Amoebae as training grounds for intracellular bacterial pathogens

Applied and Environmental Microbiology

Volumn 71, Issue 1, 2005, Pages 20-28

  Molmeret, Maëlle ^a   Horn, Matthias ^b   Wagner, Michael ^b   Santic, Marina ^a,c   Kwaik, Yousef Abu ^a  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF RIJEKA   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM;

AMOEBA; BACTERIUM; CHLAMYDIA; ENDOCYTOSIS; ENDOSYMBIOSIS; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MICROBIAL DIVERSITY; NEOCHLAMYDIA; NONHUMAN; SHORT SURVEY;

AMOEBA; ANIMALS; BACTERIA; EUKARYOTIC CELLS; HUMANS; SYMBIOSIS;

BACTERIA (MICROORGANISMS); CHLAMYDIA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; NEOCHLAMYDIA;

EID: 12244295183     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.1.20-28.2005     Document Type: Short Survey

References (104)

1. Abd, H., T. Johansson, I. Golovliov, G. Sandström, and M. Forsman. 2003. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microbiol. 69:600-606.
2. Abu Kwaik, Y. 1998. Induced expression of the Legionella pneumophila gene encoding a 20-kilodalton protein during intracellular infection. Infect. Immun. 66:203-212.
3. Abu Kwaik, Y. 1996. The phagosome containing Legionella pneumophila within the protozoan Hartmanella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 62:2022-2028.
4. Abu Kwaik, Y., L.-Y. Gao, O. S. Harb, and B. J. Stone. 1997. Transcriptional regulation of the macrophage-induced gene (gspA) of Legionella pneumophila and phenotypic characterization of a null mutant. Mol. Microbiol. 24:629-642.
5. Abu Kwaik, Y., L.-Y. Gao, B. J. Stone, C. Venkataraman, and O. S. Harb. 1998. Invasion of protozoa by Legionella pneumophila and its role in bacterial ecology and pathogenesis. Appl. Environ. Microbiol. 64:3127-3133.
6. Adeleke, A., J. Pruckler, R. Benson, T. Rowbotham, M. Halablab, and B. S. Fields. 1996. Legionella-like amoeba1 pathogens-phylogenetic status and possible role in respiratory disease. Emerg. Infect. Dis. 2:225-229.
7. Alli, O. A., S. Zink, N. K. von Lackum, and Y. Abu-Kwaik. 2003. Comparative assessment of virulence traits in Legionella spp. Microbiology 149:631-641.
8. Amann, R., N. Springer, W. Ludwig, H.-D. Gortz, and K.-H. Schleifer. 1991. Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161-164.
9. Amann, R., N. Springer, W. Schonhuber, W. Ludwig, E. N. Schmid, K.-D. Muller, and R. Michel. 1997. Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl. Environ. Microbiol. 63: 115-121.
10. Barker, J., and M. R. Brown. 1994. Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140:1253-1259.
11. Barker, J., M. R. W. Brown, P. J. Collier, I. Farrell, and P. Gilbert. 1992. Relationships between Legionella pneumophila and Acanthamoeba polyphaga: physiological status and susceptibility to chemical inactivation. Appl. Environ. Microbiol. 58:2420-2425.
12. Barker, J., P. A. Lambert, and M. R. W. Brown. 1993. Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect. Immun. 61:3503-3510.
13. Barker, J., H. Scaife, and M. R. W. Brown. 1995. Intraphagocytic growth induces an antibiotic-resistant phenotype of Legionella pneumophila. Antimicrob. Agents Chemother. 39:2684-2688.
14. Beier, C. L., M. Horn, R. Michel, M. Schweikert, H.-D. Görtz, and M. Wagner. 2002. The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl. Environ. Microbiol. 68:6043-6050.
15. Berk, S. G., R. S. Ting, G. W. Turner, and R. J. Ashburn. 1998. Production of respirable vesicles containing live Legionella pneumophila cells by two Acanthamoeba spp. Appl. Environ. Microbiol. 64:279-286.
16. Birtles, R. J., T. J. Rowbotham, R. Michel, D. G. Pitcher, B. Lascola, S. Alexiou-Daniel, and D. Raoult. 2000. 'Candidatus Odyssella thessalonicensis' gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int. J. Syst. Evol. Microbiol. 50:63-72.
