The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and interleukin 1 receptor pathways

Evolution and Development

Volumn 12, Issue 5, 2010, Pages 519-533

  Gauthier, Marie E A ^a,c   Du Pasquier, Louis ^b   Degnan, Bernard M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR; TOLL LIKE RECEPTOR;

ANTIBIOTICS; ANTIGEN; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOME; LARVAL DEVELOPMENT; SPONGE;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; EMBRYO DEVELOPMENT; EVOLUTION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR GENETICS; PRENATAL DEVELOPMENT; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPONGE (PORIFERA);

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GENOME; LARVA; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PORIFERA; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-1; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

AMPHIMEDON; ANIMALIA; BILATERIA; EUKARYOTA; EUMETAZOA; METAZOA; PLACOZOA;

EID: 77957129335     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2010.00436.x     Document Type: Article

References (98)

1. Adamska M. The evolutionary origin of hedgehog proteins. Curr. Biol. 2007, 17:R836-R837.
2. Anderson K V, Jürgens G, Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 1985, 42:779-789.
3. Auron P E. The interleukin 1 receptor: ligand interactions and signal transduction. Cytokine Growth Factor Rev. 1998, 9:221-237.
4. Ausubel F M. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 2005, 6:973-979.
5. Beamer L J, Carroll S F, Eisenberg D. Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 1997, 276:1861-1864.
6. Bishop C D, Brandhorst B P. On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles. Evol. Dev. 2003, 5:542-550.
7. Böhm M. Molecular response of the sponge Suberites domuncula to bacterial infection. Mar. Biol. 2001, 139:1037-1045.
8. Böhm M, Schröder H C, Müller I M, Müller W E G, Gamulin V. The mitogen-activated protein kinase p38 pathway is conserved in metazoans: cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol. Cell 2000, 92:95-1004.
9. Borchiellini C, Manuel M, Alivon E, Boury-Esnault N, Vacelet J, Le Parco Y. Sponge paraphyly and the origin of Metazoa. J. Evol. Biol. 2001, 14:171-179.
10. Bosch T C G. Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 2009, 33:559-569.
11. Bowie A G, Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 2008, 8:911-922.
12. Burns K. Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat. Cell. Biol. 2000, 2:346-351.
13. Burns K. MyD88, an adapter protein involved in interleukin-1 signaling. J. Biol. Chem. 1998, 273:12203-12209.
14. Cavalier-Smith T, Chao E E-Y. Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J. Mol. Evol. 2003, 56:540-563.
15. Chambon J P. Tail regression in Ciona intestinalis (Prochordate) involves a Caspase-dependent apoptosis event associated with ERK activation. Development 2002, 129:3105-3114.
16. Chen G, Zhuchenko O, Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 2007, 317:678-681.
17. Chen Y, Aulia S, Li L, Tang B L. AMIGO and friends: an emerging family of brain-enriched, neuronal growth modulating, type I transmembrane proteins with leucine-rich repeats (LRR) and cell adhesion molecule motifs. Brain Res. Rev. 2006, 51:265-274.
18. Davidson B, Swalla B J. A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 2002, 129:4739-4751.
19. DeYoung B J, Innes R W. Plant NBS-LRR proteins in pathogen sensing and host defense. Nat. Immunol. 2006, 7:1243-1249.
20. Dunn C W. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
21. Dunn S R, Weis V M. Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environ. Microbiol. 2009, 11:268-276.
22. Dunne A, O'Neill L A J. The Interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci. STKE 2003, 2003:re3.
23. Gauthier M E A, Degnan B M. The transcription factor NF-kappaB in the demosponge Amphimedon queenslandica: insights on the evolutionary origin of the Rel homology domain. Dev. Genes Evol. 2008, 218:23-32.
24. Gazzano-Santoro H. High-affinity binding of the bactericidal/permeability-increasing protein and a recombinant amino-terminal fragment to the lipid A region of lipopolysaccharide. Infect. Immun. 1992, 60:4754-4761.
25. Han J, Mathison J C, Ulevitch R J, Tobias P S. Lipopolysaccharide (LPS) binding protein, truncated at Ile-197, binds LPS but does not transfer LPS to CD14. J. Biol. Chem. 1994, 269:8172-8175.
26. Hashimoto C, Hudson K L, Anderson K V. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 1988, 52:269-279.
27. Hemmrich G, Miller D J, Bosch T C G. The evolution of immunity: a low life perspective. Trends Immunol. 2007, 28:449-454.
28. Hibino T. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 2006, 300:349-365.
29. Hobert O, Westphal H. Functions of LIM-homeobox genes. Trends Genet. 2000, 16:75-83.
