The professional phagocyte Dictyostelium discoideum as a model host for bacterial pathogens

Current Drug Targets

Volumn 12, Issue 7, 2011, Pages 942-954

  Bozzaro, Salvatore ^a   Eichinger, Ludwig ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Amoeba; Dictyostelium discoideum; Drug targets; Functional analysis; Infection; Legionella pneumophila; Model organism; Mycobacteria; Pathogen; Salmonella typhimurium; Social amoeba; Virulence factor

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 MORPHOLINO 8 PHENYLCHROMONE; ALPHA ACTININ; CALCIUM; CALNEXIN; CALRETICULIN; CISPLATIN; EDETIC ACID; EGTAZIC ACID; F ACTIN; KHELLIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROFILIN; VALPROIC ACID; WORTMANNIN;

AUTOPHAGY; BACTERIAL GENE; BACTERIAL VIRULENCE; BETA CHAIN; BURKHOLDERIA CENOCEPACIA; CALCIUM SIGNALING; CELL ADHESION; CELL MATURATION; CHEMOTAXIS; DICTYOSTELIUM DISCOIDEUM; GENE SEQUENCE; HOST CELL; HOST PATHOGEN INTERACTION; KLEBSIELLA PNEUMONIAE; LEGIONELLA PNEUMOPHILA; MAMMAL CELL; MYCOBACTERIUM; MYCOBACTERIUM AVIUM; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PHAGOSOME; PINOCYTOSIS; PROTOZOAL GENETICS; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; VIBRIO CHOLERAE;

EID: 79958128488     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/138945011795677782     Document Type: Review

References (198)

1. Kessin RH. Dictyostelium-evolution, cell biology, and the development of multicellularity. Cambridge, UK: Cambridge Univ Press; 2001.
2. Eichinger L. Revamp a model-status and prospects of the Dictyostelium genome project. Curr Genet 2003; 44(2): 59-72.
3. King JS, Insall RH. Chemotaxis: finding the way forward with Dictyostelium. Trends Cell Biol 2009; 19(10): 523-30.
4. Weijer CJ. Collective cell migration in development. J Cell Sci 2009; 122(Pt 18): 3215-23.
5. Robinson DN, Spudich JA. Mechanics and regulation of cytokinesis. Curr Opin Cell Biol 2004; 16(2): 182-8.
6. Chisholm RL, Firtel RA. Insights into morphogenesis from a simple developmental system. Nat Rev Mol Cell Biol 2004; 5(7): 531-41.
7. Glöckner G, Eichinger L, Szafranski K, et al. Sequence and analysis of chromosome 2 of Dictyostelium discoideum. Nature 2002; 418(6893): 79-85.
8. Eichinger L, Pachebat JA, Glockner G, et al. The genome of the social amoeba Dictyostelium discoideum. Nature 2005; 435(7038): 43-57.
9. Williams JG, Noegel AA, Eichinger L. Manifestations of multicellularity: Dictyostelium reports in. Trends Genet 2005; 21(7): 392-8.
10. Bozzaro S, Bucci C, Steinert M. Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages. Int Rev Cell Mol Biol 2008; 271: 253-300.
11. Cosson P, Soldati T. Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol 2008; 11(3): 271-6.
12. Clarke M. Recent insights into host-pathogen interactions from Dictyostelium. Cell Microbiol 2010; 12(3): 283-91.
13. Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 2004; 17(2): 413-33.
14. Steenbergen JN, Shuman HA, Casadevall A. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci USA 2001; 98(26): 15245-50.
15. Goy G, Thomas V, Rimann K, Jaton K, Prod'hom G, Greub G. The Neff strain of Acanthamoeba castellanii, a tool for testing the virulence of Mycobacterium kansasii. Res Microbiol 2007; 158(4): 393-7.
16. Duhon D, Cardelli J. The regulation of phagosome maturation in Dictyostelium. J Muscle Res Cell Motil 2002; 23: 803-8.
17. Haas A. The phagosome: compartment with a license to kill. Traffic 2007; 8(4): 311-30.
18. Depraitere C, Darmon M. [Growth of "Dictyostelium discoideum" on different species of bacteria (author's transl)]. Ann Microbiol (Paris) 1978; 129 B(3): 451-61.
