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Ancient origin of the integrin-mediated adhesion and signaling machinery

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Sebé-Pedrós, Arnau, Roger, Andrew J., Lang, Franz B., King, Nicole, Ruiz-Trillo, Iñaki·2010·Proceedings of the National Academy of Sciences

Abstract

The evolution of animals (metazoans) from their unicellular ancestors required the emergence of novel mechanisms for cell adhesion and cell–cell communication. One of the most important cell adhesion mechanisms for metazoan development is integrin-mediated adhesion and signaling. The integrin adhesion complex mediates critical interactions between cells and the extracellular matrix, modulating several aspects of cell physiology. To date this machinery has been considered strictly metazoan specific. Here we report the results of a comparative genomic analysis of the integrin adhesion machinery, using genomic data from several unicellular relatives of Metazoa and Fungi. Unexpectedly, we found that core components of the integrin adhesion complex are encoded in the genome of the apusozoan protist Amastigomonas sp., and therefore their origins predate the divergence of Opisthokonta, the clade that includes metazoans and fungi. Furthermore, our analyses suggest that key components of this apparatus have been lost independently in fungi and choanoflagellates. Our data highlight the fact that many of the key genes that had formerly been cited as crucial for metazoan origins have a much earlier origin. This underscores the importance of gene cooption in the unicellular-to-multicellular transition that led to the emergence of the Metazoa.

