Host signal transduction and protein kinases implicated in legionella infection

Current Topics in Microbiology and Immunology

Volumn 376, Issue , 2013, Pages 249-269

  Hempstead, Andrew D ^a   Isberg, Ralph R ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3 RECEPTOR; COMPLEMENT COMPONENT C3B; DUAL SPECIFICITY PHOSPHATASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN KINASE C;

ARTICLE; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BACTERIAL TRANSLOCATION; BACTERIUM ADHERENCE; CELL CONTACT; CELL SURVIVAL; CELLULAR DISTRIBUTION; DICTYOSTELIUM DISCOIDEUM; HUMAN; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; MAMMAL CELL; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TYPE IV SECRETION SYSTEM;

HUMANS; LEGIONELLA PNEUMOPHILA; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84886691921     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/82-2013-342     Document Type: Article

References (90)

1. Adams SA, Robson SC, Gathiram V, Jackson TF, Pillay TS et al (1993) Immunological similarity between the 170 kD amoebic adherence glycoprotein and human beta 2 integrins. Lancet 341:17-19
2. Abu-Zant A, Jones S, Asare R, Suttles J, Price C et al (2007) Anti-apoptotic signaling by the Dot/Icm secretion system of L. pneumophila. Cell Microbiol 9:246-264
3. Backert S, Tegtmeyer N, Selbach M (2010) The versatility of Helicobacter pylori CagA effector protein functions: the master key hypothesis. Helicobacter 15:163-176
4. Bardill JP, Miller JL, Vogel JP (2005) IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 56:90-103
5. Bartfeld S, Engels C, Bauer B, Aurass P, Flieger A et al (2009) Temporal resolution of two-tracked NF-kappaB activation by Legionella pneumophila. Cell Microbiol 11:1638-1651
6. Berger KH, Isberg RR (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7:7-19
7. Black JD (2000) Protein kinase C-mediated regulation of the cell cycle. Front Biosci 5:D406-D423
8. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351-1362
9. Burstein D, Zusman T, Degtyar E, Viner R, Segal G et al (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5:e1000508
10. Caffrey DR, O'Neill LA, Shields DC (1999) The evolution of the MAP kinase pathways: coduplication of interacting proteins leads to new signaling cascades. J Mol Evol 49:567-582
11. Cambronne ED, Roy CR (2007) The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog 3:e188
12. Cargnello M, Roux PP (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75:50-83
13. Charpentier X, Gabay JE, Reyes M, Zhu JW, Weiss A et al (2009) Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog 5:e1000501
14. Chin AI, Dempsey PW, Bruhn K, Miller JF, Xu Y et al (2002) Involvement of receptor-interacting protein 2 in innate and adaptive immune responses. Nature 416:190-194
15. Coers J, Kagan JC, Matthews M, Nagai H, Zuckman DM et al (2000) Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol Microbiol 38:719-736
16. Cohen P (2001) The role of protein phosphorylation in human health and disease. The Sir Hans Krebs Medal Lecture. Eur J Biochem 268:5001-5010
17. Coxon PY, Summersgill JT, Ramirez JA, Miller RD (1998) Signal transduction during Legionella pneumophila entry into human monocytes. Infect Immun 66:2905-2913
18. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M et al (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4:e10000117
19. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF et al (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 187:7716-7726
20. Dorer MS, Kirton D, Bader JS, Isberg RR (2006) RNA interference analysis of Legionella in Drosophila cells: exploitation of early secretory apparatus dynamics. PLoS Pathog 2:e34
21. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR et al (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734-737
22. Fields BS (1996) The molecular ecology of legionellae. Trends Microbiol 4:286-290
23. Fields BS, Nerad TA, Sawyer TK, King CH, Barbaree JM et al (1990) Characterization of an axenic strain of Hartmannella vermiformis obtained from an investigation of nosocomial legionellosis. J Protozool 37:581-583
24. Fontana MF, Banga S, Barry KC, Shen X, Tan Y et al (2011) Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog 7:e1001289
25. Fontana MF, Shin S, Vance RE (2012) Activation of host mitogen-activated protein kinases by secreted Legionella pneumophila effectors that inhibit host protein translation. Infect Immun 80:3570-3575
26. Franco IS, Shohdy N, Shuman HA (2012) The Legionella pneumophila effector VipA is an actin nucleator that alters host cell organelle trafficking. PLoS Pathog 8:e1002546
27. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A et al (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736
