Dynamic evolution of toll-like receptor multigene families in echinoderms

Frontiers in Immunology

Volumn 3, Issue JUN, 2012, Pages

  Buckley, Katherine M ^a   Rast, Jonathan P ^a  

^a Sunnybrook Health Sciences Centre   (Canada)

Author keywords

Evolution; Innate immunity; Multigene family; Sea urchins; Toll like receptors

Indexed keywords

EID: 84874023911     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00136     Document Type: Article

References (49)

1. Alcaide, M., and Edwards, S. V. (2011). Molecular evolution of the toll-like receptor multigene family in birds. Mol. Biol. Evol. 28, 1703-1715.
2. Areal, H., Abrantes, J., and Esteves, P. J. (2011). Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evol. Biol. 11, 368. doi:10.1186/1471-2148-11-368
3. Bell, J. K., Mullen, G. E., Leifer, C. A., Mazzoni, A.,Davies,D. R., and Segal, D. M. (2003). Leucine-rich repeats and pathogen recognition in Tolllike receptors. Trends Immunol. 24, 528-533.
4. Biermann, C. H., Kessing, B. D., and Palumbi, S. R. (2003). Phylogeny and development of marine model species: strongylocentrotid sea urchins. Evol. Dev. 5, 360-371.
5. Bosch, T. C., Augustin, R., Anton-Erxleben, F., Fraune, S., Hemmrich, G., Zill, H., Rosenstiel, P., Jacobs, G., Schreiber, S., Leippe, M., Stanisak, M., Grotzinger, J., Jung, S., Podschun, R., Bartels, J., Harder, J., and Schroder, J. M. (2009). Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 33, 559-569.
6. Britten, R. J., Cetta, A., and Davidson, E. H. (1978). The single-copy DNA sequence polymorphism of the sea urchin Strongylocentrotus purpuratus. Cell 15, 1175-1186.
7. Cameron, R. A., Samanta, M., Yuan, A., He, D., and Davidson, E. (2009). SpBase: the sea urchin genome database and web site. Nucleic Acids Res. 37, D750-D754.
8. Davidson, C. R., Best, N. M., Francis, J. W., Cooper, E. L., and Wood, T. C. (2008). Toll-like receptor genes (TLRs) from Capitella capitata and Helobdella robusta (Annelida). Dev. Comp. Immunol. 32, 608-612.
9. Durbin, R., Eddy, S., Krogh, A., and Mitchison, G. (1998). Biological Sequence Analysis, Probability Models of Proteins and Nucleic Acids. Cambridge: Cambridge University Press.
10. Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.6. Seattle: University of Washington.
11. Gay, N. J., and Keith, F. J. (1991). Drosophila Toll and IL-1 receptor. Nature 351, 355-356.
12. Gross, P. S., Clow, L. A., and Smith, L. C. (2000). SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 51, 1034-1044.
13. Hall, T. A. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. (Oxf.) 41, 95-98.
14. Hibino, T., Loza-Coll, M., Messier, C., Majeske, A. J., Cohen, A. H., Terwilliger, D. P., Buckley, K. M., Brockton, V., Nair, S. V., Berney, K., Fugmann, S. D., Anderson, M. K., Pancer, Z., Cameron, R. A., Smith, L. C., and Rast, J. P. (2006). The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 300, 349-365.
15. Hinegardner, R. (1974). Cellular DNA content of the echinodermata. Comp. Biochem. Physiol. B 49, 219-226.
16. Holland, L. Z., Albalat, R., Azumi, K., Benito-Gutierrez, E., Blow, M. J., Bronner-Fraser, M.,Brunet, F.,Butts, T.,Candiani, S., Dishaw, L. J., Ferrier, D. E., Garcia-Fernandez, J., Gibson-Brown, J. J., Gissi, C., Godzik, A., Hallbook, F., Hirose, D., Hosomichi, K., Ikuta, T., Inoko, H., Kasahara, M., Kasamatsu, J., Kawashima, T., Kimura, A., Kobayashi, M., Kozmik, Z., Kubokawa, K., Laudet, V., Litman, G.W.,McHardy, A. C.,Meulemans, D., Nonaka, M., Olinski, R. P., Pancer, Z., Pennacchio, L. A., Pestarino, M., Rast, J. P., Rigoutsos, I., Robinson-Rechavi, M., Roch, G., Saiga, H., Sasakura, Y., Satake, M., Satou, Y., Schubert, M., Sherwood, N., Shiina, T., Takatori, N., Tello, J., Vopalensky, P., Wada, S., Xu, A., Ye, Y.,Yoshida, K.,Yoshizaki, F.,Yu, J. K., Zhang, Q., Zmasek, C. M., de Jong, P. J., Osoegawa, K., Putnam, N. H., Rokhsar, D. S., Satoh, N., and Holland, P. W. (2008). The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100-1111.
