Are innate immune signaling pathways in plants and animals conserved?

Nature Immunology

Volumn 6, Issue 10, 2005, Pages 973-979

  Ausubel, Frederick M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CASPASE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CELL RECEPTOR; FLAGELLIN; GLYCOPROTEIN GP 91; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; LEUCINE; LIPOPOLYSACCHARIDE; MANNAN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDOGLYCAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR;

APOPTOSIS; ARABIDOPSIS; CONVERGENT EVOLUTION; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; IMMUNITY; INSECT; INVERTEBRATE; MAMMAL; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MOLECULAR RECOGNITION; NONHUMAN; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; VERTEBRATE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL ADHESION MOLECULES; CYTOSKELETAL PROTEINS; EVOLUTION; IMMUNITY, NATURAL; IMMUNOGLOBULINS; INSECTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE GLYCOPROTEINS; PLANTS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VERTEBRATES;

EID: 27144540463     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni1253     Document Type: Review

References (90)

1. Medzhitov, R. & Janeway, C., Jr. Innate immunity. N. Engl. J. Med. 343, 338-344 (2000).
2. Medzhitov, R. & Janeway, C.A., Jr. An ancient system of host defense. Curr. Opin. Immunol. 10, 12-15 (1998).
3. Gravato-Nobre, M.J. & Hodgkin, J. Caenorhabditis elegans as a model for innate immunity to pathogens. Cell. Microbiol. 7, 741-751 (2005).
4. Kim, D.H. & Ausubel, F.M. Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr. Opin. Immunol. 17, 4-10 (2005).
5. Kurz, C.L. & Ewbank, J.J. Caenorhabditis elegans: An emerging genetic model for the study of innate immunity. Nat. Rev. Genet. 4, 380-390 (2003).
6. Millet, A.C. & Ewbank, J.J. Immunity in Caenorhabditis elegans. Curr. Opin. Immunol. 16, 4-9 (2004).
7. Schulenburg, H., Kurz, C.L. & Ewbank, J.J. Evolution of the innate immune system: The worm perspective. Immunol. Rev. 198, 36-58 (2004).
8. Beutler, B. & Rehli, M. Evolution of the TIR, tolls and TLRs: Functional inferences from computational biology. Curr. Top. Microbiol. Immunol. 270, 1-21 (2002).
9. Brennan, C.A. & Anderson, K.V. Drosophila: The genetics of innate immune recognition and response. Annu. Rev. Immunol. 22, 457-483 (2004).
10. Hoffmann, J.A. & Reichhart, J.M. Drosophila innate immunity: An evolutionary perspective. Nat. Immunol. 3, 121-126 (2002).
11. Janeway, C.A., Jr. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
12. Medzhitov, R. & Janeway, C., Jr. The Toll receptor family and microbial recognition. Trends Microbiol. 8, 452-456 (2000).
13. Royet, J. Infectious non-self recognition in invertebrates: Lessons from Drosophila and other insect models. Mol. Immunol. 41, 1063-1075 (2004).
14. Aderem, A. & Ulevitch, R.J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787 (2000).
15. Anderson, K.V. Toll signaling pathways in the innate immune response. Curr. Opin. Immunol. 12, 13-19 (2000).
16. Belvin, M.P. & Anderson, K.V. A conserved signaling pathway: The Drosophila toll-dorsal pathway. Annu. Rev. Cell Dev. Biol. 12, 393-416 (1996).
17. Gay, N.J. & Keith, F.J. Drosophila Toll and IL-1 receptor. Nature 351, 355-356 (1991).
18. Sun, S.C., Lindstrom, I., Lee, J.Y. & Faye, I. Structure and expression of the attacin genes in Hyalophora cecropia. Eur. J. Biochem. 196, 247-254 (1991).
19. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.M. & Hoffmann, J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983 (1996).
20. Medzhitov, R., Preston-Hurlburt, P. & Janeway, C.A., Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397 (1997).
21. Poltorak, A. et al. Defective LPS signaling in C3H/HeJ and C57BL/ 10ScCr mice: Mutations in Tlr4 gene. Science 282, 2085-2088 (1998).
22. Georgel, P. et al. Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev. Cell 1, 503-514 (2001).
23. Gottar, M. et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416, 640-644 (2002).