19. Solomon JM, Rupper A, Cardelli JA, Isberg RR. Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect Immun 2000; 68(5): 2939-47.
20. Hägele S, Kohler R, Merkert H, Schleicher M, Hacker J, Steinert M. Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2000; 2(2): 165-71.
21. Dorer MS, Isberg RR. Non-vertebrate hosts in the analysis of hostpathogen interactions. Microbes Infect 2006; 8: 1637-46.
22. Jin T, Xu X, Fang J, et al. How human leukocytes track down and destroy pathogens: lessons learned from the model organism Dictyostelium discoideum. Immunol Res 2009; 43(1-3): 118-27.
23. Hilbi H, Weber SS, Ragaz C, Nyfeler Y, Urwyler S. Environmental predators as models for bacterial pathogenesis. Environ Microbiol 2007; 9(3): 563-75.
24. Isberg RR, O'Connor TJ, Heidtman M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nature Rev Microbiol 2009; 7(1): 12-24.
25. Kuspa A, Loomis WF. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci USA 1992; 89(18): 8803-7.
26. Li Z, Dugan AS, Bloomfield G, et al. The amoebal MAP kinase response to Legionella pneumophila is regulated by DupA. Cell Host Microbe 2009; 6(3): 253-67.
27. Cosson P, Zulianello L, Join-Lambert O, et al. Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 2002; 184(11): 3027-33.
28. Froquet R, Lelong E, Marchetti A, Cosson P. Dictyostelium discoideum: a model host to measure bacterial virulence. Nature Protoc 2009; 4(1): 25-30.
29. Steinert M, Heuner K. Dictyostelium as host model for pathogenesis. Cell Microbiol 2005; 7(3): 307-14.
30. Weber SS, Ragaz C, Hilbi H. The inositol polyphosphate 5-phosphatase OCRL1 restricts intracellular growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE. Cell Microbiol 2009; 11(3): 442-60.
31. Fraser DW, Tsai TR, Orenstein W, et al. Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 1977; 297(22): 1189-97.
32. Cordevant C, Tang JS, Cleland D, Lange M. Characterization of members of the Legionellaceae family by automated ribotyping. J Clin Microbiol 2003; 41(1): 34-43.
33. Fields BS, Benson RF, Besser RE. Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 2002; 15(3): 506-26.
34. Kwaik YA. Fatal attraction of mammalian cells to Legionella pneumophila. Mol Microbiol 1998; 30(4): 689-95.
35. Lamoth F, Greub G. Amoebal pathogens as emerging causal agents of pneumonia. FEMS Microbiol Rev 2010; 34(3): 260-80.
36. Horwitz MA. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 1983; 158(6): 2108-26.
37. Horwitz MA, Maxfield FR. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol 1984; 99(6): 1936-43.
38. Wintermeyer E, Ludwig B, Steinert M, Schmidt B, Fischer G, Hacker J. Influence of site specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect Immun 1995; 63(12): 4576-83.
39. Francione L, Smith PK, Accari SL, et al. Legionella pneumophila multiplication is enhanced by chronic AMPK signalling in mitochondrially diseased Dictyostelium cells. Dis Model Mech 2009; 2(9-10): 479-89.
40. Swanson MS, Hammer BK. Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 2000; 54: 567-613.
41. Gao LY, Abu Kwaik Y. Activation of caspase 3 during Legionella pneumophila-induced apoptosis. Infect Immun 1999; 67(9): 4886-94.
42. Zhang C, Kuspa A. Transcriptional down-regulation and rRNA cleavage in Dictyostelium discoideum mitochondria during Legionella pneumophila infection. PLoS One 2009; 4(5): e5706.
43. Vogel JP, Andrews HL, Wong SK, Isberg RR. Conjugative transfer by the virulence system of Legionella pneumophila. Science. 1998; 279(5352): 873-6.
44. Cazalet C, Rusniok C, Bruggemann H, et al. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 2004; 36(11): 1165-73.
45. Lau HY, Ashbolt NJ. The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water. J Appl Microbiol 2009; 107(2): 368-78.
46. Steinert M, Leippe M, Roeder T. Surrogate hosts: protozoa and invertebrates as models for studying pathogen-host interactions. Int J Med Microbiol 2003; 293(5): 321-32.
