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BioMed Research International
Volume 2016 (2016), Article ID 2456062, 12 pages
http://dx.doi.org/10.1155/2016/2456062
Research Article

Neurotrophin, p75, and Trk Signaling Module in the Developing Nervous System of the Marine Annelid Platynereis dumerilii

1Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany
2Institute for Biological and Medical Imaging and Institute of Developmental Genetics, Helmholtz Zentrum München, Ingolstädter Landstraße 1, 85764 München, Germany

Received 11 September 2015; Revised 30 November 2015; Accepted 1 December 2015

Academic Editor: Sidi Chen

Copyright © 2016 Antonella Lauri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Bibel and Y.-A. Barde, “Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system,” Genes and Development, vol. 14, no. 23, pp. 2919–2937, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. E. J. Huang and L. F. Reichardt, “Neurotrophins: roles in neuronal development and function,” Annual Review of Neuroscience, vol. 24, pp. 677–736, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. E. J. Huang and L. F. Reichardt, “Trk receptors: roles in neuronal signal transduction,” Annual Review of Biochemistry, vol. 72, pp. 609–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Cohen, R. Levi-Montalcini, and V. Hamburger, “A nerve growth-stimulating factor isolated from sarcomas 37 and 180,” Proceedings of the National Academy of Sciences of the United States of America, vol. 40, no. 10, pp. 1014–1018, 1954. View at Publisher · View at Google Scholar
  5. R. Levi-Montalcini, “Tissue and nerve growth promoting factors,” Proceedings of the Royal Society of Medicine, vol. 58, no. 5, pp. 357–360, 1965. View at Google Scholar
  6. L. Minichiello, M. Korte, D. Wolfer et al., “Essential role for TrkB receptors in hippocampus-mediated learning,” Neuron, vol. 24, no. 2, pp. 401–414, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Minichiello, A. M. Calella, D. L. Medina, T. Bonhoeffer, R. Klein, and M. Korte, “Mechanism of TrkB-mediated hippocampal long-term potentiation,” Neuron, vol. 36, no. 1, pp. 121–137, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. R. E. van Kesteren, M. Fainzilber, G. Hauser et al., “Early evolutionary origin of the neurotrophin receptor family,” The EMBO Journal, vol. 17, no. 9, pp. 2534–2542, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Beck, D. W. Munno, Z. Levy et al., “Neurotrophic activities of trk receptors conserved over 600 million years of evolution,” Journal of Neurobiology, vol. 60, no. 1, pp. 12–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. È. Benito-Gutiérrez, C. Nake, M. Llovera, J. X. Comella, and J. Garcia-Fernàndez, “The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells,” Development, vol. 132, no. 9, pp. 2191–2202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. B. Zhu, J. A. Pennack, P. McQuilton et al., “Drosophila neurotrophins reveal a common mechanism for nervous system formation,” PLoS Biology, vol. 6, no. 11, article e284, 2008. View at Publisher · View at Google Scholar
  12. K. H. Wilson, “The genome sequence of the protostome Daphnia pulex encodes respective orthologues of a neurotrophin, a Trk and a p75NTR: evolution of neurotrophin signaling components and related proteins in the bilateria,” BMC Evolutionary Biology, vol. 9, article 243, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. S. R. Kassabov, Y.-B. Choi, K. A. Karl, H. D. Vishwasrao, C. H. Bailey, and E. R. Kandel, “A single Aplysia neurotrophin mediates synaptic facilitation via differentially processed isoforms,” Cell Reports, vol. 3, no. 4, pp. 1213–1227, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. F. C. Bronfman and M. Fainzilber, “Multi-tasking by the p75 neurotrophin receptor: sortilin things out?” EMBO Reports, vol. 5, no. 9, pp. 867–871, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. G. Arnett, J. M. Ryals, and D. E. Wright, “pro-NGF, sortilin, and p75NTR: potential mediators of injury-induced apoptosis in the mouse dorsal root ganglion,” Brain Research, vol. 1183, no. 1, pp. 32–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Volosin, C. Trotter, A. Cragnolini et al., “Induction of proneurotrophins and activation of p75NTR-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures,” The Journal of Neuroscience, vol. 28, no. 39, pp. 9870–9879, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Hallböök, L.-G. Lundin, and K. Kullander, “Lampetra fluviatilis neurotrophin homolog, descendant of a neurotrophin ancestor, discloses the early molecular evolution of neurotrophins in the vertebrate subphylum,” The Journal of Neuroscience, vol. 18, no. 21, pp. 8700–8711, 1998. View at Google Scholar · View at Scopus