17. Birtles, R. J., T. J. Rowbotham, D. Raoult, and T. G. Harrison. 1996. Phylogenetic diversity of intra-amoebal legionellae as revealed by 16S rRNA gene sequence comparison. Microbiology 142:3525-3530.
18. Birtles, R. J., T. J. Rowbotbam, C. Storey, T. J. Marrie, and D. Raoult. 1997. Chlamydia-like obligate parasite of free-living amoebae. Lancet 349: 925-926.
19. Bitar, D. M., M. Molmeret, and Y. Abu Kwaik. 2004. Molecular and cell biology of Legionella pneumophila. Int. J. Med. Microbiol. 293:519-527.
20. Biurrun, A., L. Caballero, C. Pelaz, E. Leon, and A. Gago. 1999. Treatment of a Legionella pneumophila-colonized water distribution system using copper-silver ionization and continuous chlorination. Infect. Control Hosp. Epidemiol. 20:426-428.
21. Bozue, J. A., and W. Johnson. 1996. Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect. Immun. 64:668-673.
22. Brieland, J. K., J. C. Fantone, D. G. Remick, M. LeGendre, M. McClain, and N. C. Engleberg. 1997. The role of Legionella pneumophila-infected Hartmanella vermiformis as an infectious particle in a murine model of Legionnaires' disease. Infect. Immun. 65:4892-4896.
23. Campbell, L. A., and C. C. Kuo. 2003. Chlamydia pneumoniae and atherosclerosis. Semin. Respir. Infect. 18:48-54.
24. Christie, P. J., and J. P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
25. Cianciotto, N. P., and B. S. Fields. 1992. Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl. Acad. Sci. USA 89:5188-5191.
26. Cirillo, J. D., S. L. Cirillo, L. Van, L. E. Bermudez, S. Falkow, and L. S. Tompkins. 1999. Intracellular growth in Acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of Legionella pneumophila. Infect. Immun. 67:4427-4434.
27. Cirillo, J. D., L. S. Tompkins, and S. Falkow. 1994. Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion. Infect. Immun. 62:3254-3261.
28. Corsaro, D., D. Venditti, A. Le Faou, P. Guglielmetti, and M. Valassina. 2001. A new chlamydia-like 16S rDNA sequence from a clinical sample. Microbiology 147:515-516.
29. Corsaro, D., D. Venditti, and M. Valassina. 2002. New parachlamydial 16S rDNA phylotypes detected in human clinical samples. Res. Microbiol. 153: 563-567.
30. Darelid, J., S. Löfgren, and B.-E. Malmvall. 2002. Control of nosocomial Legionnaires' disease by keeping the circulating hot water temperature above 55°C: experience from a 10-year surveillance programme in a district general hospital. J. Hosp. Infect. 50:213-219.
31. De Bary, A. 1879. Die Erscheinung der Symbiose. Verlag Von Karl J. Trubner, Strassburg, Austria.
32. Essig, A., M. Heinemann, U. Simnacher, and R. Marre. 1997. Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl. Environ. Microbiol. 63:1396-1399.
33. Everett, K. D., R. M. Bush, and A. A. Andersen. 1999. Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int. J. Syst. Bacteriol. 49:415-440.
34. Fields, B. S. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-290.
35. Fields, B. S., R. F. Benson, and R. E. Besser. 2002. Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15:506-526.
36. Fields, B. S., T. A. Nerad, T. K. Sawyer, C. H. King, J. M. Barbaree, W. T. Martin, W. E. Morrill, and G. N. Sanden. 1990. Characterization of an axenic strain of Hartmannella vermiformis obtained from an investigation of nosocomial legionellosis. J. Protozool. 37:581-583.
37. Fliermans, C. B. 1996. Ecology of Legionella: from data to knowledge with a little wisdom. Microb. Ecol. 32:203-228.
38. Fritsche, T. R., R. K. Gautom, S. Seyedirashti, D. L. Bergeron, and T. D. Lindquist. 1993. Occurrence of bacterial endosymbionts in Acanthamoeba spp. isolated from corneal and environmental specimens and contact lenses. J. Clin. Microbiol. 31:1122-1126.
