The origin and evolution of synaptic proteins - Choanoflagellates lead the way

Journal of Experimental Biology

Volumn 218, Issue 4, 2015, Pages 506-514

  Burkhardt, Pawel ^a  

^a THE LABORATORY   (United Kingdom)

Author keywords

Homer; Metazoans; Munc18; Postsynaptic scaffold; SNARE; Synapse evolution

Indexed keywords

CHOANOFLAGELLIDA; METAZOA;

NERVE PROTEIN;

ANIMAL; CHOANOFLAGELLATE; EVOLUTION; GENETICS; GENOME; PHYSIOLOGY; SYNAPSE;

ANIMALS; BIOLOGICAL EVOLUTION; CHOANOFLAGELLATA; GENOME, PROTOZOAN; NERVE TISSUE PROTEINS; SYNAPSES;

EID: 84926392515     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.110247     Document Type: Review

References (78)

1. Abedin, M. and King, N. (2008). The Premetazoan Ancestry of Cadherins. Science 319, 946-948.
2. Alegado, R. A., Brown, L. W., Cao, S., Dermenjian, R. K., Zuzow, R., Fairclough, S. R., Clardy, J. and King, N. (2012). A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1, e00013.
3. Alié, A. and Manuel, M. (2010). The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol. Biol. 10, 34.
4. Babu, K., Cai, Y., Bahri, S., Yang, X. and Chia, W. (2004). Roles of Bifocal, Homer, and F-actin in anchoring Oskar to the posterior cortex of Drosophila oocytes. Genes Dev. 18, 138-143.
5. Bickel, P. E., Scherer, P. E., Schnitzer, J. E., Oh, P., Lisanti, M. P. and Lodish, H. F. (1997). Flotillin and epidermal surface antigen define a new family of caveolaeassociated integral membrane proteins. J. Biol. Chem. 272, 13793-13802.
6. Boxem, M., Maliga, Z., Klitgord, N., Li, N., Lemmens, I., Mana, M., de Lichtervelde, L., Mul, J. D., van de Peut, D., Devos, M. et al. (2008). A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134, 534-545.
7. Brakeman, P. R., Lanahan, A. A., O'Brien, R., Roche, K., Barnes, C. A., Huganir, R. L. and Worley, P. F. (1997). Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386, 284-288.
8. Burkhardt, P., Hattendorf, D. A., Weis, W. I. and Fasshauer, D. (2008). Munc18a controls SNARE assembly through its interaction with the syntaxin N-peptide. EMBO J. 27, 923-933.
9. Burkhardt, P., Stegmann, C. M., Cooper, B., Kloepper, T. H., Imig, C., Varoqueaux, F., Wahl, M. C. and Fasshauer, D. (2011). Primordial neurosecretory apparatus identified in the choanoflagellate Monosiga brevicollis. Proc. Natl. Acad. Sci. USA 108, 15264-15269.
10. Burkhardt, P., Grønborg, M., McDonald, K., Sulur, T., Wang, Q. and King, N. (2014). Evolutionary insights into premetazoan functions of the neuronal protein homer. Mol. Biol. Evol. 31, 2342-2355.
11. Cai, X. (2008). Unicellular Ca2+ signaling 'toolkit' at the origin of metazoa. Mol. Biol. Evol. 25, 1357-1361.
12. Carr, M., Leadbeater, B. S. C., Hassan, R., Nelson, M. and Baldauf, S. L. (2008). Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc. Natl. Acad. Sci. USA 105, 16641-16646.
13. Cheng, D., Hoogenraad, C. C., Rush, J., Ramm, E., Schlager, M. A., Duong, D. M., Xu, P., Wijayawardana, S. R., Hanfelt, J., Nakagawa, T. et al. (2006). Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 5, 1158-1170.
14. Chiarello, C., Bortoloso, E., Carpi, A., Furlan, S. and Volpe, P. (2013). Negative feedback regulation of Homer 1a on norepinephrine-dependent cardiac hypertrophy. Exp. Cell Res. 319, 1804-1814.
15. Dayel, M. J., Alegado, R. A., Fairclough, S. R., Levin, T. C., Nichols, S. A., McDonald, K. and King, N. (2011). Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev. Biol. 357, 73-82.
16. Dreger, M., Bengtsson, L., Schöneberg, T., Otto, H. and Hucho, F. (2001). Nuclear envelope proteomics: novel integral membrane proteins of the inner nuclear membrane. Proc. Natl. Acad. Sci. USA 98, 11943-11948.