17. Huang, A. M., Rusch, J., and Levine, M. (1997). An anteroposterior dorsal gradient in the Drosophila embryo. Genes Dev. 11, 1963-1973.
18. Huang, S., Yuan, S., Guo, L., Yu, Y., Li, J., Wu, T., Liu, T., Yang, M., Wu, K., Liu, H., Ge, J., Yu, Y., Huang, H., Dong, M., Yu, C., Chen, S., and Xu, A. (2008). Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res. 18, 1112-1126.
19. Jin, M. S., and Lee, J. O. (2008). Structures of the toll-like receptor family and its ligand complexes. Immunity 29, 182-191.
20. Kang, J. Y., and Lee, J. O. (2011). Structural biology of the Toll-like receptor family. Annu. Rev. Biochem. 80, 917-941.
21. Kasamatsu, J., Oshiumi, H.,Matsumoto, M., Kasahara, M., and Seya, T. (2010). Phylogenetic and expression analysis of lamprey toll-like receptors. Dev. Comp. Immunol. 34, 855-865.
22. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
23. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R.,McGettigan, P. A., McWilliam, H.,Valentin, F.,Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
24. Lee, Y. H. (2003). Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Mol. Biol. Evol. 20, 1211-1221.
25. Lemaitre, B., and Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743.
26. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M., and Hoffmann, J. A. (1996). The dorsoventral regulatory gene cassette spatzle/ Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983.
27. Leulier, F., and Lemaitre, B. (2008). Tolllike receptors - taking an evolutionary approach. Nat. Rev. Genet. 9, 165-178.
28. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C. A. Jr. (1997). A humanhomologue of theDrosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397.
29. Messier-Solek, C., Buckley, K. M., and Rast, J. P. (2010). Highly diversified innate receptor systems and new forms of animal immunity. Semin. Immunol. 22, 39-47.
30. Miller, D. J., Hemmrich, G., Ball, E. E., Hayward, D. C., Khalturin, K., Funayama, N., Agata, K., and Bosch, T. C. (2007). The innate immune repertoire in cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8, R59.
31. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., andWold,B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628.
32. Narbonne-Reveau, K., Charroux, B., and Royet, J. (2011). Lack of an Antibacterial response defect in Drosophila Toll-9 mutant. PLoS ONE 6, 17470. doi:10.1371/journal. pone.0017470
33. Offord, V., Coffey, T. J., and Werling, D. (2010). LRRfinder: a web application for the identification of leucinerich repeats and an integrative Tolllike receptor database. Dev. Comp. Immunol. 34, 1035-1041.
34. O'Neill, L. A., and Bowie, A. G. (2007). The family of five: TIRdomain-containing adaptors in Tolllike receptor signalling. Nat. Rev. Immunol. 7, 353-364.
35. Ooi, J. Y., Yagi, Y., Hu, X., and Ip, Y. T. (2002). The Drosophila Toll-9 activates a constitutive antimicrobial defense. EMBO Rep. 3, 82-87.
36. Pespeni, M. H., Garfield, D. A., Manier, M. K., and Palumbi, S. R. (2011). Genome-wide polymorphisms show unexpected targets of natural selection. Proc. Biol. Sci. 279, 1412-1420.
37. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
38. Roach, J. C., Glusman, G., Rowen, L., Kaur, A., Purcell, M. K., Smith, K. D., Hood, L. E., and Aderem, A. (2005). The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. U.S.A. 102, 9577-9582.
39. Rock, F. L., Hardiman, G., Timans, J. C., Kastelein, R. A., and Bazan, J. F. (1998). A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. U.S.A. 95, 588-593.
40. Sackton, T. B., Lazzaro, B. P., Schlenke, T. A., Evans, J. D., Hultmark, D., and Clark, A. G. (2007). Dynamic evolution of the innate immune system in Drosophila. Nat. Genet. 39, 1461-1468.
41. Sasaki, N.,Ogasawara, M., Sekiguchi, T., Kusumoto, S., and Satake, H. (2009). Toll-like receptors of the ascidian, Ciona intestinalis: prototypes with hybrid functionalities of vertebrate Toll-like receptors. J. Biol. Chem. 284, 27336-27343.
