Genomic survey of premetazoans shows deep conservation of cytoplasmic tyrosine kinases and multiple radiations of receptor tyrosine kinases

Science Signaling

Volumn 5, Issue 222, 2012, Pages

  Suga, Hiroshi ^a,b   Dacre, Michael ^c   De Mendoza, Alex ^a,b   Shalchian Tabrizi, Kamran ^d   Manning, Gerard ^c   Ruiz Trillo, Iñaki ^a,b,e  

^a INSTITUTE OF EVOLUTIONARY BIOLOGY CSIC UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d UNIVERSITY OF OSLO   (Norway)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE; TYROSINE KINASE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CHOANOFLAGELLATE; CONTROLLED STUDY; CYTOPLASM; GENE SEQUENCE; GENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; ENZYMOLOGY; EUKARYOTE; GENETICS; GENOME; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYSIOLOGY;

CAPSASPORA OWCZARZAKI; CHOANOFLAGELLIDA; METAZOA; MINISTERIA VIBRANS;

BASE SEQUENCE; CYTOPLASM; EUKARYOTA; EVOLUTION, MOLECULAR; GENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84860710663     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002733     Document Type: Article

References (56)

1. J. T. Bonner, The origins of multicellularity. Integr. Biol. 1, 27-36 (1998).
2. N. King, The unicellular ancestry of animal development. Dev. Cell 7, 313-325 (2004).
3. A. Rokas, The molecular origins of multicellular transitions. Curr. Opin. Genet. Dev. 18, 472-478 (2008).
4. K. Shalchian-Tabrizi, M. A. Minge,M. Espelund, R. Orr, T. Ruden, K. S. Jakobsen, T. Cavalier-Smith, Multigene phylogeny of choanozoa and the origin of animals. PLoS One 3, e2098 (2008).
5. I. Ruiz-Trillo, A. J. Roger, G. Burger, M. W. Gray, B. F. Lang, A phylogenomic investigation into the origin of metazoa. Mol. Biol. Evol. 25, 664-672 (2008).
6. A. Sebé-Pedrós, A. J. Roger, F. B. Lang, N. King, I. Ruiz-Trillo, Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl. Acad. Sci. U.S.A. 107, 10142-10147 (2010).
7. N. King, M. J. Westbrook, S. L. Young, A. Kuo, M. Abedin, J. Chapman, S. Fairclough, U. Hellsten, Y. Isogai, I. Letunic, M. Marr, D. Pincus, N. Putnam, A. Rokas, K. J. Wright, R. Zuzow, W. Dirks, M. Good, D. Goodstein, D. Lemons, W. Li, J. B. Lyons, A. Morris, S. Nichols, D. J. Richter, A. Salamov, J. Sequencing, P. Bork, W. A. Lim, G. Manning, W. T. Miller, W. McGinnis, H. Shapiro, R. Tjian, I. V. Grigoriev, D. Rokhsar, The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788 (2008).
8. A. Sebé-Pedrós, A. de Mendoza, B. F. Lang, B. M. Degnan, I. Ruiz-Trillo, Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 28, 1241-1254 (2011).
9. W. J. Fantl, D. E. Johnson, L. T. Williams, Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62, 453-481 (1993).
10. P. van der Geer, T. Hunter, R. A. Lindberg, Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 10, 251-337 (1994).
11. J. Gerhart, 1998 Warkany lecture: Signaling pathways in development. Teratology 60, 226-239 (1999).
12. H. Suga, K. Kuma, N. Iwabe, N. Nikoh, K. Ono, M. Koyanagi, D. Hoshiyama, T. Miyata, Intermittent divergence of the protein tyrosine kinase family during animal evolution. FEBS Lett. 412, 540-546 (1997).
13. G. Apic, J. Gough, S. A. Teichmann, Domain combinations in archaeal, eubacterial and eukaryotic proteomes. J. Mol. Biol. 310, 311-325 (2001).
14. E. V. Koonin, Y. I. Wolf, G. P. Karev, The structure of the protein universe and genome evolution. Nature 420, 218-223 (2002).
15. S. Wuchty, Scale-free behavior in protein domain networks. Mol. Biol. Evol. 18, 1694-1702 (2001).
16. T. Miyata, H. Suga, Divergence pattern of animal gene families and relationship with the Cambrian explosion. Bioessays 23, 1018-1027 (2001).
17. H. Suga, K. Katoh, T. Miyata, Sponge homologs of vertebrate protein tyrosine kinases and frequent domain shufflings in the early evolution of animals before the parazoan-eumetazoan split. Gene 280, 195-201 (2001).
18. H. Suga, M. Koyanagi, D. Hoshiyama, K. Ono, N. Iwabe, K. Kuma, T. Miyata, Extensive gene duplication in the early evolution of animals before the parazoan-eumetazoan split demonstrated by G proteins and protein tyrosine kinases from sponge and hydra. J. Mol. Evol. 48, 646-653 (1999).
19. H. Suga, G. Sasaki, K. Kuma, H. Nishiyori, N. Hirose, Z. H. Su, N. Iwabe, T. Miyata, Ancient divergence of animal protein tyrosine kinase genes demonstrated by a gene family tree including choanoflagellate genes. FEBS Lett. 582, 815-818 (2008).
20. S. K. Hanks, A. M. Quinn, T. Hunter, The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains. Science 241, 42-52 (1988).
21. S. K. Hanks, T. Hunter, The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596 (1995).
22. G. Manning, G. D. Plowman, T. Hunter, S. Sudarsanam, Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 27, 514-520 (2002).
23. R. A. Lindberg, A. M. Quinn, T. Hunter, Dual-specificity protein kinases: Will any hydroxyl do? Trends Biochem. Sci. 17, 114-119 (1992).