  18. F. Lapraz, E. Röttinger, V. Duboc et al., “RTK and TGF-β signaling pathways genes in the sea urchin genome,” Developmental Biology, vol. 300, no. 1, pp. 132–152, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Bothwell, “Evolution of the neurotrophin signaling system in invertebrates,” Brain, Behavior and Evolution, vol. 68, no. 3, pp. 124–132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. T. H. Struck, C. Paul, N. Hill et al., “Phylogenomic analyses unravel annelid evolution,” Nature, vol. 471, no. 7336, pp. 95–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Arendt, K. Tessmar-Raible, H. Snyman, A. W. Dorresteijn, and J. Wittbrodf, “Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain,” Science, vol. 306, no. 5697, pp. 869–871, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Lauri, T. Brunet, M. Handberg-Thorsager et al., “Development of the Annelid Axochord: insights into notochord evolution,” Science, vol. 345, no. 6202, pp. 1365–1368, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Wlesmann, M. H. Ultsch, S. H. Bass, and A. M. de Vos, “Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor,” Nature, vol. 401, no. 6749, pp. 184–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Gong, P. Cao, H.-J. Yu, and T. Jiang, “Crystal structure of the neurotrophin-3 and p75NTR symmetrical complex,” Nature, vol. 454, no. 7205, pp. 789–793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. E. C. Seaver, K. Thamm, and S. D. Hill, “Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages,” Evolution and Development, vol. 7, no. 4, pp. 312–326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Nordberg, M. Cantor, S. Dusheyko et al., “The genome portal of the Department of Energy Joint Genome Institute: 2014 updates,” Nucleic Acids Research, vol. 42, no. 1, pp. D26–D31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. C. J. A. Sigrist, L. Cerutti, E. de Castro et al., “PROSITE, a protein domain database for functional characterization and annotation,” Nucleic Acids Research, vol. 38, no. 1, Article ID gkp885, pp. D161–D166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. T. N. Petersen, S. Brunak, G. von Heijne, and H. Nielsen, “SignalP 4.0: discriminating signal peptides from transmembrane regions,” Nature Methods, vol. 8, no. 10, pp. 785–786, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Duckert, S. Brunak, and N. Blom, “Prediction of proprotein convertase cleavage sites,” Protein Engineering, Design and Selection, vol. 17, no. 1, pp. 107–112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Nielsen, C. Lundegaard, O. Lund, and T. N. Petersen, “CPHmodels-3.0-remote homology modeling using structure-guided sequence profiles,” Nucleic Acids Research, vol. 38, supplement 2, Article ID gkq535, pp. W576–W581, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Fernandez-Fuentes, C. J. Madrid-Aliste, B. K. Rai, J. E. Fajardo, and A. Fiser, “M4T: a comparative protein structure modeling server,” Nucleic Acids Research, vol. 35, no. 2, pp. W363–W368, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. E. F. Pettersen, T. D. Goddard, C. C. Huang et al., “UCSF Chimera—a visualization system for exploratory research and analysis,” Journal of Computational Chemistry, vol. 25, no. 13, pp. 1605–1612, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. UniProt Consortium, “UniProt: a hub for protein information,” Nucleic Acids Research, vol. 43, pp. D204–D212, 2015. View at Publisher · View at Google Scholar
  34. J. McEntyre and J. Ostell, The NCBI Handbook, National Center for Biotechnology Information, Bethesda, Md, USA, 2002.
  35. R. C. Edgar, “MUSCLE: multiple sequence alignment with high accuracy and high throughput,” Nucleic Acids Research, vol. 32, no. 5, pp. 1792–1797, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Kearse, R. Moir, A. Wilson et al., “Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data,” Bioinformatics, vol. 28, no. 12, Article ID bts199, pp. 1647–1649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Guindon, F. Lethiec, P. Duroux, and O. Gascuel, “PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference,” Nucleic Acids Research, vol. 33, no. 2, pp. W557–W559, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Tessmar-Raible, P. R. H. Steinmetz, H. Snyman, M. Hassel, and D. Arendt, “Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development,” BioTechniques, vol. 39, no. 4, pp. 460–462, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Schindelin, I. Arganda-Carreras, E. Frise et al., “Fiji: an open-source platform for biological-image