17. Dulubova, I., Sugita, S., Hill, S., Hosaka, M., Fernandez, I., Südhof, T. C. and Rizo, J. (1999). A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18, 4372-4382.
18. Emes, R. D. and Grant, S. G. N. (2012). Evolution of synapse complexity and diversity. Annu. Rev. Neurosci. 35, 111-131.
19. Fairclough, S. R., Dayel, M. J. and King, N. (2010). Multicellular development in a choanoflagellate. Curr. Biol. 20, R875-R876.
20. Fairclough, S. R., Chen, Z., Kramer, E., Zeng, Q., Young, S., Robertson, H. M., Begovic, E., Richter, D. J., Russ, C., Westbrook, M. J. et al. (2013). Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 14, R15.
21. Folk, P., Půta, F. and Skruzný, M. (2004). Transcriptional coregulator SNW/SKIP: the concealed tie of dissimilar pathways. Cell. Mol. Life Sci. 61, 629-640.
22. Gerasimenko, O. and Gerasimenko, J. (2004). New aspects of nuclear calcium signalling. J. Cell Sci. 117, 3087-3094.
23. Gómez, V., Sesé, M., Santamaría, A., Martínez, J. D., Castellanos, E., Soler, M., Thomson, T. M. and Paciucci, R. (2010). Regulation of aurora B kinase by the lipid raft protein flotillin-1. J. Biol. Chem. 285, 20683-20690.
24. Guerrier, S., Coutinho-Budd, J., Sassa, T., Gresset, A., Jordan, N. V., Chen, K., Jin, W. L., Frost, A. and Polleux, F. (2009). The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138, 990-1004.
25. Gur Barzilai, M., Reitzel, A. M., Kraus, J. E. M., Gordon, D., Technau, U., Gurevitz, M. and Moran, Y. (2012). Convergent evolution of sodium ion selectivity in metazoan neuronal signaling. Cell Reports 2, 242-248.
26. Hayashi, M. K., Tang, C., Verpelli, C., Narayanan, R., Stearns, M. H., Xu, R.-M., Li, H., Sala, C. and Hayashi, Y. (2009). The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137, 159-171.
27. Hosono, R., Hekimi, S., Kamiya, Y., Sassa, T., Murakami, S., Nishiwaki, K., Miwa, J., Taketo, A., Kodaira, K. I. (1992). The unc-18 gene encodes a novel protein affecting the kinetics of acetylcholine metabolism in the nematode Caenorhabditis elegans. J. Neurochem. 58, 1517-1525.
28. Huang, G. N., Huso, D. L., Bouyain, S., Tu, J., McCorkell, K. A., May, M. J., Zhu, Y., Lutz, M., Collins, S., Dehoff, M. et al. (2008). NFAT binding and regulation of T cell activation by the cytoplasmic scaffolding Homer proteins. Science 319, 476-481.
29. Ishiguro, K. and Xavier, R. (2004). Homer-3 regulates activation of serum response element in T cells via its EVH1 domain. Blood 103, 2248-2256.
30. Jahn, R. and Fasshauer, D. (2012). Molecular machines governing exocytosis of synaptic vesicles. Nature 490, 201-207.
31. James-Clark, H. (1868). On the spongiae ciliatae as infusoria flagellata; or observations on the structure, animality, and relationship of Leucosolenia botryoides. Ann. Mag. Nat. His. 1, 133-142, 188-215, 250-264.
32. King, N., Hittinger, C. T. and Carroll, S. B. (2003). Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301, 361-363.
33. King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I. et al. (2008). The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788.
34. Kloepper, T. H., Kienle, C. N. and Fasshauer, D. (2008). SNAREing the basis of multicellularity: consequences of protein family expansion during evolution. Mol. Biol. Evol. 25, 2055-2068.
35. Laval, M. (1971). Ultrastructure and feeding mode of the choanoflagellate Salpinogoeca pelagica sp. nov. - comparison with sponge choanocytes (Translated from French). Protistologica 7, 325-336.
36. Leadbeater, B. S. C. and Thomsen, H. A. (2000). Order Choanoflagellida. In The Illustrated Guide to The Protozoa, Vol. 1, 2nd edn (ed. J. J. Lee, G. F. Leedale and P. Bradbury), pp 14-38. Lawrence, KS: Society of Protozoologists, .