47. Peracino B, Balest A, Bozzaro S. Differential regulation by phosphoinositides of bacterial phagocytosis and Nramp1 (Slc11a1)-induced resistance to Legionella infection in Dictyostelium. J Cell Sci 2010; 123(23): 4039-51.
48. Watarai M, Derre I, Kirby J, Growney JD, Dietrich WF, Isberg RR. Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/Icm system and the mouse Lgn1 locus. J Exp Med 2001; 194(8): 1081-96.
49. Solomon JM, Isberg RR. Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions. Trends Microbiol 2000; 8(10): 478-80.
50. Lu H, Clarke M. Dynamic properties of Legionella-containing phagosomes in Dictyostelium amoebae. Cell Microbiol. 2005; 7: 995-1007.
51. Rook GA, Hamelmann E, Brunet LR. Mycobacteria and allergies. Immunobiology 2007; 212(6): 461-73.
52. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 1999; 282(7): 677-86.
53. DiGiuseppe Champion PA, Champion MM, Manzanillo P, Cox JS. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol Microbiol 2009; 73(5): 950-62.
54. Cole ST, Brosch R, Parkhill J, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393(6685): 537-44.
55. Ramakrishnan L, Federspiel NA, Falkow S. Granuloma-specific expression of Mycobacterium virulence proteins from the glycinerich PE-PGRS family. Science 2000; 288(5470): 1436-9.
56. Chaitra MG, Shaila MS, Nayak R. Detection of interferon gammasecreting CD8+ T lymphocytes in humans specific for three PE/PPE proteins of Mycobacterium tuberculosis. Microbes Infect 2008; 10(8): 858-67.
57. Mehta PK, Pandey AK, Subbian S, et al. Identification of Mycobacterium marinum macrophage infection mutants. Microb Pathog 2006; 40(4): 139-51.
58. Gluckman SJ. Mycobacterium marinum. Clin Dermatol 1995; 13(3): 273-6.
59. Tobin DM, Ramakrishnan L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell Microbiol 2008; 10(5): 1027-39.
60. Shiloh MU, DiGiuseppe Champion PA. To catch a killer. What can mycobacterial models teach us about Mycobacterium tuberculosis pathogenesis? Curr Opin Microbiol 2010; 13(1): 86-92.
61. Pozos TC, Ramakrishnan L. New models for the study of Mycobacterium-host interactions. Curr Opin Immunol 2004; 16(4): 499-505.
62. Zhang S, Kingsley RA, Santos RL, et al. Molecular pathogenesis of Salmonella enterica serotype typhimurium-induced diarrhea. Infect Immun 2003; 71(1): 1-12.
63. Zhou D, Galan J. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 2001; 3(14-15): 1293-8.
64. Patel JC, Galan JE. Manipulation of the host actin cytoskeleton by Salmonella--all in the name of entry. Curr Opin Microbiol 2005; 8(1): 10-5.
65. Drecktrah D, Knodler LA, Ireland R, Steele-Mortimer O. The mechanism of Salmonella entry determines the vacuolar environment and intracellular gene expression. Traffic 2006; 7(1): 39-51.
66. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V. Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 2009; 12(1): 117-24.
67. Valdez Y, Ferreira RB, Finlay BB. Molecular mechanisms of Salmonella virulence and host resistance. Curr Top Microbiol Immunol 2009; 337: 93-127.
68. Rathman M, Sjaastad MD, Falkow S. Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect Immun 1996; 64(7): 2765-73.
69. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1999; 1(1): 33-49.
70. Shea JE, Hensel M, Gleeson C, Holden DW. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 1996; 93(6): 2593-7.
71. Cirillo DM, Valdivia RH, Monack DM, Falkow S. Macrophagedependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 1998; 30(1): 175-88.
72. Hensel M, Shea JE, Waterman SR, et al. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 1998; 30(1): 163-74.
73. Ibarra JA, Steele-Mortimer O. Salmonella--the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 2009; 11(11): 1579-86.
74. Boucrot E, Henry T, Borg JP, Gorvel JP, Meresse S. The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 2005; 308(5725): 1174-8.