24. Ramet, M., Manfruelli, P., Pearson, A., Mathey-Prevot, B. & Ezekowitz, R.A. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416, 644-648 (2002).
25. Steiner, H. Peptidoglycan recognition proteins: On and off switches for innate immunity. Immunol. Rev. 198, 83-96 (2004).
26. Hoffmann, J.A. The immune response of Drosophila. Nature 426 33-38 (2003).
27. Athman, R. & Philpott, D. Innate immunity via Toll-like receptors and Nod proteins. Curr. Opin. Microbiol. 7, 25-32 (2004).
28. Girardin, S.E. & Philpott, D.J. Mini-review: The role of peptidoglycan recognition in innate immunity. Eur. J. Immunol. 34, 1777-1782 (2004).
29. Philpott, D.J. & Girardin, S.E. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 41, 1099-1108 (2004).
30. Viala, J., Sansonetti, P. & Philpott, D.J. Nods and 'intracellular' innate immunity. C. R. Biol. 327, 551-555 (2004).
31. Ting, J.P. & Davis, B.K. CATERPILLER: A novel gene family important in immunity, cell death, and diseases. Annu. Rev. Immunol. 23, 387-414 (2005).
32. Chamaillard, M. et al. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 4, 702-707 (2003).
33. Chamaillard, M., Girardin, S.E., Viala, J. & Philpott, D.J. Nods, Nalps and Naip: Intracellular regulators of bacterial-induced inflammation. Cell. Microbiol. 5, 581-592 (2003).
34. Girardin, S.E. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278 8869-8872 (2003).
35. Tschopp, J., Martinon, F. & Burns, K. NALPs: A novel protein family involved in inflammation. Nat. Rev. Mol. Cell Biol. 4, 95-104 (2003).
36. Martinon, F., Agostini, L., Meylan, E. & Tschopp, J. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14, 1929-1934 (2004).
37. Nurnberger, T., Brunner, F., Kemmerling, B. & Piater, L. Innate immunity in plants and animals: Striking similarities and obvious differences. Immunol. Rev. 198, 249-266 (2004).
38. Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983 (2002).
39. Felix, G., Duran, J.D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276 (1999).
40. Gomez-Gomez, L. & Boller, T. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cells 5, 1003-1011 (2000).
41. Gomez-Gomez, L., Felix, G. & Boller, T. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277-284 (1999).
42. Meindl, T., Boller, T. & Felix, G. The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12, 1783-1794 (2000).
43. Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764-767 (2004).
44. Gomez-Gomez, L. & Boller, T. Flagellin perception: A paradigm for innate immunity. Trends Plant Sci. 7, 251-256 (2002).
45. Shiu, S.H. & Bleecker, A.B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98, 10763-10768 (2001).
46. Shiu, S.H. & Bleecker, A. B. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530-543 (2003).
47. Donnelly, M.A. & Steiner, T.S. Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of toll-like receptor 5. J. Biol. Chem. 277, 40456-40461 (2002).
48. Holt, B.F., III, Hubert, D.A. & Dangl, J.L. Resistance gene signaling in plants-complex similarities to animal innate immunity. Curr. Opin. Immunol. 15, 20-25 (2003).
49. Nimchuk, Z., Eulgem, T., Holt, B.F., III & Dangl, J.L. Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579-609 (2003).
50. Meyers, B.C., Kozik, A., Griego, A., Kuang, H. & Michelmore, R.W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809-834 (2003).
51. Zhou, T. et al. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol. Genet. Genomics 271, 402-415 (2004).
52. Bais, H.P., Prithiviraj, B., Jha, A.K., Ausubel, F.M. & Vivanco, J.M. Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434, 217-221 (2005).
53. Hauck, P., Thilmony, R. & He, S.Y. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100, 8577-8582 (2003).
54. He, P. et al. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J. 37, 589-602 (2004).
55. Hotson, A., Chosed, R., Shu, H., Orth, K. & Mudgett, M.B. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50, 377-389 (2003).
56. Kim, M.G. et al. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121, 749-759 (2005).