37. Levin, T. C. and King, N. (2013). Evidence for sex and recombination in the choanoflagellate Salpingoeca rosetta. Curr. Biol. 23, 2176-2180.
38. Levin, T. C., Greaney, A. J., Wetzel, L. and King, N. (2014). The rosetteless gene controls development in the choanoflagellate S. rosetta. Elife 3, e04070.
39. Liebeskind, B. J., Hillis, D. M. and Zakon, H. H. (2011). Evolution of sodium channels predates the origin of nervous systems in animals. Proc. Natl. Acad. Sci. USA 108, 9154-9159.
40. Ma, C., Li, W., Xu, Y. and Rizo, J. (2011). Munc13 mediates the transition from the closed syntaxin-Munc18 complex to the SNARE complex. Nat. Struct. Mol. Biol. 18, 542-549.
41. Misura, K. M., Scheller, R. H. and Weis, W. I. (2000). Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404, 355-362.
42. Nichols, S. A., Dayel, M. J. and King, N. (2009). Genomic, phylogenetic and cell biological insights into metazoan origins. In Animal Evolution: Genomes, Fossils and Trees (ed. M. J. Telford and D. T. J. Littlewood), pp. 24-32. Oxford: Oxford University Press.
43. Nichols, S. A., Roberts, B. W., Richter, D. J., Fairclough, S. R. and King, N. (2012). Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β- catenin complex. Proc. Natl. Acad. Sci. USA 109, 13046-13051.
44. Nielsen, C. (2008). Six major steps in animal evolution: are we derived sponge larvae? Evol. Dev. 10, 241-257.
45. Pettitt, M. E., Orme, B. A. A., Blake, J. R. and Leadbeater, B. S. C. (2002). The hydrodynamics of filter feeding in choanoflagellates. Eur. J. Protistol. 38, 313-332.
46. Pevsner, J., Hsu, S. C., Braun, J. E., Calakos, N., Ting, A. E., Bennett, M. K. and Scheller, R. H. (1994). Specificity and regulation of a synaptic vesicle docking complex. Neuron 13, 353-361.
47. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E. et al. (2009). Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706-712.
48. Richter, D. J. and King, N. (2013). The genomic and cellular foundations of animal origins. Annu. Rev. Genet. 47, 509-537.
49. Rizo, J. and Rosenmund, C. (2008). Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674.
50. Roper, M., Dayel, M. J., Pepper, R. E. and Koehl, M. A. R. (2013). Cooperatively generated stresslet flows supply fresh fluid to multicellular choanoflagellate colonies. Phys. Rev. Lett. 110, 228104.
51. Ruiz-Trillo, I., Roger, A. J., Burger, G., Gray, M. W. and Lang, B. F. (2008). A phylogenomic investigation into the origin of metazoa. Mol. Biol. Evol. 25, 664-672.
52. Ryan, T. J. and Grant, S. G. N. (2009). The origin and evolution of synapses. Nat. Rev. Neurosci. 10, 701-712.
53. Sakarya, O., Armstrong, K. A., Adamska, M., Adamski, M., Wang, I. F., Tidor, B., Degnan, B. M., Oakley, T. H. and Kosik, K. S. (2007). A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2, e506.
54. Sala, C., Piëch, V., Wilson, N. R., Passafaro, M., Liu, G. and Sheng, M. (2001). Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31, 115-130.
55. Santamaría, A., Castellanos, E., Gómez, V., Benedit, P., Renau-Piqueras, J., Morote, J., Reventós, J., Thomson, T. M. and Paciucci, R. (2005). PTOV1 enables the nuclear translocation and mitogenic activity of flotillin-1, a major protein of lipid rafts. Mol. Cell. Biol. 25, 1900-1911.
56. Schulte, T., Paschke, K. A., Laessing, U., Lottspeich, F. and Stuermer, C. A. (1997). Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124, 577-587.
57. Schulze, K. L., Littleton, J. T., Salzberg, A., Halachmi, N., Stern, M., Lev, Z. and Bellen, H. J. (1994). rop, a Drosophila homolog of yeast Sec1 and vertebrate n- Sec1/Munc-18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron 13, 1099-1108.