75. Henry T, Gorvel JP, Meresse S. Molecular motors hijacking by intracellular pathogens. Cell Microbiol 2006; 8(1): 23-32.
76. Skriwan C, Fajardo M, Hagele S, et al. Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int J Med Microbiol 2002; 291(8): 615-24.
77. Jia K, Thomas C, Akbar M, et al. Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signalingregulated pathogen resistance. Proc Natl Acad Sci USA 2009; 106(34): 14564-9.
78. Amyere M, Mettlen M, Van der Smissen P, et al. Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int J Med Microbiol 2002; 291: 487-94.
79. Maniak M. Conserved features of endocytosis in Dictyostelium. Int Rev Cytol 2002; 221(6): 257-87.
80. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008; 9(8): 639-49.
81. Francis CL, Ryan TA, Jones BD, Smith SJ, Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 1993; 364(6438): 639-42.
82. Alpuche-Aranda CM, Racoosin EL, Swanson JA, Miller SI. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med 1994; 179(2): 601-8.
83. Greenberg S. Signal transduction of phagocytosis. Trends Cell Biol 1995; 5(3): 93-9.
84. Cox D, Greenberg S. Phagocytic signaling strategies: Fc(gamma)receptor-mediated phagocytosis as a model system. Semin Immunol 2001; 13(6): 339-45.
85. Gu H, Botelho RJ, Yu M, Grinstein S, Neel BG. Critical role for scaffolding adapter Gab2 in Fc gamma R-mediated phagocytosis. J Cell Biol 2003; 161(6): 1151-61.
86. Peracino B, Borleis J, Jin T, et al. G protein beta subunit-null mutants are impaired in phagocytosis and chemotaxis due to inappropriate regulation of the actin cytoskeleton. J Cell Biol 1998; 141(7): 1529-37.
87. Gotthardt D, Blancheteau V, Bosserhoff A, Ruppert T, Delorenzi M, Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Mol Cell Proteomics 2006; 5(12): 2228-43.
88. Fey P, Stephens S, Titus MA, Chisholm RL. SadA, a novel adhesion receptor in Dictyostelium. J Cell Biol 2002; 159(6): 1109-19.
89. Cornillon S, Gebbie L, Benghezal M, et al. An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features. EMBO Rep 2006; 7(6): 617-21.
90. Cornillon S, Pech E, Benghezal M, et al. Phg1p is a ninetransmembrane protein superfamily member involved in dictyostelium adhesion and phagocytosis. J Biol Chem 2000; 275(44): 34287-92.
91. Lemmon MA. Pleckstrin homology (PH) domains and phosphoinositides. Biochem Soc Symp 2007; (74): 81-93.
92. Botelho RJ, Teruel M, Dierckman R, et al. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J Cell Biol 2000; 151(7): 1353-68.
93. Vieira OV, Botelho RJ, Rameh L, et al. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J Cell Biol 2001; 155(1): 19-25.
94. Dormann D, Weijer G, Dowler S, Weijer CJ. In vivo analysis of 3-phosphoinositide dynamics during Dictyostelium in phagocytosis and chemotaxis. J Cell Sci 2004; 117: 6497-509.
95. Scott CC, Dobson W, Botelho RJ, et al. Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J Cell Biol 2005; 169(1): 139-49.
96. Zhou K, Pandol S, Bokoch G, Traynor-Kaplan AE. Disruption of Dictyostelium PI3K genes reduces [32P]phosphatidylinositol 3, 4 bisphosphate and [32P]phosphatidylinositol trisphosphate levels, alters F-actin distribution and impairs pinocytosis. J Cell Sci 1998; 111: 283-94.
97. Seastone DJ, Zhang LY, Buczynski G, et al. The small Mr Ras-like GTPase Rap1 and the phospholipase C pathway act to regulate phagocytosis in Dictyostelium discoideum. Mol Biol Cell 1999; 10: 393-406.
98. Cheeseman KL, Ueyama T, Michaud TM, et al. Targeting of protein kinase C-epsilon during Fcgamma receptor-dependent phagocytosis requires the epsilonC1B domain and phospholipase C-gamma1. Mol Biol Cell 2006; 17(2): 799-813.
99. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006; 16(10): 522-9.