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Show all 7 references

Research works printed but not linked: 58

  1. N King, The unicellular ancestry of animal development. Dev Cell 7, 313–325 (2004). · DOI · Paper page
  2. A Rokas, The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42, 235–251 (2008). · DOI · Paper page
  3. M Srivastava, et al., The Trichoplax genome and the nature of placozoans. Nature 454, 955–960 (2008). · DOI · Paper page
  4. SA Nichols, W Dirks, JS Pearse, N King, Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103, 12451–12456 (2006). · DOI · Paper page
  5. C Larroux, et al., Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25, 980–996 (2008). · DOI · Paper page
  6. ET Steenkamp, J Wright, SL Baldauf, The protistan origins of animals and fungi. Mol Biol Evol 23, 93–106 (2006). · DOI · Paper page
  7. I Ruiz-Trillo, AJ Roger, G Burger, MW Gray, BF Lang, A phylogenomic investigation into the origin of metazoa. Mol Biol Evol 25, 664–672 (2008). · DOI · Paper page
  8. I Ruiz-Trillo, CE Lane, JM Archibald, AJ Roger, Insights into the evolutionary origin and genome architecture of the unicellular opisthokonts Capsaspora owczarzaki and Sphaeroforma arctica. J Eukaryot Microbiol 53, 1–6 (2006). · DOI
  9. M Carr, BS Leadbeater, R Hassan, M Nelson, SL Baldauf, Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc Natl Acad Sci USA 105, 16641–16646 (2008). · DOI · Paper page
  10. M Abedin, N King, The premetazoan ancestry of cadherins. Science 319, 946–948 (2008). · DOI
  11. K Shalchian-Tabrizi, et al., Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE 3, e2098 (2008). · DOI · Paper page
  12. RO Hynes, Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11–25 (1992). · DOI · Paper page
  13. DS Harburger, DA Calderwood, Integrin signalling at a glance. J Cell Sci 122, 159–163 (2009). · DOI · Paper page
  14. TE O'Toole, et al., Integrin cytoplasmic domains mediate inside-out signal transduction. J Cell Biol 124, 1047–1059 (1994). · DOI · Paper page
  15. S Dedhar, GE Hannigan, Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr Opin Cell Biol 8, 657–669 (1996). · DOI · Paper page
  16. CA Whittaker, RO Hynes, Distribution and evolution of von Willebrand/integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13, 3369–3387 (2002). · DOI · Paper page
  17. SE LaFlamme, KL Auer, Integrin signaling. Semin Cancer Biol 7, 111–118 (1996). · DOI
  18. B Sjöblom, A Salmazo, K Djinović-Carugo, Alpha-actinin structure and regulation. Cell Mol Life Sci 65, 2688–2701 (2008). · DOI · Paper page
  19. KL Wegener, et al., Structural basis of integrin activation by talin. Cell 128, 171–182 (2007). · DOI · Paper page
  20. DR Critchley, Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu Rev Biophys 38, 235–254 (2009). · DOI · Paper page
  21. WH Ziegler, RC Liddington, DR Critchley, The structure and regulation of vinculin. Trends Cell Biol 16, 453–460 (2006). · DOI · Paper page
  22. NO Deakin, CE Turner, Paxillin comes of age. J Cell Sci 121, 2435–2444 (2008). · DOI · Paper page
  23. KR Legate, E Montañez, O Kudlacek, R Fässler, ILK, PINCH and parvin: The tIPP of integrin signalling. Nat Rev Mol Cell Biol 7, 20–31 (2006). · DOI · Paper page
  24. SN Nikolopoulos, CE Turner, Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J Biol Chem 276, 23499–23505 (2001). · DOI · Paper page
  25. EG Arias-Salgado, et al., Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc Natl Acad Sci USA 100, 13298–13302 (2003). · DOI · Paper page
  26. JT Parsons, KH Martin, JK Slack, JM Taylor, SA Weed, Focal adhesion kinase: A regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606–5613 (2000). · DOI · Paper page
  27. R Zaidel-Bar, Evolution of complexity in the integrin adhesome. J Cell Biol 186, 317–321 (2009). · DOI
  28. I Ruiz-Trillo, et al., The origins of multicellularity: A multi-taxon genome initiative. Trends Genet 23, 113–118 (2007). · DOI
  29. MS Johnson, N Lu, K Denessiouk, J Heino, D Gullberg, Integrins during evolution: Evolutionary trees and model organisms. Biochim Biophys Acta 1788, 779–789 (2009). · DOI
  30. D Valdramidou, MJ Humphries, AP Mould, Distinct roles of beta1 metal ion-dependent adhesion site (MIDAS), adjacent to MIDAS (ADMIDAS), and ligand-associated metal-binding site (LIMBS) cation-binding sites in ligand recognition by integrin alpha2beta1. J Biol Chem 283, 32704–32714 (2008). · DOI
  31. JP Xiong, et al., Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science 294, 339–345 (2001). · DOI · Paper page
  32. DL Brower, SM Brower, DC Hayward, EE Ball, Molecular evolution of integrins: Genes encoding integrin beta subunits from a coral and a sponge. Proc Natl Acad Sci USA 94, 9182–9187 (1997). · DOI
  33. PD Tahiliani, L Singh, KL Auer, SE LaFlamme, The role of conserved amino acid motifs within the integrin beta3 cytoplasmic domain in triggering focal adhesion kinase phosphorylation. J Biol Chem 272, 7892–7898 (1997). · DOI
  34. BA Knack, et al., Unexpected diversity of cnidarian integrins: Expression during coral gastrulation. BMC Evol Biol 8, 136 (2008). · DOI
  35. MW Brown, FW Spiegel, JD Silberman, Phylogeny of the “forgotten” cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol 26, 2699–2709 (2009). · DOI
  36. E Kim, AG Simpson, LE Graham, Evolutionary relationships of apusomonads inferred from taxon-rich analyses of 6 nuclear encoded genes. Mol Biol Evol 23, 2455–2466 (2006). · DOI
  37. T Cavalier-Smith, EE Chao, Phylogeny of choanozoa, apusozoa, and other protozoa and early eukaryote megaevolution. J Mol Evol 56, 540–563 (2003). · DOI
  38. I Ruiz-Trillo, Y Inagaki, LA Davis, S Sperstad, B Landfald, AJ Roger, Capsaspora owczarzaki is an independent opisthokont lineage. Curr Biol 14, R946–947 (2004). · DOI
  39. W Li, SL Young, N King, WT Miller, Signaling properties of a non-metazoan Src kinase and the evolutionary history of Src negative regulation. J Biol Chem 283, 15491–15501 (2008). · DOI
  40. S Cornillon, et al., An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features. EMBO Rep 7, 617–621 (2006). · DOI
  41. E Simionato, et al., Origin and diversification of the basic helix-loop-helix gene family in metazoans: Insights from comparative genomics. BMC Evol Biol 7, 33 (2007). · DOI · Paper page
  42. M Gauthier, BM Degnan, The transcription factor NF-kappaB in the demosponge Amphimedon queenslandica: Insights on the evolutionary origin of the Rel homology domain. Dev Genes Evol 218, 23–32 (2008). · DOI
  43. A Yamada, K Pang, MQ Martindale, S Tochinai, Surprisingly complex T-box gene complement in diploblastic metazoans. Evol Dev 9, 220–230 (2007). · DOI
  44. D Pincus, I Letunic, P Bork, WA Lim, Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc Natl Acad Sci USA 105, 9680–9684 (2008). · DOI
  45. G Manning, SL Young, WT 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 USA 105, 9674–9679 (2008). · DOI
  46. BM Degnan, M Vervoort, C Larroux, GS Richards, Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19, 591–599 (2009). · DOI
  47. A de Mendoza, H Suga, I Ruiz-Trillo, Evolution of the MAGUK protein gene family in premetazoan lineages. BMC Evol Biol 10, 93 (2010). · DOI
  48. O Johnsborg, V Eldholm, LS Håvarstein, Natural genetic transformation: Prevalence, mechanisms and function. Res Microbiol 158, 767–778 (2007). · DOI · Paper page
  49. BE Layton, et al., Collagen's triglycine repeat number and phylogeny suggest an interdomain transfer event from a Devonian or Silurian organism into Trichodesmium erythraeum. J Mol Evol 66, 539–554 (2008). · DOI
  50. RF Yeh, LP Lim, CB Burge, Computational inference of homologous gene structures in the human genome. Genome Res 11, 803–816 (2001). · DOI · Paper page
  51. M Stanke, et al., AUGUSTUS: Ab initio prediction of alternative transcripts. Nucleic Acids Res 34, W435–W439 (2006). · DOI · Paper page
  52. G Moreno-Hagelsieb, K Latimer, Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 24, 319–324 (2008). · DOI · Paper page
  53. SR Eddy, Profile hidden Markov models. Bioinformatics 14, 755–763 (1998). · DOI · Paper page
  54. JD Bendtsen, H Nielsen, G von Heijne, S Brunak, Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783–795 (2004). · DOI · Paper page
  55. RC Edgar, MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004). · DOI · Paper page
  56. F Ronquist, JP Huelsenbeck, MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003). · DOI · Paper page
  57. MA Minge, et al., Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proc Biol Sci 276, 597–604 (2008).
  58. Y Liu, et al., Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol Biol 9, 272 (2009). · DOI

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Metadata

Authors
Sebé-Pedrós, A., Roger, A. J., Lang, F. B., King, N., & Ruiz-Trillo, I.
Venue
Proceedings of the National Academy of Sciences
Published
2010-05-17
Volume
107
Issue
22
Pages
10142-10147
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2152824691
Cited by
254
References
7
FWCI
13.77
Type
journal article
Language
en
Open access
bronze

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Sebé-Pedrós, A., Roger, A. J., Lang, F. B., King, N., & Ruiz-Trillo, I. (2010). Ancient origin of the integrin-mediated adhesion and signaling machinery. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1002257107

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