Metazoans evolved by taking domains from soluble proteins to expand intercellular communication network

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Nam, Hyun Jun ^a   Kim, Inhae ^a   Bowie, James U ^b   Kim, Sanguk ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ANIMAL; CELL ADHESION; CELL COMMUNICATION; EVOLUTION; GENETICS; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL EVOLUTION; CELL ADHESION; CELL COMMUNICATION; MEMBRANE PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84928964293     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09576     Document Type: Article

References (57)

1. Eichinger, L. et al. The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57 (2005).
2. King, N., Hittinger, C. T. & Carroll, S. B. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301, 361-3 (2003).
3. Ruiz-Trillo, I. et al. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet 23, 113-8 (2007).
4. Escudero, L. M. et al. Epithelial organisation revealed by a network of cellular contacts. Nat Commun 2, 526 (2011).
5. Ekman, D., Bjorklund, A. K. & Elofsson, A. Quantification of the elevated rate of domain rearrangements in metazoa. J Mol Biol 372, 1337-48 (2007).
6. Copley, R. R., Schultz, J., Ponting, C. P. & Bork, P. Protein families in multicellular organisms. Curr Opin Struct Biol 9, 408-15 (1999).
7. King, N. et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-8 (2008).
8. Nam, H. J., Jeon, J. & Kim, S. Bioinformatic approaches for the structure and function of membrane proteins. BMB Rep 42, 697-704 (2009).
9. Elofsson, A. & von Heijne, G. Membrane protein structure: prediction versus reality. Annu Rev Biochem 76, 125-40 (2007).
10. Oberai, A., Ihm, Y., Kim, S. &Bowie, J. U. Alimited universe ofmembrane protein families and folds. Protein Sci 15, 1723-34 (2006).
11. Todd, A. E., Orengo, C. A. & Thornton, J. M. Evolution of function in protein superfamilies, from a structural perspective. J Mol Biol 307, 1113-43 (2001).
12. Vogel, C., Teichmann, S. A. & Pereira-Leal, J. The relationship between domain duplication and recombination. J Mol Biol 346, 355-65 (2005).
13. Liu, Y., Gerstein, M. & Engelman, D. M. Transmembrane protein domains rarely use covalent domain recombination as an evolutionary mechanism. Proc Natl Acad Sci U S A 101, 3495-7 (2004).
14. Nam, H. J., Han, S. K., Bowie, J. U. & Kim, S. Rampant exchange of the structure and function of extramembrane domains between membrane and water soluble proteins. PLoS Comput Biol 9, e1002997 (2013).
15. Biederer, T. Hooking up new synapses. Nat Neurosci 9, 1203-4 (2006).
16. Kim, S. et al. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9, 1294-301 (2006).
17. Shimaoka, M. et al. Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112, 99-111 (2003).
18. Zhang, H. et al. An unusual allosteric mobility of the C-terminal helix of a highaffinity alphaL integrin I domain variant bound to ICAM-5. Mol Cell 31, 432-7 (2008).
19. Stumpf, M. P. et al. Estimating the size of the human interactome. Proc Natl Acad Sci U S A 105, 6959-64 (2008).
20. Martin, S. et al. Construction of a large extracellular protein interaction network and its resolution by spatiotemporal expression profiling. Mol Cell Proteomics 9, 2654-65 (2010).
21. Kirouac, D. C. et al. Dynamic interaction networks in a hierarchically organized tissue. Mol Syst Biol 6, 417 (2010).
22. Wu, Y., Garmire, L. X. & Fan, R. Inter-cellular signaling network reveals a mechanistic transition in tumor microenvironment. Integr Biol (Camb) 4, 1478-86 (2012).
23. Goh, K. I., Kahng, B. & Kim, D. Universal behavior of load distribution in scalefree networks. Phys Rev Lett 87, 278701 (2001).
24. Wagner, A. & Fell, D. A. The small world inside large metabolic networks. Proc Biol Sci 268, 1803-10 (2001).
25. Jeong, H., Tombor, B., Albert, R., Oltvai, Z. N. & Barabasi, A. L. The large-scale organization of metabolic networks. Nature 407, 651-4 (2000).