100. Pollitt AY, Insall RH. Loss of Dictyostelium HSPC300 causes a scar-like phenotype and loss of SCAR protein. BMC Cell Biol 2009; 10: 13.
101. Somesh BP, Neffgen C, Iijima M, Devreotes P, Rivero F. Dictyostelium RacH regulates endocytic vesicular trafficking and is required for localization of vacuolin. Traffic 2006; 7: 1194-212.
102. Rupper A, Grove B, Cardelli J. Rab7 regulates phagosome maturation in Dictyostelium. J Cell Sci 2001; 114: 2449-60.
103. Gotthardt D, Warnatz HJ, Henschel O, Bruckert F, Schleicher M, Soldati T. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell 2002; 13: 3508-20.
104. Clarke M, Kohler J, Arana Q, Liu TY, Heuser J, Gerisch G. Dynamics of the vacuolar H+-ATPase in the contractile vacuole complex and the endosomal pathway of Dictyostelium cells. J Cell Sci 2002; 115: 2893-905.
105. Peracino B, Wagner C, Balest A, et al. Function and mechanism of action of Dictyostelium Nramp1 (Slc11a1) in bacterial infection. Traffic 2006; 7(1): 22-38.
106. Ellson CD, Anderson KE, Morgan G, et al. Phosphatidylinositol 3-phosphate is generated in phagosomal membranes. Curr Biol 2001; 11(20): 1631-5.
107. Yeung T, Ozdamar B, Paroutis P, Grinstein S. Lipid metabolism and dynamics during phagocytosis. Curr Opin Cell Biol 2006; 18(4): 429-37.
108. Clarke M, Maddera L, Engel U, Gerisch G. Retrieval of the vacuolar H-ATPase from phagosomes revealed by live cell imaging. PLoS One 2010; 5(1): e8585.
109. Vieira OV, Bucci C, Harrison RE, et al. Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol 2003; 23(7): 2501-14.
110. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 2003; 23(18): 6494-506.
111. Kitano M, Nakaya M, Nakamura T, Nagata S, Matsuda M. Imaging of Rab5 activity identifies essential regulators for phagosome maturation. Nature 2008; 453(7192): 241-5.
112. Laurent O, Bruckert F, Adessi C, Satre M. In vitro reconstituted Dictyostelium discoideum early endosome fusion is regulated by Rab7 but proceeds in the absence of ATP-Mg2+ from the bulk solution. J Biol Chem 1998; 273: 793-9.
113. Harris E, Cardelli J. RabD, a Dictyostelium Rab14-related GTPase, regulates phagocytosis and homotypic phagosome and lysosome fusion. J Cell Sci 2002; 115: 3703-13.
114. Smith AC, Heo WD, Braun V, et al. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 2007; 176(3): 263-8.
115. Urwyler S, Nyfeler Y, Ragaz C, et al. Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases. Traffic 2009; 10(1): 76-87.
116. Shevchuk O, Batzilla C, Hagele S, et al. Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium. Int J Med Microbiol 2009; 299(7): 489-508.
117. Voth DE, Heinzen RA. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 2007; 9(4): 829-40.
118. Voth DE, Heinzen RA. Coxiella type IV secretion and cellular microbiology. Curr Opin Microbiol 2009; 12(1): 74-80.
119. Subbian S, Mehta PK, Cirillo SL, Bermudez LE, Cirillo JD. A Mycobacterium marinum mel2 mutant is defective for growth in macrophages that produce reactive oxygen and reactive nitrogen species. Infect Immun 2007; 75(1): 127-34.
120. Philips JA. Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 2008; 10(12): 2408-15.
121. Hagedorn M, Soldati T. Flotillin and RacH modulate the intracellular immunity of Dictyostelium to Mycobacterium marinum infection. Cell Microbiol 2007; 9(11): 2716-33.
122. Hagedorn M, Rohde KH, Russell DG, Soldati T. Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 2009; 323(5922): 1729-33.
123. Derre I, Isberg RR. Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 2004; 72(5): 3048-53.
124. Kagan JC, Stein MP, Pypaert M, Roy CR. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 2004; 199(9): 1201-11.
125. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2006; 2(5): e46.