analysis,” Nature Methods, vol. 9, no. 7, pp. 676–682, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. R. H. Lipsky and A. M. Marini, “Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity,” Annals of the New York Academy of Sciences, vol. 1122, pp. 130–143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Minichiello, “TrkB signalling pathways in LTP and learning,” Nature Reviews Neuroscience, vol. 10, no. 12, pp. 850–860, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Urfer, P. Tsoulfas, L. O'Connell, D. L. Shelton, L. F. Parada, and L. G. Presta, “An immunoglobulin-like domain determines the specificity of neurotrophin receptors,” The EMBO Journal, vol. 14, no. 12, pp. 2795–2805, 1995. View at Google Scholar · View at Scopus
  43. È. Benito-Gutiérrez, J. Garcia-Fernàndez, and J. X. Comella, “Origin and evolution of the Trk family of neurotrophic receptors,” Molecular and Cellular Neuroscience, vol. 31, no. 2, pp. 179–192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Kanda, T. Igaki, H. Kanuka, T. Yagi, and M. Miura, “Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling,” The Journal of Biological Chemistry, vol. 277, no. 32, pp. 28372–28375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. W. S. Sossin, “Tracing the evolution and function of the Trk superfamily of receptor tyrosine kinases,” Brain, Behavior and Evolution, vol. 68, no. 3, pp. 145–156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. P. D. Sun and D. R. Davies, “The cystine-knot growth-factor superfamily,” Annual Review of Biophysics and Biomolecular Structure, vol. 24, no. 1, pp. 269–291, 1995. View at Publisher · View at Google Scholar
  47. U. A. Vitt, S. Y. Hsu, and A. J. W. Hsueh, “Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules,” Molecular Endocrinology, vol. 15, no. 5, pp. 681–694, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Murray-Rust, N. Q. McDonald, T. L. Blundell et al., “Topological similarities in TGF-β 2, PDGF-BB and NGF define a superfamily of polypeptide growth factors,” Structure, vol. 1, no. 2, pp. 153–159, 1993. View at Google Scholar
  49. M. J. Butte, “Neurotrophic factor structures reveal clues to evolution, binding, specificity, and receptor activation,” Cellular and Molecular Life Sciences, vol. 58, no. 8, pp. 1003–1013, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. J. T. Bridgham, J. A. Wilder, H. Hollocher, and A. L. Johnson, “All in the family: evolutionary and functional relationships among death receptors,” Cell Death and Differentiation, vol. 10, no. 1, pp. 19–25, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. N. H. Putnam, M. Srivastava, U. Hellsten et al., “Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization,” Science, vol. 317, no. 5834, pp. 86–94, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Hallböök, “Evolution of the vertebrate neurotrophin and Trk receptor gene families,” Current Opinion in Neurobiology, vol. 9, no. 5, pp. 616–621, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Pu, A. M. Kopec, H. D. Boyle, and T. J. Carew, “A novel cysteine-rich neurotrophic factor in Aplysia facilitates growth, MAPK activation, and long-term synaptic facilitation,” Learning and Memory, vol. 21, no. 4, pp. 215–222, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Marlow, M. A. Tosches, R. Tomer et al., “Larval body patterning and apical organs are conserved in animal evolution,” BMC Biology, vol. 12, article 7, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. M. A. Tosches, D. Bucher, P. Vopalensky, and D. Arendt, “Melatonin signaling controls circadian swimming behavior in marine zooplankton,” Cell, vol. 159, no. 1, pp. 46–57, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. F.-Q. Liang, R. Walline, and D. J. Earnest, “Circadian rhythm of brain-derived neurotrophic factor in the rat suprachiasmatic nucleus,” Neuroscience Letters, vol. 242, no. 2, pp. 89–92, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. A. H. L. Fischer, T. Henrich, and D. Arendt, “The normal development of Platynereis dumerilii (Nereididae, Annelida),” Frontiers in Zoology, vol. 7, article 31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Demilly, P. Steinmetz, E. Gazave, L. Marchand, and M. Vervoort, “Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii,” Nature Communications, vol. 4, article 1915, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Lauri, The evolution of the neural crest from an annelid perspective: conserved cell types and signaling pathways in Platynereis dumerilii [Ph.D. thesis], Combined Faculties for the Natural Sciences and for Mathematics of the Ruperto-Carola University of Heidelberg, Heidelberg, Germany, 2013.