39. Fritsche, T. R., M. Horn, S. Seyedirashti, R. K. Gautom, K.-H. Schleifer, and M. Wagner. 1999. In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl. Environ. Microbiol. 65:206-212.
40. Fritsche, T. R., M. Horn, M. Wagner, R. P. Herwig, K.-H. Schleifer, and R. K. Gautom. 2000. Phylogenetic diversity among geographically dispersed Chlamydiales endosymbionts recovered from clinical and environmental isolates of Acanthamoeba spp. Appl. Environ. Microbiol. 66:2613-2619.
41. Gao, L.-Y., O. S. Harb, and Y. Abu Kwaik. 1998. Identification of macrophage-specific infectivity loci (mil) of Legionella pneumophila that are not required for infectivity of protozoa. Infect. Immun. 66:883-892.
42. Gao, L.-Y., O. S. Harb, and Y. Abu Kwaik. 1997. Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant hosts, mammalian and protozoan cells. Infect. Immun. 65:4738-4746.
43. Gao, L.-Y., M. Susa, B. Ticac, and Y. Abu Kwaik. 1999. Heterogeneity in intracellular replication and cytopathogenicity of Legionella pneumophila and Legionella micdadei in mammalian and protozoan cells. Microb. Pathog. 27:273-287.
44. Greub, G., J.-L. Mege, and D. Raoult. 2003. Parachlamydia acanthamoebae enters and multiplies within human macrophages and induces their apoptosis. Infect. Immun. 71:5979-5985.
45. Greub, G., and D. Raoult. 2003. History of the ADP/ATP-translocase- encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl. Environ. Microbiol. 69:5530-5535.
46. Hagele, S., R. Kohler, H. Merkert, M. Schleicher, J. Hacker, and M. Steinert. 2000. Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell. Microbiol. 2:165-171.
47. Harb, O. S., L.-Y. Gao, and Y. Abu Kwaik. 2000. From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol. 2:251-265.
48. Harb, O. S., C. Venkataraman, B. J. Haack, L.-Y. Gao, and Y. Abu Kwaik. 1998. Heterogeneity in the attachment and uptake mechanisms of the Legionnaires' disease bacterium, Legionella pneumophila, by protozoan hosts. Appl. Environ. Microbiol. 64:126-132.
49. Hatch, T. P. 1999. Developmental biology, p. 29-67. In R. S. Stephens (ed.), Chlamydia. American Society for Microbiology, Washington, D.C.
50. Henning, K., G. Schares, H. Granzow, U. Polster, M. Hartmann, H. Hotzel, K. Sachse, M. Peters, and M. Rauser. 2002. Neospora caninum and Waddlia chondrophila strain 2032/99 in a septic stillborn calf. Vet. Microbiol. 85: 285-292.
51. Hilbi, H., G. Segal, and H. A. Shuman. 2001. Icm/Dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42:603-617.
52. Hoebe, C. J., and J. L. Kool. 2000. Control of legionella in drinking-water systems. Lancet 355:2093-2094.
53. Horn, M., A. Collingro, S. Schmitz-Esser, C. L. Beier, U. Purkhold, B. Fartmann, P. Brandt, G. J. Nyakatura, M. Droege, D. Frishman, T. Rattei, H. W. Mewes, and M. Wagner. 2004. Illuminating the evolutionary history of chlamydiae. Science 304:728-730.
54. Horn, M., T. R. Fritsche, R. K. Gautom, K. H. Schleifer, and M. Wagner. 1999. Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ. Microbiol. 1:357-367.
55. Horn, M., T. R. Fritsche, T. Linner, R. K. Gautom, M. D. Harzenetter, and M. Wagner. 2002. Obligate bacterial endosymbionts of Acanthamoeba spp. related to the beta-Proteobacteria: proposal of 'Candidatus Procabacter acanthamoebae' gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 52:599-605.
56. Horn, M., M. D. Harzenetter, T. Linner, E. N. Schmid, K.-D. Müller, R. Michel, and M. Wagner. 2001. Members of the Cytophaga-Flavobacterium- Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of 'Candidatus Amoebophilus asiaticus.' Environ. Microbiol. 3:440-449.
57. Horn, M., and M. Wagner. 2001. Evidence for additional genus-level diversity of Chlamydiales in the environment. FEMS Microbiol. Lett. 204:71-74.
58. Horn, M., M. Wagner, K.-D. Müller, E. N. Schmid, T. R. Pritsche, K.-H. Schleifer, and R. Michel. 2000. Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology 146:1231-1239.