126. Ragaz C, Pietsch H, Urwyler S, Tiaden A, Weber SS, Hilbi H. The Legionella pneumophila phosphatidylinositol-4 phosphate-binding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell Microbiol 2008; 10(12): 2416-33.
127. Schoebel S, Blankenfeldt W, Goody RS, Itzen A. High-affinity binding of phosphatidylinositol 4-phosphate by Legionella pneumophila DrrA. EMBO Rep 2010; 11(8): 598-604.
128. Kyei GB, Vergne I, Chua J, et al. Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J 2006; 25(22): 5250-9.
129. Roberts EA, Chua J, Kyei GB, Deretic V. Higher order Rab programming in phagolysosome biogenesis. J Cell Biol 2006; 174(7): 923-9.
130. Parra-Lopez C, Lin R, Aspedon A, Groisman EA. A Salmonella protein that is required for resistance to antimicrobial peptides and transport of potassium. EMBO J 1994; 13(17): 3964-72.
131. Blanc-Potard AB, Groisman EA. The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 1997; 16(17): 5376-85.
132. Ammendola S, Pasquali P, Pistoia C, et al. High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect Immun 2007; 75(12): 5867-76.
133. Papp-Wallace KM, Nartea M, Kehres DG, et al. The CorA Mg2+ channel is required for the virulence of Salmonella enterica serovar typhimurium. J Bacteriol 2008; 190(19): 6517-23.
134. Gobin J, Horwitz MA. Exochelins of Mycobacterium tuberculosis remove iron from human iron-binding proteins and donate iron to mycobactins in the M. tuberculosis cell wall. J Exp Med 1996; 183(4): 1527-32.
135. Robey M, Cianciotto NP. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun 2002; 70(10): 5659-69.
136. De Voss JJ, Rutter K, Schroeder BG, Su H, Zhu Y, Barry CE, 3rd. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc Natl Acad Sci USA 2000; 97(3): 1252-7.
137. Courville P, Chaloupka R, Cellier MF. Recent progress in structure-function analyses of Nramp proton-dependent metal-ion transporters. Biochem Cell Biol 2006; 84(6): 960-78.
138. Bellamy R. Susceptibility to mycobacterial infections: the importance of host genetics. Genes Immun 2003; 4(1): 4-11.
139. Jabado N, Cuellar-Mata P, Grinstein S, Gros P. Iron chelators modulate the fusogenic properties of Salmonella-containing phagosomes. Proc Natl Acad Sci USA 2003; 100(10): 6127-32.
140. Malik S, Abel L, Tooker H, et al. Alleles of the NRAMP1 gene are risk factors for pediatric tuberculosis disease. Proc Natl Acad Sci USA 2005; 102(34): 12183-8.
141. Huang J, Klionsky DJ. Autophagy and human disease. Cell Cycle 2007; 6(15): 1837-49.
142. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10(7): 458-67.
143. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9(10): 1102-9.
144. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119(6): 753-66.
145. Kumar D, Nath L, Kamal MA, et al. Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 2010; 140(5): 731-43.
146. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, Krut O. Staphylococcus aureus subvert autophagy for induction of caspaseindependent host cell death. J Biol Chem 2007; 282(4): 2695-706.
147. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular Shigella from autophagy. Science. 2005 Feb 4; 307(5710): 727-31.
148. Otto GP, Wu MY, Clarke M, et al. Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum. Mol Microbiol 2004; 51(1): 63-72.
149. Farbrother P, Wagner C, Na J, et al. Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 2006; 8(3): 438-56.
150. Tung SM, Unal C, Ley A, et al. Loss of Dictyostelium ATG9 results in a pleiotropic phenotype affecting growth, development, phagocytosis and clearance and replication of Legionella pneumophila. Cell Microbiol 2010; 12(6): 765-80.
151. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6(4): 463-77.
152. West CM, McMahon D, Molday RS. Identification of glycoproteins, using lectins as probes, in plasma membranes from Dictyostelium discoideum and human erythrocytes. J Biol Chem 1978; 253(5): 1716-24.
153. Schaloske R, Sordano C, Bozzaro S, Malchow D. Stimulation of calcium influx by platelet activating factor in Dictyostelium. J Cell Sci 1995; 108 (Pt 4): 1597-603.
