibroblast- and epithelial-derived cells. FEMS Immunol. Med. Microbiol. 9:199-205.
38. Prescott, J. F. 1991. Rhodococcus equi: an animal and human pathogen. Clin. Microbiol. Rev. 4:20-34.
39. Schaible, U. E., H. L. Collins, and S. H. E. Kaufmann. 1999. Confrontation between intracellular bacteria and the immune system. Adv. Immunol. 71: 267-377.
40. Shah, G. M., R. G. Shah, and G. C. Poirier. 1996. Different cleavage patterns for Poly(ADP-ribose)polymerase during necrosis and apoptosis in HL-60 cells. Biochem. Biophys. Res. Commun. 229:838-844.
41. Sutcliffe, I. C. 1997. Macroamphiphilic cell envelope components of Rhodococcus equi and closely related bacteria. Vet. Microbiol. 56:287-299.
42. Swannie, H. C., and S. B. Kaye. 2002. Protein kinase C inhibitors. Curr. Oncol. Rep. 4:37-46.
43. Syntichaki, P., and N. Tavernarakis. 2002. Death by necrosis. EMBO Rep. 3:604-609.
44. Takai, S., T. Sekizaki, T. Ozawa, T. Sugawara, Y. Watanabe, and S. Tsubaki. 1991. Association between a large plasmid and 15- to 17-kilodalton antigens in virulent Rhodococcus equi. Infect. Immun. 59:4056-4060.
45. Takai, S., M. Iie, Y. Watanabe, S. Tsubaki, and T. Sekizaki. 1992. Virulence-associated 15- to 17-kilodalton antigens in Rhodococcus equi: temperature-dependent expression and location of the antigens. Infect. Immun. 60:2995-2997.
46. Takai, S., T. Sugawara, Y. Watanabe, Y. Sasaki, S. Tsubaki, and T. Sekizaki. 1994. Effect of growth temperature on maintenance of virulent Rhodococcus equi. Vet. Microbiol. 39:187-192.
47. Takai, S., Y. Sasaki, T. Ikeda, Y. Uchida, S. Tsubaki, and T. Sekizaki. 1994. Virulence of Rhodococcus equi isolates from patients with and without AIDS. J. Clin. Microbiol. 32:457-460.
48. Takai, S., Y. Imai, N. Fukunaga, Y. Uchida, K. Kamisawa, Y. Sasak, S. Tsubaki, and T. Sekizaki. 1995. Identification of virulence-associated antigens and plasmids in Rhodococcus equi from patients with AIDS. J. Infect. Dis. 172:1306-1311.
49. Takai, S., H. Madarame, C. Matsumoto, M. Inoue, Y. Sasaki, Y. Hasegawa, S. Tsubaki, and A. Nakane. 1995. Pathogenesis of Rhodococcus equi infection in mice: roles of virulence plasmids and granulomagenic activity of bacteria. FEMS Immunol. Med. Microbiol. 11:181-190.
50. Takai, S., T. Ikeda, Y. Sasaki, Y. Watanabe, T. Ozawa, S. Tsubaki, and T. Sekizaki. 1995. Identification of virulent Rhodococcus equi by amplification of gene coding for 15-to-17-kilodalton antigens. J. Clin. Microbiol. 3:1624-1627.
51. Takai, S., N. Fukunaga, S. Ochiai, Y. Imai, Y. Sasaki, S. Tsubaki, and T. Sekizaki. 1996. Identification of intermediately virulent Rhodococcus equi isolates from pigs. J. Clin. Microbiol. 34:1034-1037.
52. Takai, S., N. Fukunaga, S. Ochiai, T. Sakai, Y. Sasaki, and S. Tsubaki. 1996. isolation of virulent and intermediately virulent Rhodococcus equi from soil and sand on parks and yards in Japan. J. Vet. Med. Sci. 58:669-672.
53. Takai, S., S. A. Hines, T. Sekizaki, V. M. Nicholson, D. A. Alperin, M. Osaki, D. Takamatsu, M. Nakamura, K. Suzuki, N. Ogino, T. Kakuda, H. Dan, and J. F. Prescott. 2000. DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect. Immun. 68:6840-6847.
54. Takai, S., T. Anzai, Y. Fujita, O. Akita, M. Shoda, S. Tsubaki, and R. Wada. 2000. Pathogenicity of Rhodococcus equi expressing a virulence-associated 20 kDa protein (VapB) in foals. Vet. Microbiol. 76:71-80.
55. Takasugi, J. E., and J. D. Godwin. 1991. Lung abscess caused by Rhodococcus equi. J. Thorac. Imaging 6:72-74.
56. Thornberry, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281:1312-1316.
57. Tkachuk-Saad, O., and J. F. Prescott. 1991. Rhodococcus equi plasmids: isolation and partial characterization. J. Clin. Microbiol. 29:2696-2700.
58. Verme, I., C. Haanen, and C. Reutlingsperger. 2000. Flow cytometry of apoptotic cell death. J. Immunol. Methods 243:167-190.
59. Votava, M., B. Skalk, H. Hrstkova, R. Tejkalova, and L. Dvorska. 1997. Review of 105 cases of isolation of Rhodococcus equi in humans. Cas. Lek. Cesk. 136:51-53.
60. Wada, R., M. Kamada, T. Anzai, A. Nakanishi, T. Kanemaru, S. Takai, and S. Tsubaki. 1997. Pathogenicity and virulence of Rhodococcus equi in foals following intratracheal challenge. Vet. Microbiol. 56:301-312.
61. Zhang, J., M. C. Reedy, Y. A. Hannun, and L. M. Obeid. 1999. Inhibition of caspases inhibits the release of apoptotic bodies: Bcl-2 inhibits the initiation of formation of apoptotic bodies in chemotherapeutic agent-induced apoptosis. J. Cell Biol. 145:99-108.
62. Zink, M. C., J. A. Yager, J. F. Prescott, and M. A. Fernando. 1987. Electron microscopic investigation of intracellular events after ingestion of Rhodococcus equi by foal alveolar macrophages. Vet. Microbiol. 14:295-305.