Intracellular pathogenic bacteria and fungi - A case of convergent evolution?

Nature Reviews Microbiology

Volumn 7, Issue 2, 2009, Pages 165-171

  Bliska, James B ^a   Casadevall, Arturo ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONVERGENT EVOLUTION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FUNGAL VIRULENCE; HOST PATHOGEN INTERACTION; HUMAN; INTRACELLULAR KILLING; NONHUMAN; PATHOGENICITY; PHAGOCYTE; PHAGOSOME; PLAGUE; PREDATION; PRIORITY JOURNAL; PROTOZOON; YERSINIA PESTIS;

CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; EVOLUTION; HUMANS; MACROPHAGES; PLAGUE; RESPIRATORY TRACT INFECTIONS; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); FILOBASIDIELLA NEOFORMANS; FUNGI; YERSINIA PESTIS;

EID: 58549119536     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2049     Document Type: Article

References (82)

1. Harb, O. S., Gao, L. Y. & Abu Kwaik, Y. From protozoa to mammalian cells: A new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol. 2, 251-265 (2000).
2. Solomon, J. M. & Isberg, R. R. Growth of Legionella pneumophila in Dictyostelium discoideum: A novel system for genetic analysis of host-pathogen interactions. Trends Microbiol. 8, 478-480 (2000).
3. Swanson, M. S. & Hammer, B. K. Legionella pneumophila pathogenesis: A fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54, 567-613 (2000).
4. McLendon, M. K., Apicella, M. A. & Allen, L. A. Francisella tularensis: Taxonomy, genetics, and immunopathogenesis of a potential agent of biowarfare. Annu. Rev. Microbiol. 60, 167-185 (2006).
5. Santic, M., Molmeret, M., Klose, K. E. & Abu, K. Y. Francisella tularensis travels a novel, twisted road within macrophages. Trends Microbiol. 14, 37-44 (2006).
6. Sjostedt, A. Intracellular survival mechanisms of Francisella tularensis, a stealth pathogen. Microbes Infect. 8, 561-567 (2006).
7. Vogel, J. P. & Isberg, R. R. Cell biology of Legionella pneumophila. Curr. Opin. Microbiol. 2, 30-34 (1999).
8. Roy, C. R. & Tilney, L. G. The road less traveled: Transport of Legionella to the endoplasmic reticulum. J. Cell Biol. 158 415-419 (2002).
9. Prentice, M. B. & Rahalison, L. Plague. Lancet 369, 1196-1207 (2007).
10. Wren, B. W. The yersiniae - a model genus to study the rapid evolution of bacterial pathogens. Nature Rev. Microbiol. 1, 55-64 (2003).
11. Zhou, D., Han, Y. & Yang, R. Molecular and physiological insights into plague transmission, virulence and etiology. Microbes Infect. 8 273-284 (2006).
12. Pujol, C. & Bliska, J. B. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect. Immun. 71, 5892-5899 (2003).
13. Tauxe, R. V. Salad and pseudoappendicitis: Yersinia pseudotuberculosis as a foodborne pathogen. J. Infect. Dis. 189, 761-763 (2004).
14. Fukushima, H. Direct isolation of Yersinia pseudotuberculosis from fresh water in Japan. Appl. Environ. Microbiol. 58, 2688-2690 (1992).
15. Eisen, R. J. et al. Persistence of Yersinia pestis in soil under natural conditions. Emerg. Infect. Dis. 14, 941-943 (2008).
16. Drancourt, M., Houhamdi, L. & Raoult, D. Yersinia pestis as a telluric, human ectoparasite-borne organism. Lancet Infect. Dis. 6, 234-241 (2006).
17. Cavanaugh, D. C. & Randall, R. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of flea-borne plague. J. Immunol. 83, 348-363 (1959).
18. Bacon, G. A. & Burrows, T. W. The basis of virulence in Pasteurella pestis: An antigen determining virulence. Br. J. Exp. Pathol. 37, 481-493 (1956).
19. Pujol, C. & Bliska, J. B. Turning Yersinia pathogenesis outside in: Subversion of macrophage function by intracellular yersiniae. Clin. Immunol. 114, 216-226 (2005).
20. Lathem, W. W., Crosby, S. D., Miller, V. L. & Goldman, W. E. Progression of primary pneumonic plague: A mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl Acad. Sci. USA 102, 17786-17791 (2005).
21. Viboud, G. I. & Bliska, J. B. Yersinia outer proteins: Role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59, 69-89 (2005).
22. Marketon, M. M., DePaolo, R. W., DeBord, K. L., Jabri, B. & Schneewind, O. Plague bacteria target immune cells during infection. Science 309, 1739-1741 (2005).
23. Du, Y., Rosqvist, R. & Forsberg, A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70, 1453-1460 (2002).
24. Finegold, M. J. Pneumonic plague in monkeys. An electron microscopic study. Am. J. Pathol. 54, 167-185 (1969).