154. Funamoto S, Milan K, Meili R, Firtel RA. Role of phosphatidylinositol 3' kinase and a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in dictyostelium. J Cell Biol 2001; 153(4): 795-810.
155. Kortholt A, King JS, Keizer-Gunnink I, Harwood AJ, Van Haastert PJ. Phospholipase C regulation of phosphatidylinositol 3,4,5-trisphosphate-mediated chemotaxis. Mol Biol Cell 2007; 18(12): 4772-9.
156. Brown SS, Spudich JA. Cytochalasin inhibits the rate of elongation of actin filament fragments. J Cell Biol 1979; 83(3): 657-62.
157. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 1995; 83(6): 915-24.
158. Konzok A, Weber I, Simmeth E, Hacker U, Maniak M, Muller-Taubenberger A. DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol 1999; 146(2): 453-64.
159. Janetopoulos C, Ma L, Devreotes PN, Iglesias PA. Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc Natl Acad Sci USA 2004; 101(24): 8951-6.
160. Schaloske R, Malchow D. Mechanism of cAMP-induced Ca2+ influx in Dictyostelium: role of phospholipase A2. Biochem J 1997; 327(Pt 1): 233-8.
161. Chen L, Iijima M, Tang M, et al. PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev Cell 2007; 12(4): 603-14.
162. Beug H, Katz FE, Stein A, Gerisch G. Quantitation of membrane sites in aggregating Dictyostelium cells by use of tritiated univalent antibody. Proc Natl Acad Sci USA 1973; 70: 3150-4.
163. Seastone DJ, Lee E, Bush J, Knecht D, Cardelli J. Overexpression of a novel Rho family GTPase, RacC, induces unusual actin-based structures and positively affects phagocytosis in Dictyostelium discoideum. Mol Biol Cell 1998; 9: 2891-904.
164. Eichinger L, Rivero F. Methods in Molecular Biology-Dictyostelium discoideum Protocols. Totowa, NJ: Humana Press; 2006.
165. Schweiger A, Mihalache O, Ecke M, Gerisch G. Stage-specific tyrosine phosphorylation of actin in Dictyostelium discoideum cells. J Cell Sci 1992; 102(Pt 3): 601-9.
166. Howard PK, Sefton BM, Firtel RA. Tyrosine phosphorylation of actin in Dictyostelium associated with cell-shape changes. Science 1993; 259(5092): 241-4.
167. Jungbluth A, Eckerskorn C, Gerisch G, Lottspeich F, Stocker S, Schweiger A. Stress-induced tyrosine phosphorylation of actin in Dictyostelium cells and localization of the phosphorylation site to tyrosine-53 adjacent to the DNase I binding loop. FEBS Lett 1995; 375(1-2): 87-90.
168. Gamper M, Kim E, Howard PK, Ma H, Hunter T, Firtel RA. Regulation of Dictyostelium protein-tyrosine phosphatase-3 (PTP3) through osmotic shock and stress stimulation and identification of pp130 as a PTP3 substrate. J Biol Chem 1999; 274(17): 12129-38.
169. Tillner J, Nau H, Winckler T, Dingermann T. Evaluation of the teratogenic potential of valproic acid analogues in transgenic dictyostelium discoideum strains. Toxicol In Vitro 1998; 12(4): 463-9.
170. Li G, Alexander H, Schneider N, Alexander S. Molecular basis for resistance to the anticancer drug cisplatin in Dictyostelium. Microbiology 2000; 146(Pt 9): 2219-27.
171. Williams RS, Cheng L, Mudge AW, Harwood AJ. A common mechanism of action for three mood-stabilizing drugs. Nature 2002; 417(6886): 292-5.
172. Van Driessche N, Alexander H, Min J, Kuspa A, Alexander S, Shaulsky G. Global transcriptional responses to cisplatin in Dictyostelium discoideum identify potential drug targets. Proc Natl Acad Sci USA 2007; 104(39): 15406-11.
173. Fajardo M, Schleicher M, Noegel A, et al. Calnexin, calreticulin and cytoskeleton-associated proteins modulate uptake and growth of Legionella pneumophila in Dictyostelium discoideum. Microbiology 2004; 150(Pt 9): 2825-35.