26. Dunn, R., Dudbridge, F. & Sanderson, C. M. The use of edge-betweenness clustering to investigate biological function in protein interaction networks. BMC Bioinformatics 6, 39 (2005).
27. Ashburner, M. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25, 25-9 (2000).
28. Magrane, M. & Consortium, U. UniProt Knowledgebase: a hub of integrated protein data. Database (Oxford) 2011, bar009 (2011).
29. Gumbiner, B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-57 (1996).
30. Poliak, S. et al. Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K1channels. Neuron 24, 1037-47 (1999).
31. Li, X., Zhang, J., Cao, Z., Wu, J. & Shi, Y. Solution structure of GOPC PDZ domain and its interaction with the C-terminal motif of neuroligin. Protein Sci 15, 2149-58 (2006).
32. Barrett, J. C. & Shelby, M. D. Mechanisms of human carcinogens. Prog Clin Biol Res 374, 415-34 (1992).
33. Muller, W. E. & Muller, I. M. Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43, 281-92 (2003).
34. Sun, M. & Fink, P. J. A new class of reverse signaling costimulators belongs to the TNF family. J Immunol 179, 4307-12 (2007).
35. Cambi, A. & Figdor, C. Necrosis: C-type lectins sense cell death. Curr Biol 19, R375-8 (2009).
36. Shimizu, T., Mitsuke, H., Noto, K. & Arai, M. Internal gene duplication in the evolution of prokaryotic transmembrane proteins. J Mol Biol 339, 1-15 (2004).
37. Rapp, M., Granseth, E., Seppala, S. & von Heijne, G. Identification and evolution of dual-topology membrane proteins. Nat Struct Mol Biol 13, 112-6 (2006).
38. Bowie, J. U. Flip-flopping membrane proteins. Nat Struct Mol Biol 13, 94-6 (2006).
39. Hynes, R. O. The evolution of metazoan extracellular matrix. J Cell Biol 196, 671-9 (2012).
40. Murray, P. S. & Zaidel-Bar, R. Pre-metazoan origins and evolution of the cadherin adhesome. Biol Open 3, 1183-95 (2014).
41. Kobe, B. & Kajava, A. V. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11, 725-32 (2001).
42. Gay, N. J., Packman, L. C., Weldon, M. A. & Barna, J. C. A leucine-rich repeat peptide derived from the Drosophila Toll receptor forms extended filaments with a beta-sheet structure. FEBS Lett 291, 87-91 (1991).
43. Litman, G. W. & Cooper, M. D. Why study the evolution of immunity? Nat Immunol 8, 547-8 (2007).
44. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-87 (2002).
45. Springer, T. A. Complement and themultifaceted functions ofVWA and integrin I domains. Structure 14, 1611-6 (2006).
46. Gerhart, J. 1998 Warkany lecture: signaling pathways in development. Teratology 60, 226-39 (1999).
47. Sakarya, O. et al. A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2, e506 (2007).
48. Garcia, M. L. & Strehler, E. E. Plasma membrane calcium ATPases as critical regulators of calcium homeostasis during neuronal cell function. Front Biosci 4, D869-82 (1999).
49. Muller, D., Buchs, P. A., Stoppini, L. & Boddeke, H. Long-term potentiation, protein kinase C, and glutamate receptors. Mol Neurobiol 5, 277-88 (1991).
50. Ryan, T. J. & Grant, S. G. The origin and evolution of synapses. Nat Rev Neurosci 10, 701-12 (2009).
51. Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res 42, D222-30 (2014).
52. Moller, S., Croning, M. D. &Apweiler, R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17, 646-53 (2001).
53. Chen, C. P., Kernytsky, A. & Rost, B. Transmembrane helix predictions revisited. Protein Sci 11, 2774-91 (2002).
54. Cuthbertson, J. M., Doyle, D. A. & Sansom, M. S. Transmembrane helix prediction: a comparative evaluation and analysis. Protein Eng Des Sel 18, 295-308 (2005).
55. Eddy, S. R. Accelerated Profile HMM Searches. PLoS Comput Biol 7, e1002195 (2011).
56. Kim, J. et al. Rewiring of PDZ domain-ligand interaction network contributed to eukaryotic evolution. PLoS Genet 8, e1002510.
57. Bromberg, K. D., Ma'ayan, A., Neves, S. R. & Iyengar, R. Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth. Science 320, 903-9 (2008).