25. Meyer, K. F. Immunity in plague; a critical consideration of some recent studies. J. Immunol. 64, 139-163 (1950).
26. Bosio, C. M., Goodyear, A. W. & Dow, S. W. Early interaction of Yersinia pestis with APCs in the lung. J. Immunol. 175, 6750-6756 (2005).
27. Bubeck, S. S., Cantwell, A. M. & Dube, P. H. Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. Infect. Immun. 75, 697-705 (2007).
28. Groisman, E. A. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183, 1835-1842 (2001).
29. Ernst, R. K., Guina, T. & Miller, S. I. How intracellular bacteria survive: Surface modifications that promote resistance to host innate immune responses. J. Infect. Dis. 179 (Suppl. 2), 326-330 (1999).
30. Oyston, P. C. et al. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68, 3419-3425 (2000).
31. Grabenstein, J. P., Fukuto, H. S., Palmer, L. E. & Bliska, J. B. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74, 3727-3741 (2006).
32. Sebbane, F., Gardner, D., Long, D., Gowen, B. B. & Hinnebusch, B. J. Kinetics of disease progression and host response in a rat model of bubonic plague. Am. J. Pathol. 166, 1427-1439 (2005).
33. Sebbane, F., Jarrett, C. O., Gardner, D., Long, D. & Hinnebusch, B. J. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl Acad. Sci. USA 103, 5526-5530 (2006).
34. Jarrett, C. O. et al. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect. Dis. 190 783-792 (2004).
35. Hinnebusch, B. J. The evolution of flea-borne transmission in Yersinia pestis. Curr. Issues Mol. Biol. 7, 197-212 (2005).
36. Lukaszewski, R. A. et al. Pathogenesis of Yersinia pestis infection in BALB/c mice: Effects on host macrophages and neutrophils. Infect. Immun. 73, 7142-7150 (2005).
37. Diamond, R. D. & Bennett, J. E. Growth of Cryptococcus neoformans within human macrophages in vitro. Infect. Immun. 7, 231-236 (1973).
38. Casadevall, A. & Perfect, J. R. Cryptococcus neoformans (American Society for Microbiology, Washington DC, 1998).
39. Feldmesser, M., Tucker, S. C. & Casadevall, A. Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol. 9 273-278 (2001).
40. Rittershaus, P. C. et al. Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J. Clin. Invest. 116, 1651-1659 (2006).
41. Weeks, S., Hill, J., Friedlander, A. & Welkos, S. Anti-V antigen antibody protects macrophages from Yersinia pestis-induced cell death and promotes phagocytosis. Microb. Pathog. 32, 227-237 (2002).
42. Cowan, C., Philipovskiy, A. V., Wulff-Strobel, C. R., Ye, Z. & Straley, S. C. Anti-LcrV antibody inhibits delivery of Yops by Yersinia pestis KIM5 by directly promoting phagocytosis. Infect. Immun. 73 6127-6137 (2005).
43. Lahteenmaki, K., Kuusela, P. & Korhonen, T. K. Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552 (2001).
44. Cowan, C., Jones, H. A., Kaya, Y. H., Perry, R. D. & Straley, S. C. Invasion of epithelial cells by Yersinia pestis: Evidence for a Y. pestis-specific invasin. Infect. Immun. 68, 4523-4530 (2000).
45. Liu, F., Chen, H., Galvan, E. M., Lasaro, M. A. & Schifferli, D. M. Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect. Immun. 74, 5636-5644 (2006).
46. Chang, Y. C. et al. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infect. Immun. 72, 4985-4995 (2004).
47. Chen, S. H. et al. Cryptococcus neoformans induces alterations in the cytoskeleton of human brain microvascular endothelial cells. J. Med. Microbiol. 52, 961-970 (2003).
48. Shao, X. et al. An innate immune system cell is a major determinant of species-related susceptibility differences to fungal pneumonia. J. Immunol. 175, 3244-3251 (2005).
49. Feldmesser, M., Kress, Y., Novikoff, P. & Casadevall, A. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68, 4225-4237 (2000).
50. Zaragoza, O., Alvarez, M., Telzak, A., Rivera, J. & Casadevall, A. The relative susceptibility of mouse strains to pulmonary Cryptococcus neoformans infection is associated with pleiotropic differences in the immune response. Infect. Immun. 75, 2729-2739 (2007).
51. Straley, S. C. & Harmon, P. A. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect. Immun. 45, 655-659 (1984).
52. Tucker, S. C. & Casadevall, A. Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc. Natl Acad. Sci. USA 99, 3165-3170 (2002).
53. Levitz, S. M. et al. Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect. Immun. 67, 885-890 (1999).
54. +-ATPase activity. Microb. Pathog. 27 253-263 (1999).