174. Dannat K, Tillner J, Winckler T, Weiss M, Eger K, Dingermann T. Effects of medicinal compounds on the differentiation of the eukaryotic microorganism dictyostelium discoideum: can this model be used as a screening test for reproductive toxicity in humans? Pharmazie 2003; 58(3): 204-10.
175. Alexander S, Min J, Alexander H. Dictyostelium discoideum to human cells: pharmacogenetic studies demonstrate a role for sphingolipids in chemoresistance. Biochim Biophys Acta 2006; 1760(3): 301-9.
176. Solomon JM, Leung GS, Isberg RR. Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin. Inf Immun 2003; 71: 3578-86.
177. Pukatzki S, Kessin RH, Mekalanos JJ. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 2002; 99(5): 3159-64.
178. Pukatzki S, Ma AT, Sturtevant D, et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 2006; 103: 1528-33.
179. Benghezal M, Fauvarque MO, Tournebize R, et al. Specific host genes required for the killing of Klebsiella bacteria by phagocytes. Cell Microbiol 2006; 8(1): 139-48.
180. Colucci AM, Peracino B, Tala A, Bozzaro S, Alifano P, Bucci C. Dictyostelium discoideum as a model host for meningococcal pathogenesis. Med Sci Monit 2008; 14(7): BR134-40.
181. Aubert DF, Flannagan RS, Valvano MA. A novel sensor kinaseresponse regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 2008; 76(5): 1979-91.
182. Shina MC, Unal C, Eichinger L, et al. A Coronin7 homolog with functions in actin-driven processes. J Biol Chem 2010; 285(12): 9249-61.
183. Schreiner T, Mohrs MR, Blau-Wasser R, et al. Loss of the F-actin binding and vesicle-associated protein comitin leads to a phagocytosis defect. Eukaryot Cell 2002; 1(6): 906-14.
184. Li Z, Solomon JM, Isberg RR. Dictyostelium discoideum strains lacking the RtoA protein are defective for maturation of the Legionella pneumophila replication vacuole. Cell Microbiol 2005; 7(3): 431-42.
185. Chen G, Zhuchenko O, Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 2007; 317(5838): 678-81.
186. Chen J, deFelipe KS, Clarke M, et al. Legionella effectors that promote nonlytic release from protozoa. Science 2004; 303: 1358-61.
187. Chen J, Reyes M, Clarke M, Shuman HA. Host cell-dependent secretion and translocation of the lepA and lepB effectors of Legionella pneumophila. Cell Microbiol 2007; 9: 1660-71.
188. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR. A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci USA 2006; 103: 18745-50.
189. VanRheenen SM, Luo ZQ, O'Connor T, Isberg RR. Members of a Legionella pneumophila family of proteins with ExoU (phospholipase A) active sites are translocated to target cells. Infect Immun 2006; 74: 3597-606.
190. Tiaden A, Spirig T, Weber SS, et al. The Legionella pneumophila response regulator LqsR promotes host cell interactions as an element of the virulence regulatory network controlled by RpoS and LetA. Cell Microbiol 2007; 9: 2903-20.
191. Tiaden A, Spirig T, Carranza P, et al. Synergistic contribution of the Legionella pneumophila lqs genes to pathogen-host interactions. J Bacteriol 2008; 190(22): 7532-47.
192. Tiaden A, Spirig T, Sahr T, et al. The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ Microbiol 2010; 12(5): 1243-59.
193. Liu Y, Luo ZQ. The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 2007; 75(2): 592-603.
194. Liu M, Conover GM, Isberg RR. Legionella pneumophila EnhC is required for efficient replication in tumour necrosis factor alphastimulated macrophages. Cell Microbiol 2008; 10(9): 1906-23.
195. de Felipe KS, Glover RT, Charpentier X, et al. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 2008; 4(8): e1000117.
196. Hovel-Miner G, Pampou S, Faucher SP, et al. SigmaS controls multiple pathways associated with intracellular multiplication of Legionella pneumophila. J Bacteriol 2009; 191(8): 2461-73.
197. Price CT, Al-Khodor S, Al-Quadan T, et al. Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog 2009; 5(12): e1000704.
198. Alibaud L, Kohler T, Coudray A, et al. Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model. Cell Microbiol 2008; 10(3): 729-40.