59. Horwitz, M. A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158:1319-1331.
60. Horwitz, M. A. 1984. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulftnent within a pseudopod coil. Cell 36:27-33.
61. Horwitz, M. A., and S. C. Silverstein. 1981. Interaction of the Legionnaires' disease bacterium (Legionella pneumophila) with human phagocytes. II. Antibody promotes binding of L. pneumophila to monocytes but does not inhibit intracellular multiplication. J. Exp. Med. 153:398-406.
62. Iliffe-Lee, E. R., and G. McClarty. 1999. Glucose metabolism in Chlamydia trachomatis: the 'energy parasite' hypothesis revisited. Mol. Microbiol. 33: 177-187.
63. Kahane, S., D. Greenberg, M. G. Friedman, H. Haikin, and R. Dagan. 1998. High prevalence of "Simkania Z," a novel Chlamydia-like bacterium, in infants with acute bronchiolitis. J. Infect. Dis. 177:1425-1429.
64. Kahane, S., E. Metzer, and M. G. Friedman. 1995. Evidence that the novel microorganism 'Z' may belong to a new genus in the family Chlamydiaceae. FEMS Microbiol. Lett. 126:203-207.
65. Kirby, J. E., and R. R. Isberg. 1998. Legionnaires' disease: the pore macrophage and the legion of terror within. Trends Microbiol. 6:256-258.
66. Kirby, J. E., J. P. Vogel, H. L. Andrews, and R. R. Isberg. 1998. Evidence for pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27:323-336.
67. Kool, J. L., J. C. Carpenter, and B. S. Fields. 1999. Effect of monochloramine disinfection of municipal drinking water on risk of nosocomial Legionnaires' disease. Lancet 353:272-277.
68. Kusnetsov, J., E. Iivanainen, N. Elomaa, O. Zacheus, and P. J. Martikainen. 2001. Copper and silver ions more effective against legionellae than against mycobacteria in a hospital warm water system. Water Res. 35:4217-4225.
69. Lemanske, R. F., Jr. 2003. Is asthma an infectious disease? Thomas A. Neff lecture. Chest 123:3858-3908.
70. Lieberman, D., S. Kahane, and M. G. Friedman. 1997. Pneumonia with serological evidence of acute infection with the Chlamydia-like microorganism "Z." Am. J. Respir. Crit. Care Med. 156:578-582.
71. Loy, A., M. Horn, and M. Wagner. 2003. probeBase: an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res. 31:514-516.
72. Mann, B. J., B. E. Torian, T. S. Vedvick, and W. A. J. Petri. 1991. Sequence of a cysteine-rich galactose-specific lectin of Entamoeba histotytica. Proc. Natl. Acad. Sci. USA 88:3248-3252.
73. Marra, A., M. A. Horwitz, and H. A. Shuman. 1990. The HL-60 model for the interaction of human macrophages with the Legionnaires' disease bacterium. J. Immunol. 144:2738-2744.
74. Marrie, T. J., R. W. Peeling, M. J. Fine, D. E. Singer, C. M. Coley, and W. N. Kapoor. 1996. Ambulatory patients with community-acquired pneumonia: the frequency of atypical agents and clinical course. Am. J. Med. 101:508-515.
75. Marrie, T. J., D. Raoult, B. La Scola, R. J. Birtles, and E. de Carolis. 2001. Legionella-like and other amoebal pathogens as agents of community-acquired pneumonia. Emerg. Infect. Dis. 7:1026-1029.
76. Molmeret, M., D. M. Bitar, L. Han, and Y. A. Kwaik. 2004. Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect. Immun. 72:4040-4051.
77. Muraca, P., J. E. Stout, and V. L. Yu. 1987. Comparative assessment of chlorine, heat, ozone, and UV light for killing Legionella pneumophila within a model plumbing system. Appl. Environ. Microbiol. 53:447-453.
78. Newsome, A. L., R. L. Baker, R. D. Miller, and R. R. Arnold. 1985. Interactions between Naegleria fowleri and Legionella pneumophila. Infect. Immun. 50:449-452.
79. O'Brein, S. J., and R. S. Bhopal. 1993. Legionnaires' disease: the infective dose paradox. Lancet 342:5-6.
80. Ossewaarde, J. M., and A. Meijer. 1999. Molecular evidence for the existence of additional members of the order Chlamydiales. Microbiology 145: 411-417.
