Modulation of caspases and their non-apoptotic functions by Legionella pneumophila

Cellular Microbiology

Volumn 12, Issue 2, 2010, Pages 140-147

  Amer, Amal O ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CASPASE; CASPASE 3; CASPASE 7; FLAGELLIN; INTERLEUKIN 1BETA CONVERTING ENZYME; NEURONAL APOPTOSIS INHIBITORY PROTEIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR 4; PROTEIN DOT; PROTEIN ICM; UNCLASSIFIED DRUG;

APOPTOSIS; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIRULENCE; CELL VACUOLE; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; MACROPHAGE ACTIVATION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TYPE IV SECRETION SYSTEM; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; MURINAE;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; CASPASE 1; CASPASE 3; CASPASE 7; CASPASES; LEGIONELLA PNEUMOPHILA; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 77649202817     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01401.x     Document Type: Review

References (88)

1. Abu-Zant A, Santic M, Molmeret M, Jones S, Helbig J, Abu Kwaik Y. Incomplete activation of macrophage apoptosis during intracellular replication of Legionella pneumophila. Infect Immun 2005, 73:5339-5349.
2. Abu-Zant A, Jones S, Asare R, Suttles J, Price C, Graham J, Kwaik YA. Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell Microbiol 2007, 9:246-264.
3. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. [see comment]. Immunity 2004, 20:319-325.
4. Akhter A, Gavrilin MA, Frantz L, Washington S, Ditty C, Limoli D. Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 2009, 5:e1000361.
5. Akira S. Innate immunity to pathogens: diversity in receptors for microbial recognition. Immunolog Rev 2009, 227:5-8.
6. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, Taxman DJ. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. [see comment]. Immunity 2009, 30:556-565.
7. Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 2005, 7:765-778.
8. Amer AO, Franchi L, Kanneganti TD, Body-Malapel M, Ozoren N, Brady G. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J Biol Chem 2006, 281:35217-35223.
9. Amor JC, Swails J, Zhu X, Roy CR, Nagai H, Ingmundson A. The structure of RalF, an ADP-ribosylation factor guanine nucleotide exchange factor from Legionella pneumophila, reveals the presence of a cap over the active site. J Biol Chem 2005, 280:1392-1400.
10. Banga S, Gao P, Shen X, Fiscus V, Zong WX, Chen L, Luo ZQ. Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci USA 2007, 104:5121-5126.
11. Bartfeld S, Engels C, Bauer B, Aurass P, Flieger A, Brüggemann H, Meyer T. Temporal resolution of two-tracked NF-kappaB activation by Legionella pneumophila. Cell Microbiol 2009, 11:1638-1651.
12. Berger KH, Isberg RR. Intracellular survival by Legionella. Methods Cell Biol 1994, 45:247-259.
13. Berger KH, Merriam JJ, Isberg RR. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 1994, 14:809-822.
14. Byrne B, Swanson MS. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 1998, 66:3029-3034.
15. Case CL, Shin S, Roy CR. Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect Immun 2009, 77:1981-1991.
16. Cayrol C, Girard JP. The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc Natl Acad Sci USA 2009, 106:9021-9026.
17. Chai J, Wu Q, Shiozaki E, Srinivasula SM, Alnemri ES, Shi Y. Crystal structure of a procaspase-7 zymogen: mechanisms of activation and substrate binding. Cell 2001, 107:399-407.
18. Chen Q, Carroll HP, Gadina M. The newest interleukins: recent additions to the ever-growing cytokine family. Vitam Horm 2006, 74:207-228.
19. Damiano JS, Oliveira V, Welsh K, Reed JC. Heterotypic interactions among NACHT domains: implications for regulation of innate immune responses. Biochem J 2004, 381:213-219.
20. Denault JB, Salvesen GS. Human caspase-7 activity and regulation by its N-terminal peptide. J Biolog Chem 2003, 278:34042-34050.
21. Derre I, Isberg RR. Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect Immun 2004, 72:6221-6229.
22. Diez E, Yaraghi Z, MacKenzie A, Gros P. The neuronal apoptosis inhibitory protein (Naip) is expressed in macrophages and is modulated after phagocytosis and during intracellular infection with Legionella pneumophila. J Immunol 2000, 164:1470-1477.
23. Diez E, Lee SH, Gauthier S, Yaraghi Z, Tremblay M, Vidal S, Gros P. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat Genet 2003, 33:55-60.
24. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, Pericone CD, Shuman HA. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 2008, 4:e1000117.
25. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009, 458:509-513.
26. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005, 73:1907-1916.
27. Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 2006, 8:1812-1825.
28. Fischer SF, Vier J, Muller-Thomas C, Hacker G. Induction of apoptosis by Legionella pneumophila in mammalian cells requires the mitochondrial pathway for caspase activation. Microbes Infect 2006, 8:662-669.
29. Fortier A, Diez E, Gros P. Naip5/Birc1e and susceptibility to Legionella pneumophila. Trends Microbiol 2005, 13:328-335.
30. Fortier A, de Chastellier C, Balor S, Gros P. Birc1e/Naip5 rapidly antagonizes modulation of phagosome maturation by Legionella pneumophila. Cell Microbiol 2007, 9:910-923.
31. Fortier A, Doiron K, Saleh M, Grinstein S, Gros P. Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irf1/Irf8 and nod-like receptors Naip5 and Nlrc4. Infect Immun 2009, 77:4794-4805.
32. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, Jagirdar R. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. [see comment]. Nat Immunol 2006, 7:576-582.
33. Furugen M, Higa F, Hibiya K, Teruya H, Akamine M, Haranaga S. Legionella pneumophila infection induces programmed cell death, caspase activation, and release of high-mobility group box 1 protein in A549 alveolar epithelial cells: inhibition by methyl prednisolone. Respir Res 2008, 9:39.
34. Fuse ET, Tateda K, Kikuchi Y, Matsumoto T, Gondaira F, Azuma A. Role of Toll-like receptor 2 in recognition of Legionella pneumophila in a murine pneumonia model. J Med Microbiol 2007, 56:305-312.
35. Gavrilin MA, Mitra S, Seshadri S, Nateri J, Berhe F, Hall MW, Wewers MD. Pyrin critical to macrophage IL-1beta response to Francisella challenge. J Immunol 2009, 182:7982-7989.
36. Ge J, Xu H, Li T, Zhou Y, Zhang Z, Li S. A Legionella type IV effector activates the NF-{kappa}B pathway by phosphorylating the I{kappa}B family of inhibitors: Proc Natl Acad Sci USA. 2009, 106:13725-13730.
37. Harb OS, Gao LY, Abu Kwaik Y. From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ Microbiol 2000, 2:251-265.
38. Hawn TR, Berrington WR, Smith IA, Uematsu S, Akira S, Aderem A. Altered inflammatory responses in TLR5-deficient mice infected with Legionella pneumophila. J Immunol 2007, 179:6981-6987.
39. Heuner K, Steinert M. The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int J Med Microbiol 2003, 293:133-143.
40. Horwitz MA. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 1983, 158:2108-2126.
41. Isberg RR, O'Connor TJ, Heidtman M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 2009, 7:13-24.
42. Kuribayashi K, Mayes PA, El-Deiry WS. What are caspases 3 and 7 doing upstream of the mitochondria? Cancer Biol Ther 2006, 5:763-765.
43. 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, 103:18745-18750.
44. Lamkanfi M, Dixit VM. IL-33 raises alarm. Immunity 2009, 31:5-7.
45. Lamkanfi M, Kanneganti TD, Franchi L, Nunez G. Caspase-1 inflammasomes in infection and inflammation. J Leukoc Biol 2007, 82:220-225.
46. Lamkanfi M, Kanneganti TD, Van Damme P, Vanden Berghe T, Vanoverberghe I, Vandekerckhove J. Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol Cell Proteomics 2008, 7:2350-2363.
47. Lamkanfi M, Moreira LO, Makena P, Spierings DC, Boyd K, Murray PJ. Caspase-7 deficiency protects from endotoxin-induced lymphocyte apoptosis and improves survival. Blood 2009, 113:2742-2745.
48. Launay S, Hermine O, Fontenay M, Kroemer G, Solary E, Garrido C. Vital functions for lethal caspases. Oncogene 2005, 24:5137-5148.
49. Li J, Yuan J. Caspases in apoptosis and beyond. Oncogene 2008, 27:6194-6206.
50. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, Dunipace EA. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 2008, 9:1171-1178.
51. Losick VP, Isberg RR. NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J Exp Med 2006, 203:2177-2189.
52. Losick VP, Stephan K, Smirnova II, Isberg RR, Poltorak A. A hemidominant Naip5 allele in mouse strain MOLF/Ei-derived macrophages restricts Legionella pneumophila intracellular growth. Infect Immun 2009, 77:196-204.
53. Luo ZQ, Isberg RR. Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA 2004, 101:841-846.
54. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004, 430:213-218.
55. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002, 10:417-426.
56. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. [see comment]. Nat Immunol 2006, 7:569-575.
57. Molmeret M, Bitar DM, Han L, Kwaik YA. Cell biology of the intracellular infection by Legionella pneumophila. Microbes Infect 2004a, 6:129-139.
58. Molmeret M, Zink SD, Han L, Abu-Zant A, Asari R, Bitar DM, Abu Kwaik Y. Activation of caspase-3 by the Dot/Icm virulence system is essential for arrested biogenesis of the Legionella-containing phagosome. Cell Microbiol 2004b, 6:33-48.
59. Molofsky AB, Shetron-Rama LM, Swanson MS. Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 2005, 73:5720-5734.
60. Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, Tateda K, Swanson MS. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 2006, 203:1093-1104.
61. Newton CA, Perkins I, Widen RH, Friedman H, Klein TW. Role of Toll-like receptor 9 in Legionella pneumophila-induced interleukin-12 p40 production in bone marrow-derived dendritic cells and macrophages from permissive and nonpermissive mice. Infect Immun 2007, 75:146-151.
62. Nogueira C, Lindsten T, Jamieson A, Case C, Shin S, Thompson C, Roy C. Rapid pathogen-induced apoptosis: a mechanism used by dendritic cells to limit intracellular replication of Legionella pneumophila. PLoS Pathog 2009, 5:e1000478.
63. Pop C, Salvesen G. Human caspases: activation, specificity, and regulation. J Biol Chem 2009, 284:21777-21781.
64. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2006, 2:e18.
65. Roberts TL, Idris A, Dunn JA, Kelly GM, Burnton CM, Hodgson S. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009, 323:1057-1060.
66. Roy CR, Berger KH, Isberg RR. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 1998, 28:663-674.
67. Salvesen GS. Caspases and apoptosis. Essays Biochem 2002, 38:9-19.
68. Santic M, Asare R, Doric M, Abu Kwaik Y. Host-dependent trigger of caspases and apoptosis by Legionella pneumophila. Infect Immun 2007, 75:2903-2913.
69. Scott CC, Botelho RJ, Grinstein S. Phagosome maturation: a few bugs in the system. J Membr Biol 2003, 193:137-152.
70. Segal G, Shuman HA. How is the intracellular fate of the Legionella pneumophila phagosome determined? Trends Microbiol 1998, 6:253-255.
71. Shen X, Banga S, Liu Y, Xu L, Gao P, Shamovsky I. Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell Microbiol 2009, 11:911-926.
72. Shin S, Roy CR. Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 2008, 10:1209-1220.
73. Shohdy N, Efe JA, Emr SD, Shuman HA. Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci USA 2005, 102:4866-4871.
74. Swanson MS, Isberg RR. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 1995, 63:3609-3620.
75. Swanton E, Bishop N, Woodman P. Human rabaptin-5 is selectively cleaved by caspase-3 during apoptosis. J Biolog Chem 1999, 274:37583-37590.
76. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005, 17:1-14.
77. Thomas PG, Dash P, Aldridge JR, Ellebedy AH, Reynolds C, Funk AJ. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 2009, 30:566-575.
78. Thornberry NA. Caspases: key mediators of apoptosis. Chem Biol 1998, 5:R97-R103.
79. Tiemi Shio M, Eisenbarth S, Savaria M, Vinet A, Bellemare M, Harder K. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 2009, 5:e1000559.
80. Tjelle TE, Lovdal T, Berg T. Phagosome dynamics and function. Bioessays 2000, 22:255-263.
81. Van de Craen M, Declercq W, Van den brande I, Fiers W, Vandenabeele P. The proteolytic procaspase activation network: an in vitro analysis. Cell Death Differ 1999, 6:1117-1124.
82. Vieira OV, Botelho RJ, Grinstein S. Phagosome maturation: aging gracefully. Biochem J 2002, 366:689-704.
83. Vogel JP, Andrews HL, Wong SK, Isberg RR. Conjugative transfer by the virulence system of Legionella pneumophila. Science 1998, 279:873-876.
84. Willingham SB, Bergstralh DT, O'Connor W, Morrison AC, Taxman DJ, Duncan JA. Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2007, 2:147-159.
85. Wright EK, Goodart SA, Growney JD, Hadinoto V, Endrizzi MG, Long EM. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr Biol 2003, 13:27-36.
86. Yi CH, Yuan J. The Jekyll and Hyde functions of caspases. Dev Cell 2009, 16:21-34.
87. Zamboni DS, Kobayashi KS, Kohlsdorf T, Ogura Y, Long EM, Vance RE. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 2006, 7:318-325.
88. Zink SD, Pedersen L, Cianciotto NP, Abu-Kwaik Y. The Dot/Icm type IV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect Immun 2002, 70:1657-1663.