30. Horwitz A H. Expression and characterization of cysteine-modified variants of an amino-terminal fragment of bactericidal/permeability-increasing protein. Protein Expr. Purif. 1996, 8:28-40.
31. Huang S. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res. 2008, 18:1112-1126.
32. Hubacek J A, Büchler C, Aslanidis C, Schmitz G. The genomic organization of the genes for human lipopolysaccharide binding protein (LBP) and bactericidal permeability increasing protein (BPI) is highly conserved. Biochem. Biophys. Res. Commun. 1997, 236:427-430.
33. Iovine N, Eastvold J, Elsbach P, Weiss J P, Gioannini T L. The carboxyl-terminal domain of closely related endotoxin-binding proteins determines the target of protein-lipopolysaccharide complexes. J. Biol. Chem. 2002, 277:7970-7978.
34. Iwami K I, Matsuguchi T, Masuda A, Kikuchi T, Musikacharoen T, Yoshikai Y. Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J. Immunol. 2000, 165:6682-6686.
35. Jiang Z, Johnson H J, Nie H, Qin J, Bird T A, Li X. Pellino 1 is required for Interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J. Biol. Chem. 2003, 278:10952-10956.
36. Kawai T, Akira S. Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 2007, 13:460-469.
37. Khan J A, Brint E K, O'Neill L A J, Tong L. Crystal structure of the Toll/interleukin-1 receptor domain of human IL-1RAPL. J. Biol. Chem. 2004, 279:31664-31670.
38. King N. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451:783-788.
39. Larroux C, Luke G N, Koopman P, Rokhsar D S, Shimeld S M, Degnan B M. Genesis and expansion of metazoan transcription factor gene classes. Mol. Biol. Evol. 2008a, 25:980-996.
40. Larroux C. Whole-mount in situ hybridization in Amphimedon. Cold Spring Harb Protoc 2008b, 2008. 10.1101/pdb.prot5096
41. Lemaitre B, Nicolas E, Michaut L, Reichhart J M, Hoffmann J A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
42. Leulier F, Lemaitre B. Toll-like receptors-taking an evolutionary approach. Nat. Rev. Genet. 2008, 9:165-178.
43. Leys S P. Isolation of Amphimedon developmental material. Cold Spring Harb. Protoc. 2008, 10.1101/pdb.prot5095
44. Medina M, Collins A G, Silberman J D, Sogin M L. Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc. Natl. Acad. Sci. USA 2001, 98:9707-9712.
45. Medzhitov R, Preston-Hurlburt P, Janeway C A. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997, 388:394-397.
46. Mikhailov K V. The origin of Metazoa: a transition from temporal to spatial cell differentiation. BioEssays 2009, 31:758-768.
47. Miller D J. The innate immune repertoire in cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 2007, 8:R59.
48. Nakayama-Ishimura A, Chambon J P, Horie T, Satoh N, Sasakura Y. Delineating metamorphic pathways in the ascidian Ciona intestinalis. Dev. Biol. 2009, 326:357-367.
49. Nehyba J, Hrdlièková R, Bose H R. Dynamic evolution of immune system regulators: the history of the interferon regulatory factor family. Mol. Biol. Evol. 2009, 26:2539-2550.
50. Nicotra M L. A hypervariable invertebrate allodeterminant. Curr. Biol. 2009, 19:583-589.
51. Nürnberger T, Brunner F, Kemmerling B, Piater L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 2004, 198:249-266.
52. O'Neill L A J, Bowie A G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7:353-364.
53. Ooi C E, Weiss J, Elsbach P, Frangione B, Mannion B. A 25-kDa NH2-terminal fragment carries all the antibacterial activities of the human neutrophil 60-kDa bactericidal/permeability-increasing protein. J. Biol. Chem. 1987, 262:14891-14894.
54. Ordureau A. The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys63-linked polyubiquitination of IRAK1. Biochem. J. 2008, 409:43-52.
55. Pålsson-McDermott E M, O'Neill L A J. Building an immune system from nine domains. Biochem. Soc. Trans. 2007, 35:1437-1444.
56. Philippe H. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
57. Putnam N H. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94.
58. Radhakrishnan G K, Yu Q, Harms J S, Splitter G A. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J. Biol. Chem. 2009, 284:9892-9898.
59. Rast J P, Messier-Solek C. Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol. Bull. 2008, 214:274-283.
60. Rast J P, Smith L C, Loza-Coll M, Hibino T, Litman G W. Genomic insights into the immune system of the sea urchin. Science 2006, 314:952-956.
61. Richards G S, Degnan B M. The dawn of developmental signaling in the Metazoa. Cold Spring Harb. Symp. Quant. Biol. 2009, 74:81-90.
62. Richards G S, Simionato E, Perron M, Adamska M, Vervoort M, Degnan B M. Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr. Biol. 2008, 18:1156-1161.
63. Roberts B. A complement response may activate metamorphosis in the ascidian Boltenia villosa. Dev. Genes Evol. 2007, 217:449-458.