57. Orth, K. et al. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290, 1594-1597 (2000).
58. Zhao, Y. et al. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J. 36, 485-499 (2003).
59. Pujol, N. et al. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr. Biol. 11, 809-821 (2001).
60. Mallo, G.V. et al. Inducible antibacterial defense system in C. elegans. Curr. Biol. 12, 1209-1214 (2002).
61. Couillault, C. et al. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 5, 488-494 (2004).
62. Kim, D.H. et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626 (2002).
63. Kim, D.H. et al. Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc. Natl. Acad. Sci. USA 101, 10990-10994 (2004).
64. Liberati, N.T. et al. Requirement for a conserved Toll/ interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. USA 101, 6593-6598 (2004).
65. Matsuzawa, A. et al. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat. Immunol. 6, 587-592 (2005).
66. Mochida, Y. et al. ASK1 inhibits interleukin-1-induced NF-kappa B activity through disruption of TRAF6-TAK1 interaction. J. Biol. Chem. 275, 32747-32752 (2000).
67. Glazebrook, J. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4, 301-308 (2001).
68. Chern, M., Canlas, P.E., Fitzgerald, H.A. & Ronald, P.C. Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant J. 43, 335-345 (2005).
69. Durrant, W.E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209 (2004).
70. Pieterse, C.M. & Van Loon, L.C. NPR1: The spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol. 7, 456-464 (2004).
71. 2+ binding motifs. Plant Cell 10, 255-266 (1998).
72. Torres, M.A. et al. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14, 365-370 (1998).
73. Torres, M.A., Dangl, J.L. & Jones, J.D. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 517-522 (2002).
74. Song, W.Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804-1806 (1995).
75. Burdman, S., Shen, Y., Lee, S.W., Xue, Q. & Ronald, P. RaxH/RaxR: A two-component regulatory system in Xanthomonas oryzae pv. oryzae required for AvrXa21 activity. Mol. Plant Microbe Interact. 17, 602-612 (2004).
76. da Silva, F.G. et al. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol. Plant Microbe Interact. 17, 593-601 (2004).
77. Shen, Y., Sharma, P., da Silva, F.G. & Ronald, P. The Xanthomonas oryzae pv. lozengeoryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5′-phosphosulphate kinase that are required for AvrXa21 avirulence activity. Mol. Microbiol. 44, 37-48 (2002).
78. Dangl, J.L. & Jones, J.D. Plant pathogens and integrated defence responses to infection. Nature 411, 826-833 (2001).
79. Axtell, M.J. & Staskawicz, B.J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369-377 (2003).
80. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R. & Dangl, J.L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389 (2003).
81. Mackey, D., Holt, B.F., Wiig, A. & Dangl, J.L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743-754 (2002).
82. Friedman, R. & Hughes, A.L. Molecular evolution of the NF-κB signaling system. Immunogenetics 53, 964-974 (2002).
83. Luo, C. & Zheng, L. Independent evolution of Toll and related genes in insects and mammals. Immunogenetics 51, 92-98 (2000).
84. Pancer, Z. et al. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430, 174-180 (2004).
85. Nurnberger, T. & Volker, L. Non-host resistance in plants: New insights into an old phenomenon. Mol. Plant Pathol. 6, 335-345 (2005).
86. Meyerowitz, E.M. Plants compared to animals: The broadest comparative study of development. Science 295, 1482-1485 (2002).
87. Diez, E. et al. Bircle is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33, 55-60 (2003).
88. Wright, E.K. et al. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13 27-36 (2003).
89. Stremlau, M. et al. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427, 848-853 (2004).
90. Pan, H. et al. Ipr1 gene mediates innate immunity to tuberculosis. Nature 434, 767-772 (2005).