42. Smith, A. B., Pisani, D., Mackenzie-Dodds, J. A., Stockley, B., Webster, B. L., and Littlewood, D. T. (2006). Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata).Mol. Biol. Evol. 23, 1832-1851.
43. Smith, L. C., Ghosh, J., Buckley, K. M., Clow, L. A., Dheilly, N. M., Haug, T., Henson, J. H., Li, C., Lun, C. M., Majeske, A. J., Matranga, V., Nair, S. V., Rast, J. P., Raftos, D. A., Roth, M., Sacchi, S., Schrankel, C. S., and Stensvag, K. (2011). Echinodermimmunity. Adv. Exp.Med. Biol. 708, 260-301.
44. Sodergren, E.,Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D., Coffman, J. A., Dean, M., Elphick, M. R., Ettensohn, C. A., Foltz, K. R., Hamdoun, A., Hynes, R. O., Klein, W. H., Marzluff, W., McClay, D. R.,Morris, R. L.,Mushegian, A., Rast, J. P., Smith, L. C., Thorndyke, M. C., Vacquier, V. D., Wessel, G. M., Wray, G., Zhang, L., Elsik, C. G., Ermolaeva, O., Hlavina, W., Hofmann, G., Kitts, P., Landrum, M. J., Mackey, A. J., Maglott, D., Panopoulou, G., Poustka, A. J., Pruitt, K., Sapojnikov, V., Song, X., Souvorov, A., Solovyev, V., Wei, Z., Whittaker, C. A.,Worley, K., Durbin, K. J., Shen, Y., Fedrigo, O., Garfield, D., Haygood, R., Primus, A., Satija, R., Severson, T., Gonzalez-Garay, M. L., Jackson, A. R., Milosavljevic, A., Tong, M., Killian, C. E., Livingston, B. T.,Wilt, F. H.,Adams, N., Belle, R., Carbonneau, S., Cheung, R., Cormier, P., Cosson, B., Croce, J., Fernandez-Guerra, A., Geneviere, A. M., Goel, M., Kelkar, H.,Morales, J., Mulner-Lorillon, O., Robertson, A. J., Goldstone, J. V., Cole, B., Epel, D., Gold, B., Hahn, M. E., Howard-Ashby, M., Scally, M., Stegeman, J. J., Allgood, E. L., Cool, J., Judkins, K. M.,McCafferty, S. S.,Musante, A. M., Obar, R. A., Rawson, A. P., Rossetti, B. J., Gibbons, I. R., Hoffman, M. P., Leone, A., Istrail, S., Materna, S. C., Samanta, M. P., Stolc,V., Tongprasit, W., Tu, Q., Bergeron, K. F., Brandhorst, B. P.,Whittle, J., Berney, K., Bottjer, D. J., Calestani, C., Peterson, K.,Chow, E.,Yuan, Q. A., Elhaik, E., Graur, D., Reese, J. T., Bosdet, I., Heesun, S., Marra, M. A., Schein, J., Anderson, M. K., Brockton, V., Buckley, K. M., Cohen, A. H., Fugmann, S. D., Hibino, T., Loza-Coll, M.,Majeske,A. J.,Messier, C.,Nair,S. V., Pancer, Z., Terwilliger,D. P.,Agca, C.,Arboleda, E., Chen, N., Churcher, A. M., Hallbook, F., Humphrey, G. W., Idris,M. M.,Kiyama,T., Liang, S., Mellott,D.,Mu, X.,Murray, G., Olinski, R. P., Raible, F., Rowe, M., Taylor, J. S., Tessmar-Raible, K., Wang, D., Wilson, K. H., Yaguchi, S., Gaasterland, T., Galindo, B. E., Gunaratne, H. J., Juliano, C.,Kinukawa, M.,Moy, G. W., Neill, A. T., Nomura, M., Raisch, M., Reade, A., Roux, M. M., Song, J. L., Su, Y. H., Townley, I. K., Voronina, E.,Wong, J. L., Amore, G., Branno, M., Brown, E. R., Cavalieri,V., Duboc, V., Duloquin, L., Flytzanis, C., Gache, C., Lapraz, F., Lepage, T.,Locascio, A.,Martinez,P.,Matassi, G.,Matranga,V., Range, R., Rizzo, F., Rottinger, E., Beane, W., Bradham, C., Byrum, C., Glenn, T.,Hussain, S., Manning, G., Miranda, E., Thomason, R., Walton, K., Wikramanayke, A., Wu, S. Y., Xu, R., Brown, C. T., Chen, L., Gray, R. F., Lee, P. Y., Nam, J., Oliveri, P., Smith, J., Muzny, D., Bell, S., Chacko, J.,Cree, A.,Curry, S., Davis, C., Dinh, H., Dugan-Rocha, S., Fowler, J., Gill, R., Hamilton, C., Hernandez, J., Hines, S., Hume, J., Jackson, L., Jolivet, A., Kovar, C., Lee, S., Lewis, L., Miner, G., Morgan, M., Nazareth, L. V., Okwuonu, G., Parker, D., Pu, L. L., Thorn, R., and Wright, R. (2006). The genome of the sea urchin Strongylocentrotus purpuratus. Science 314, 941-952.
45. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximumparsimony methods. Mol. Biol. Evol. 28, 2731-2739.
46. Tschirren, B., Raberg, L., and Westerdahl, H. (2011). Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents. J. Evol. Biol. 24, 1232-1240.
47. Wlasiuk, G., and Nachman, M. W. (2010).Adaptation and constraint at Toll-like receptors in primates. Mol. Biol. Evol. 27, 2172-2186.
48. Yang, Z. (1998). Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15, 568-573.
49. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.