24. G. Manning, S. L. Young, W. T. Miller, Y. Zhai, The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc. Natl. Acad. Sci. U.S.A. 105, 9674-9679 (2008).
25. M. Srivastava, O. Simakov, J. Chapman, B. Fahey, M. E. Gauthier, T. Mitros, G. S. Richards, C. Conaco, M. Dacre, U. Hellsten, C. Larroux, N. H. Putnam, M. Stanke, M. Adamska, A. Darling, S. M. Degnan, T. H. Oakley, D. C. Plachetzki, Y. Zhai, M. Adamski, A. Calcino, S. F. Cummins, D. M. Goodstein, C. Harris, D. J. Jackson, S. P. Leys, S. Shu, B. J. Woodcroft, M. Vervoort, K. S. Kosik, G. Manning, B. M. Degnan, D. S. Rokhsar, The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-726 (2010).
26. N. King, S. B. Carroll, A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution. Proc. Natl. Acad. Sci. U.S.A. 98, 15032-15037 (2001).
27. Y. Segawa, H. Suga, N. Iwabe, C. Oneyama, T. Akagi, T. Miyata, M. Okada, Functional development of Src tyrosine kinases during evolution from a unicellular ancestor to multicellular animals. Proc. Natl. Acad. Sci. U.S.A. 103, 12021-12026 (2006).
28. W. Li, S. L. Young, N. King, W. T. Miller, Signaling properties of a non-metazoan Src kinase and the evolutionary history of Src negative regulation. J. Biol. Chem. 283, 15491-15501 (2008).
29. J. L. Tan, J. A. Spudich, Developmentally regulated protein-tyrosine kinase genes in Dictyostelium discoideum. Mol. Cell. Biol. 10, 3578-3583 (1990).
30. S. H. Shiu, W. H. Li, Origins, lineage-specific expansions, and multiple losses of tyrosine kinases in eukaryotes. Mol. Biol. Evol. 21, 828-840 (2004).
31. L. A. Hertel, C. J. Bayne, E. S. Loker, The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. Int. J. Parasitol. 32, 1183-1191 (2002).
32. J. Paps, I. Ruiz-Trillo, Animals and their unicellular ancestors, in Encyclopedia of Life Sciences (John Wiley and Sons, Chichester, UK, 2010), pp. 1-8.
33. T. Cavalier-Smith, E. E. Chao, Phylogeny and evolution of Apusomonadida (Protozoa: Apusozoa): New genera and species. Protist 161, 549-576 (2010).
34. G. Torruella, R. Derelle, J. Paps, B. F. Lang, A. J. Roger, K. Shalchian-Tabrizi, I. Ruiz-Trillo, Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains. Mol. Biol. Evol. 29, 531-544 (2012).
35. T. Y. James, P. M. Letcher, J. E. Longcore, S. E. Mozley-Standridge, D. Porter,M. J. Powell, G. W. Griffith, R. Vilgalys, A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98, 860-871 (2006).
36. I. Ruiz-Trillo, G. Burger, P. W. Holland, N. King, B. F. Lang, A. J. Roger, M. W. Gray, The origins of multicellularity: A multi-taxon genome initiative. Trends Genet. 23, 113-118 (2007).
37. H. Kishino, M. Hasegawa, Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29, 170-179 (1989).
38. M. Carr, B. S. Leadbeater, R. Hassan, M. Nelson, S. L. Baldauf, Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc. Natl. Acad. Sci. U.S.A. 105, 16641-16646 (2008).
39. P. R. Bergquist, in Invertebrate Zoology, D. T. Anderson, Ed. (Oxford Univ. Press, Victoria, 2001), pp. 10-27.
40. L. Margulis, K. V. Schwartz, Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth (W. H. Freeman and Company, New York, 1998), pp. 246-249.
41. N. K. Tonks, Protein tyrosine phosphatases: From genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7, 833-846 (2006).
42. H. Suga, D. Hoshiyama, S. Kuraku, K. Katoh, K. Kubokawa, T. Miyata, Protein tyrosine kinase cDNAs from amphioxus, hagfish, and lamprey: Isoform duplications around the divergence of cyclostomes and gnathostomes. J. Mol. Evol. 49, 601-608 (1999).
43. P. Dehal, J. L. Boore, Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005).
44. N. King, C. T. Hittinger, S. B. Carroll, Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301, 361-363 (2003).
45. T. L. Simpson, The Cell Biology of Sponges (Springer-Verlag, New York, 1984), pp. 255-340.
46. T. Mustelin, P. Burn, Regulation of src family tyrosine kinases in lymphocytes. Trends Biochem. Sci. 18, 215-220 (1993).
47. J. Sambrook, D. W. Russell, Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, New York, 2001).
48. S. R. Eddy, A new generation of homology search tools based on probabilistic inference. Genome Inform. 23, 205-211 (2009).
49. C. Burge, S. Karlin, Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94 (1997).
50. M. Stanke, S. Waack, Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 (suppl. 2), ii215-ii225 (2003).
51. J. D. Bendtsen, H. Nielsen, G. von Heijne, S. Brunak, Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (2004).
52. A. Stamatakis, RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).
53. K. Katoh, K. Kuma, T. Miyata, Genetic algorithm-based maximum-likelihood analysis for molecular phylogeny. J. Mol. Evol. 53, 477-484 (2001).
54. F. Ronquist, J. P. Huelsenbeck, MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003).
55. A. J. Roger, A. G. Simpson, Evolution: Revisiting the root of the eukaryote tree. Curr. Biol. 19, R165-R167 (2009).
56. T. Hunter, Protein kinase classification. Methods Enzymol. 200, 3-37 (1991).