58. Scott, B. L., Van Komen, J. S., Irshad, H., Liu, S., Wilson, K. A. and McNew, J. A. (2004). Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J. Cell Biol. 167, 75-85.
59. Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E. and Melia, T. J. (2007). Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183-195.
60. Shin, Y. K. (2013). Two gigs of Munc18 in membrane fusion. Proc. Natl. Acad. Sci. USA 110, 14116-14117.
61. Snell, E. A., Brooke, N. M., Taylor, W. R., Casane, D., Philippe, H. and Holland, P. W. H. (2006). An unusual choanoflagellate protein released by Hedgehog autocatalytic processing. Proc. Biol. Sci. 273, 401-407.
62. Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-6.
63. Stiber, J. A., Zhang, Z. S., Burch, J., Eu, J. P., Zhang, S., Truskey, G. A., Seth, M., Yamaguchi, N., Meissner, G., Shah, R. et al. (2008). Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol. Cell. Biol. 28, 2637-2647.
64. Stuermer, C. A. O. (2010). The reggie/flotillin connection to growth. Trends Cell Biol. 20, 6-13.
65. Südhof, T. C. and Rothman, J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
66. Suga, H., Chen, Z., de Mendoza, A., Sebé-Pedrós, A., Brown, M. W., Kramer, E., Carr, M., Kerner, P., Vervoort, M., Sánchez-Pons, N. et al. (2013). The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 4, 2325.
67. Tang, J., Maximov, A., Shin, O. H., Dai, H., Rizo, J. and Südhof, T. C. (2006). A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187.
68. Thomas, U. (2002). Modulation of synaptic signalling complexes by Homer proteins. J. Neurochem. 81, 407-413.
69. Togneri, J., Cheng, Y. S., Munson, M., Hughson, F. M. and Carr, C. M. (2006). Specific SNARE complex binding mode of the Sec1/Munc-18 protein, Sec1p. Proc. Natl. Acad. Sci. USA 103, 17730-17735.
70. Tu, J. C., Xiao, B., Yuan, J. P., Lanahan, A. A., Leoffert, K., Li, M., Linden, D. J. and Worley, P. F. (1998). Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21, 717-726.
71. Tu, J. C., Xiao, B., Naisbitt, S., Yuan, J. P., Petralia, R. S., Brakeman, P., Doan, A., Aakalu, V. K., Lanahan, A. A., Sheng, M. et al. (1999). Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23, 583-592.
72. Veit, M., Söllner, T. H. and Rothman, J. E. (1996). Multiple palmitoylation of synaptotagmin and the t-SNARE SNAP-25. FEBS Lett. 385, 119-123.
73. Verhage, M., Maia, A. S., Plomp, J. J., Brussaard, A. B., Heeroma, J. H., Vermeer, H., Toonen, R. F., Hammer, R. E., van den Berg, T. K., Missler, M. et al. (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869.
74. Volpe, P., Sandri, C., Bortoloso, E., Valle, G. and Nori, A. (2004). Topology of Homer 1c and Homer 1a in C2C12 myotubes and transgenic skeletal muscle fibers. Biochem. Biophys. Res. Commun. 316, 884-892.
75. Wellen, K. E., Hatzivassiliou, G., Sachdeva, U. M., Bui, T. V., Cross, J. R. and Thompson, C. B. (2009). ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324, 1076-1080.
76. Worley, P. F., Zeng, W., Huang, G., Kim, J. Y., Shin, D. M., Kim, M. S., Yuan, J. P., Kiselyov, K. and Muallem, S. (2007). Homer proteins in Ca2+ signaling by excitable and non-excitable cells. Cell Calcium 42, 363-371.
77. Xiao, B., Tu, J. C., Petralia, R. S., Yuan, J. P., Doan, A., Breder, C. D., Ruggiero, A., Lanahan, A. A., Wenthold, R. J. and Worley, P. F. (1998). Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707-716.
78. Yang, B., Steegmaier, M., Gonzalez, L. C., Jr and Scheller, R. H. (2000). nSec1 binds a closed conformation of syntaxin1A. J. Cell Biol. 148, 247-252.