28. Fritz JH, Ferrero RL, Philpott DJ, Girardin SE (2006) Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7:1250-1257
29. Garcia-Garcia E, Rosales C (2002) Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 72:1092-1108
30. Gaskins C, Maeda M, Firtel RA (1994) Identification and functional analysis of a developmen-tally regulated extracellular signal-regulated kinase gene in Dictyostelium discoideum. Mol Cell Biol 14:6996-7012
31. Ge J, Xu H, Li T, Zhou Y, Zhang Z et al (2009) A Legionella type IV effector activates the NF-kappaB pathway by phosphorylating the IkappaB family of inhibitors. Proc Natl Acad Sci USA 106:13725-13730
32. Ghayur T, Hugunin M, Talanian RV, Ratnofsky S, Quinlan C et al (1996) Proteolytic activation of protein kinase C delta by an ICE/CED 3-like protease induces characteristics of apoptosis. J Exp Med 184:2399-2404
33. Girardin SE, Tournebize R, Mavris M, Page AL, Li X et al (2001) CARD4/Nod1 mediates NF-kappaB and JNK activation by invasive Shigella flexneri. EMBO Rep 2:736-742
34. Guan KL, Dixon JE (1990) Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249:553-556
35. Haenssler E, Isberg RR (2011) Control of host cell phosphorylation by Legionella pneumophila. Front Microbiol 2:64
36. Hayden MS, Ghosh S (2012) NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26:203-234
37. Hervet E, Charpentier X, Vianney A, Lazzaroni JC, Gilbert C et al (2011) Protein kinase LegK2 is a type IV secretion system effector involved in endoplasmic reticulum recruitment and intracellular replication of Legionella pneumophila. Infect Immun 79:1936-1950
38. Huang G, Shi LZ, Chi H (2009) Regulation of JNK and p38 MAPK in the immune system: signal integration, propagation and termination. Cytokine 48:161-169
39. Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ et al (2011) The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 13:227-245
40. Johnson GL, Lapadat R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298:1911-1912
41. Kawai T, Akira S (2007) TLR signaling. Semin Immunol 19:24-32
42. Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ et al (1998) The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8:297-303
43. Khelef N, Shuman HA, Maxfield FR (2001) Phagocytosis of wild-type Legionella pneumophila occurs through a wortmannin-insensitive pathway. Infect Immun 69:5157-5161
44. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G et al (2002) RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416:194-199
45. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N et al (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307:731-734
46. Kubori T, Hyakutake A, Nagai H (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67:1307-1319
47. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR (2006) A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci USA 103:18745-18750
48. Li H, Xu H, Zhou Y, Zhang J, Long C et al (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315:1000-1003
49. Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2:725-734
50. Li Z, Dugan AS, Bloomfield G, Skelton J, Ivens A et al (2009) The amoebal MAP kinase response to Legionella pneumophila is regulated by DupA. Cell Host Microbe 6:253-267
51. Loegering DJ, Lennartz MR (2011) Protein kinase C and toll-like receptor signaling. Enzyme Res 2011:537821
52. Losick VP, Haenssler E, Moy MY, Isberg RR (2010) LnaB: a Legionella pneumophila activator of NF-kappaB. Cell Microbiol 12:1083-1097
53. Losick VP, Isberg RR (2006) NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J Exp Med 203:2177-2189
54. Manning G, Plowman GD, Hunter T, Sudarsanam S (2002) Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27:514-520
55. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci USA 89:9607-9611
56. Morinaga Y, Yanagihara K, Araki N, Migiyama Y, Nagaoka K et al (2012) Live Legionella pneumophila induces MUC5AC production by airway epithelial cells independently of intracellular invasion. Can J Microbiol 58:151-157
57. N'Guessan PD, Etouem MO, Schmeck B, Hocke AC, Scharf S et al (2007) Legionella pneumophila-induced PKCalpha-, MAPK-, and NF-kappaB-dependent COX-2 expression in human lung epithelium. Am J Physiol Lung Cell Mol Physiol 292:L267-L277
58. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295:679-682
59. Natoli G (2009) Control of NF-kappaB-dependent transcriptional responses by chromatin organization. Cold Spring Harb Perspect Biol 1:a000224
60. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol Microbiol 55:912-926
61. O'Connor TJ, Boyd D, Dorer MS, Isberg RR (2012) Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen. Science 338:1440-1444