81. Payne, N. R., and M. A. Horwitz. 1987. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166:1377-1389.
82. Pennisi, E. 2003. Systems biology. Tracing life's circuitry. Science 302:1646-1649.
83. Poppert, S., A. Essig, R. Marre, M. Wagner, and M. Horn. 2002. Detection and differentiation of chlamydiae by fluorescence in situ hybridization. Appl. Environ. Microbiol. 68:4081-4089.
84. Proca-Ciobanu, M., G. H. Lupascu, A. Petrovici, and M. D. Ionescu. 1975. Electron microscopic study of a pathogenic Acanthamoeba castellani strain: the presence of bacterial endosymbionts. Int. J. Parasitol. 5:49-56.
85. Rodriguez-Zaragoza, S. 1994. Ecology of free-living amoebae. Crit. Rev. Microbiol. 20:225-241.
86. Rowbotham, T. J. 1986. Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci. 22:678-689.
87. Rowbotham, T. J. 1983. Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J. Clin. Pathol. 36:978-986.
88. Rowbotham, T. J. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33: 1179-1183.
89. Roy, C. R., and L. G. Tilney. 2002. The road less traveled: transport of Legionella to the endoplasmic reticulum. J. Cell Biol. 158:415-419.
90. Rurangirwa, F. R., P. M. Dilbeck, T. B. Crawford, T. C. McGuire, and T. F. McElwain. 1999. Analysis of the 16S rRNA gene of micro-organism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov., Waddlia chondrophila gen. nov., sp. nov. Int. J. Syst. Bacteriol. 49:577-581.
91. Schachter, J. 1999. Infection and disease epidemiology, p. 139-146. In R. S. Stephens (ed.), Chlamydia. American Society for Microbiology, Washington, D.C.
92. Schmitz-Esser, S., N. Linka, A. Collingro, C. L. Beier, H. E. Neuhaus, M. Wagner, and M. Horn. 2004. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to chlamydiae and rickettsiae. J. Bacteriol. 186:683-691.
93. Segal, G., and H. A. Shuman. 1999. Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect. Immun. 67:2117-2124.
94. Solomon, J. M., and R. R. Isberg. 2000. Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions. Trends Microbiol. 8:478-480.
95. Solomon, J. M., A. Rupper, J. A. Cardelli, and R. R. Isberg. 2000. Intra-cellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect. Immun. 68:2939-2947.
96. Steinert, M., L. Emody, R. Amann, and J. Hacker. 1997. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63:2047-2053.
97. Stone, B. J., A. Brier, and Y. A. Kwaik. 1999. The Legionella pneumophila prp locus; required during infection of macrophages and amoebae. Microb. Pathog. 27:369-376.
98. Swanson, M. S., and R. R. Isberg. 1995. Formation of the Legionella pneumophila replicative phagosome. Infect. Agents Dis. 2:269-271.
99. Thao, M. L., L. Baumann, J. M. Hess, B. W. Falk, J. C. Ng, P. J. Gullan, and P. Baumann. 2003. Phylogenetic evidence for two new insect-associated chlamydia of the family Simkaniaceae. Curr. Microbiol. 47:46-50.
100. Tilney, L. G., O. S. Harb, P. S. Connelly, C. G. Robinson, and C. R. Roy. 2001. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J. Cell Sci. 114:4637-4650.
101. Tjaden, J., H. H. Winkler, C. Schwoppe, M. Van Der Laan, T. Mohlmann, and H. E. Neuhaus. 1999. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181:1196-1202.
102. Venkataraman, C., B. J. Haack, S. Bondada, and Y. Abu Kwaik. 1997. Identification of a Gal/GalNAc lectin in the protozoan Hartmannella vermiformis as a potential receptor for attachment and invasion by the Legionnaires' disease bacterium, Legionella pneumophila. J. Exp. Med. 186: 537-547.
103. Winkler, H. H., and H. E. Neuhaus. 1999. Non-mitochondrial ATP transport. Trends Biochem. Sci. 24:64-68.
104. Yamamoto, H., T. Ezaki, M. Ikedo, and E. Yabuucbi. 1991. Effects of biocidal treatments to inhibit the growth of legionellae and other microorganisms in cooling towers. Microbiol. Immunol. 35:795-802.