64. Sakarya O. A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2007, 2:e506.
65. Schauvliege R, Janssens S, Beyaert R. Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett. 2006, 580:4697-4702.
66. Schierwater B. Concatenated analysis sheds light on early metazoan evolution and fuels a modern " urmetazoon" hypothesis. PLoS Biol 2009, 7:e20.
67. Schröder H C, Perović-Ottstadt S, Grebenjuk V A, Engel S, Müller I M, Müller W E G. Biosilica formation in spicules of the sponge Suberites domuncula: synchronous expression of a gene cluster. Genomics 2005, 85:666-678.
68. Schultz H, Weiss J P. The bactericidal/permeability-increasing protein (BPI) in infection and inflammatory disease. Clin. Chim. Acta 2007, 384:12-23.
69. Schumann R R, Lamping N, Hoess A. Interchangeable endotoxin-binding domains in proteins with opposite lipopolysaccharide-dependent activities. J. Immunol. 1997, 159:5599-5605.
70. Schumann R R. Structure and function of lipopolysaccharide binding protein. Science 1990, 249:1429-1431.
71. Shimazu R. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 1999, 189:1777-1782.
72. 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 2001, 98:10763-10768.
73. Sillo A. Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 2008, 9:291.
74. Spear A M, Loman N J, Atkins H S, Pallen M J. Microbial TIR domains: not necessarily agents of subversion? Trends Microbiol. 2009, 17:393-398.
75. Sperling E A, Peterson K J, Pisani D. Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol. Biol. Evol. 2009, 26:2261-2274.
76. Srivastava M. The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955-960.
77. Srivastava M. Early evolution of the LIM homeobox gene family. BMC Biol. 2010a, 8:4.
78. Srivastava M. The genome of Amphimedon queenslandica and the evolution of animal complexity. Nature 2010b, (in press)
79. Steward R. Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 1987, 238:692-694.
80. Thakur N L, Hentschel U, Krasko A, Pabel C T, Anil A C, Müller W E G. Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for epibacterial chemical defense. Aquat. Microb. Ecol. 2003, 31:77-83.
81. Theofan G. An amino-terminal fragment of human lipopolysaccharide-binding protein retains lipid A binding but not CD14-stimulatory activity. J. Immunol. 1994, 152:3623-3629.
82. Tirapé A, Bacque C, Brizard R, Vandenbulcke F, Boulo V. Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev. Comp. Immunol. 2007, 31:859-873.
83. Tobias P S, Soldau K, Ulevitch R J. Identification of a lipid A binding site in the acute phase reactant lipopolysaccharide binding protein. J. Biol. Chem. 1989, 264:10867-10871.
84. Wells C A. Alternate transcription of the Toll-like receptor signaling cascade. Genome Biol. 2006, 7:R10.
85. Wesche H, Henzel W J, Shillinglaw W, Li S, Cao Z. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 1997, 7:837-847.
86. Wiens M. Innate immune defense of the sponge Suberites domuncula against bacteria involves a MyD88-dependent signaling pathway. Induction of a perforin-like molecule. J. Biol. Chem. 2005, 280:27949-27959.
87. Wiens M. Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol. Biol. Evol. 2007, 24:792-804.
88. Williams E A, Degnan B M, Gunter H, Jackson D J, Woodcroft B J, Degnan S M. Widespread transcriptional changes pre-empt the critical pelagic-benthic transition in the vetigastropod Haliotis asinina. Mol. Ecol. 2009, 18:1006-1025.
89. Williams E A, Degnan S M. Carry-over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina. Mol. Ecol. 2009, 18:4434-4449.
90. Woods R G. Gene expression during early ascidian metamorphosis requires signalling by Hemps, an EGF-like protein. Development 2004, 131:2921-2933.
91. Wright S D, Ramos R A, Tobias P S, Ulevitch R J, Mathison J C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS-binding protein. Science 1990, 249:1431-1433.
92. Xiao H. Pellino 3b negatively regulates interleukin-1-induced TAK1-dependent NFκB activation. J. Biol. Chem. 2008, 283:14654-14664.
93. Yamada K. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 2003, 302:842-846.
94. Yu K Y, Kwon H-J, Norman D A M, Vig E, Goebl M G, Harrington M A. Cutting edge: mouse Pellino-2 modulates IL-1 and lipopolysaccharide signaling. J. Immunol. 2002, 169:4075-4078.
95. Zapata J M, Martínez-García V, Lefebvre S. Phylogeny of the TRAF/MATH domain. Adv. Exp. Med. Biol. 2007, 597:1-24.
96. Zhang G, Ghosh S. Negative regulation of Toll-like receptor-mediated signaling by Tollip. J. Biol. Chem. 2002, 277:7059-7065.
97. Zhang Y. Up-regulation of lysozyme gene expression during metamorphosis and immune challenge of the cotton bollworm, Helicoverpa armigera. Arch. Insect. Biochem. Physiol. 2009, 70:18-29.
98. Zipfel C. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 2008, 20:10-16.