55. Vieira, O. V., Botelho, R. J. & Grinstein, S. Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704 (2002).
56. Cox, G. M. et al. Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol. Microbiol. 39, 166-175 (2001).
57. Levitz, S. M., Harrison, T. S., Tabuni, A. & Liu, X. Chloroquine induces human nononuclear phagocytes to inhibit and kill Cryptococcus neoformans by a mechanism independent of iron deprivation. J. Clin. Invest. 100, 1640-1646 (1997).
58. Harrison, T. S., Griffin, G. E. & Levitz, S. M. Conditional lethality of the diprotic weak bases chloroquine and quinacrine against Cryptococcus neoformans. J. Infect. Dis. 182, 283-289 (2000).
59. Perry, R. D. & Fetherston, J. D. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10, 35-66 (1997).
60. Perry, R. D., Mier, I. Jr & Fetherston, J. D. Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. Biometals 20, 699-703 (2007).
61. Pujol, C., Grabenstein, J. P., Perry, R. D. & Bliska, J. B. Replication of Yersinia pestis in interferon γ-activated macrophages requires ripA, a gene encoded in the pigmentation locus. Proc. Natl Acad. Sci. USA 102, 12909-12914 (2005).
62. Goulding, C. W. et al. The structure and computational analysis of Mycobacterium tuberculosis protein CitE suggest a novel enzymatic function. J. Mol. Biol. 365, 275-283 (2007).
63. Brown, S. M., Campbell, L. T. & Lodge, J. K. Cryptococcus neoformans a fungus under stress. Curr. Opin. Microbiol. 10, 320-325 (2007).
64. Giles, S. S. et al. The Cryptococcus neoformans catalase gene family and its role in antioxidant defense. Eukaryot. Cell 5, 1447-1459 (2006).
65. de Jesus-Berrios, M. et al. Enzymes that counteract nitrosative stress promote fungal virulence. Curr. Biol. 13, 1963-1968 (2003).
66. Missall, T. A. & Lodge, J. K. Function of the thioredoxin proteins in Cryptococcus neoformans during stress or virulence and regulation by putative transcriptional modulators. Mol. Microbiol. 57, 847-858 (2005).
67. Narasipura, S. D., Chaturvedi, V. & Chaturvedi, S. Characterization of Cryptococcus neoformans variety gattii SOD2 reveals distinct roles of the two superoxide dismutases in fungal biology and virulence. Mol. Microbiol. 55, 1782-1800 (2005).
68. Giles, S. S., Batinic-Haberle, I., Perfect, J. R. & Cox, G. M. Cryptococcus neoformans mitochondrial superoxide dismutase: An essential link between antioxidant function and high-temperature growth. Eukaryot. Cell 4, 46-54 (2005).
69. Cox, G. M. et al. Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect. Immun. 71, 173-180 (2003).
70. Chatuverdi, V., Wong, B. & Newman, S. L. Oxidative killing of Cryptococcus neoformans by human leukocytes. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J. Immunol. 156, 3836-3840 (1996).
71. Shea, J. M., Kechichian, T. B., Luberto, C. & Del Poeta, M. The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect. Immun. 74 5977-5988 (2006).
72. Rodrigues, M. L. et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot. Cell 6, 48-59 (2007).
73. Rodrigues, M. L. et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 7, 58-67 (2008).
74. Beatty, W. L. et al. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1, 235-247 (2000).
75. Ma, H., Croudace, J. E., Lammas, D. A. & May, R. C. Direct cell-to-cell spread of a pathogenic yeast. BMC Immunol. 8, 15 (2007).
76. Alvarez, M. & Casadevall, A. Cell-to-cell spread and massive vacuole formation after Cryptococcus neoformans infection of murine macrophages. BMC Immunol. 8, 16 (2007).
77. Greub, G. & Raoult, D. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17, 413-433 (2004).
78. Steenbergen, J. N., Nosanchuk, J. D., Malliaris, S. D. & Casadevall, A. Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect. Immun. 72, 3478-3488 (2004).
79. Alvarez, M. & Casadevall, A. Phagosome fusion and extrusion, and host cell survival following Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16, 2161-2165 (2006).
80. Newman, S. L. Macrophages in host defense against Histoplasma capsulatum. Trends Microbiol. 7, 67-71 (1999).
81. Woods, J. P. Knocking on the right door and making a comfortable home: Histoplasma capsulatum intracellular pathogenesis. Curr. Opin. Microbiol. 6, 327-331 (2003).
82. Marion, C. L., Rappleye, C. A., Engle, J. T. & Goldman, W. E. An α-(1,4)-amylase is essential for α-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol. Microbiol. 62, 970-983 (2006).