62. Ogura Y, Inohara N, Benito A, Chen FF, Yamaoka S et al (2001) Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J Biol Chem 276:4812-4818
63. Patterson KI, Brummer T, O'Brien PM, Daly RJ (2009) Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem J 418:475-489
64. Ray LB, Sturgill TW (1988) Insulin-stimulated microtubule-associated protein kinase is phosphorylated on tyrosine and threonine in vivo. Proc Natl Acad Sci USA 85:3753-3757
65. Retzlaff C, Yamamoto Y, Okubo S, Hoffman PS, Friedman H et al (1996) Legionella pneumophila heat-shock protein-induced increase of interleukin-1 beta mRNA involves protein kinase C signalling in macrophages. Immunology 89:281-288
66. Scharf S, Hippenstiel S, Flieger A, Suttorp N, N'Guessan PD (2010) Induction of human beta-defensin-2 in pulmonary epithelial cells by Legionella pneumophila: involvement of TLR2 and TLR5, p38 MAPK, JNK, NF-kappaB, and AP-1. Am J Physiol Lung Cell Mol Physiol 298:L687-L695
67. Segall JE, Kuspa A, Shaulsky G, Ecke M, Maeda M et al (1995) A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol 128:405-413
68. Shin S, Case CL, Archer KA, Nogueira CV, Kobayashi KS et al (2008) Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog 4:e1000220
69. St-Denis A, Caouras V, Gervais F, Descoteaux A (1999) Role of protein kinase C-alpha in the control of infection by intracellular pathogens in macrophages. J Immunol 163:5505-5511
70. Susa M, Marre R (1999) Legionella pneumophila invasion of MRC-5 cells induces tyrosine protein phosphorylation. Infect Immun 67:4490-4498
71. Swantek JL, Tsen MF, Cobb MH, Thomas JA (2000) IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J Immunol 164:4301-4306
72. Tachado SD, Samrakandi MM, Cirillo JD (2008) Non-opsonic phagocytosis of Legionella pneumophila by macrophages is mediated by phosphatidylinositol 3-kinase. PLoS ONE 3:e3324
73. Takamatsu R, Takeshima E, Ishikawa C, Yamamoto K, Teruya H et al (2010) Inhibition of Akt/GSK3beta signalling pathway by Legionella pneumophila is involved in induction of T-cell apoptosis. Biochem J 427:57-67
74. Tan SL, Parker PJ (2003) Emerging and diverse roles of protein kinase C in immune cell signalling. Biochem J 376:545-552
75. Trosky JE, Mukherjee S, Burdette DL, Roberts M, McCarter L et al (2004) Inhibition of MAPK signaling pathways by VopA from Vibrio parahaemolyticus. J Biol Chem 279:51953-51957
76. Ubersax JA, Ferrell JE Jr (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8:530-541
77. Vardarova K, Scharf S, Lang F, Schmeck B, Opitz B et al (2009) PKC(alpha) and PKC(epsilon) differentially regulate Legionella pneumophila-induced GM-CSF. Eur Respir J 34:1171-1179
78. Venkataraman C, Gao LY, Bondada S, Kwaik YA (1998) Identification of putative cytoskeletal protein homologues in the protozoan host Hartmannella vermiformis as substrates for induced tyrosine phosphatase activity upon attachment to the Legionnaires' disease bacterium, Legionella pneumophila. J Exp Med 188:505-514
79. Venkataraman C, Haack BJ, Bondada S, Abu Kwaik Y (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. J Exp Med 186:537-547
80. Venkataraman C, Kwaik YA (2000) Signal transduction in the protozoan host Hartmannella vermiformis upon attachment to Legionella pneumophila. Microbes Infect 2:867-875
81. Ventura C, Maioli M (2001) Protein kinase C control of gene expression. Crit Rev Eukaryot Gene Expr 11:243-267
82. Verstrepen L, Bekaert T, Chau TL, Tavernier J, Chariot A et al (2008) TLR-4, IL-1R and TNF-R signaling to NF-kappaB: variations on a common theme. Cell Mol Life Sci 65:2964-2978
83. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M et al (1998) Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 248:706-711
84. Weinstein SL, Sanghera JS, Lemke K, DeFranco AL, Pelech SL (1992) Bacterial lipopolysac-charide induces tyrosine phosphorylation and activation of mitogen-activated protein kinases in macrophages. J Biol Chem 267:14955-14962
85. Welsh CT, Summersgill JT, Miller RD (2004) Increases in c-Jun N-terminal kinase/stress-activated protein kinase and p38 activity in monocyte-derived macrophages following the uptake of Legionella pneumophila. Infect Immun 72:1512-1518
86. Xiao H, Liu M (2012) Atypical protein kinase C in cell motility. Cell Mol Life Sci doi:10.1007/s00018-012-1192-1
87. Zhang ZY, Zhou B, Xie L (2002) Modulation of protein kinase signaling by protein phosphatases and inhibitors. Pharmacol Ther 93:307-317
88. Zhu JW, Brdicka T, Katsumoto TR, Lin J, Weiss A (2008) Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28:183-196
89. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R et al (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE 6:e17638
90. Zuckman DM, Hung JB, Roy CR (1999) Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol Microbiol 32:990-1001