Sevastopol, Sevastopol, Russian Federation
Sevastopol, Sevastopol, Russian Federation
Sevastopol, Sevastopol, Russian Federation
Sevastopol State University
Sevastopol, Sevastopol, Russian Federation
Mechanoreceptors can transform external mechanical forces into electrochemical signals that induce cell membrane depolarization and initiate waves propagating along the cell surface. The TRPN1/NompC mechanotransduction channel is known to contain ankyrin repeats that act as a gating helix in Drosophila melanogaster [Jin et al., 2017]. In this work, we present for the first time a family of cationic TRPA1-channels in Trichoplax sp. H2 (Placozoa), which consists of 42 homologs ranging from 468 to 3240 aa in length. Three isolated clusters with different polypeptide chain lengths and various contents of ankyrin repeats were identified within the family. The spatial structure of TRPA1-channel RDD36842.1 was reconstructed, and aspirin, a possible TRP-channel blocker, was docked. The structure of the family members is analyzed, the mechanical model of channel operation is considered, and the probable function and physiology of these protein molecules and their role in the behavior of trichoplax are discussed. Variations in the number of ankyrin repeats at the N-terminus of TRP-proteins studied, and the differences detected at the C-terminus can indicate the polyfunctionality of these proteins in Placozoa. Perhaps TRP channels arose in early evolutionary stages before the appearance of multicellularity, but diversified in multicellular animals as the structural organization of those became more complex.
Placozoa, mechanotransduction, TRP-channels, protein 3D-reconstruction, docking
1. Jin P., Bulkley D., Guo Y., Zhang W., Guo Z., Huynh W., Wu S., Meltzer S., Cheng T., Jan L.Y., Jan Y.N., Cheng Y. Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature, 2017, vol. 547, no. 7661, pp. 118-122, doi: 10.1038/nature22981.
2. Kernan M., Cowan D., Zuker C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron, 1994, vol. 12, no. 6, pp. 1195-1206, doi: 10.1016/0896-6273(94)90437-5.
3. Walker R.G., Willingham A.T., Zuker C.S. A Drosophila mechanosensory transduction channel. Science, 2000, vol. 287, no. 5461, pp. 2229-2234, doi: 10.1126/science.287.5461.2229.
4. Cheng L.E., Song W., Looger L.L., Jan L.Y., Jan Y.N. The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron, 2010, vol. 67, no. 3, pp. 373-380, doi: 10.1016/j.neuron.2010.07.004.
5. Kang L., Gao J., Schafer W.R., Xie Z., Xu X.Z.C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron, 2010, vol. 67, no. 3, pp. 381-391, doi: 10.1016/j.neuron.2010.06.032.
6. Ramsey I.S., Delling M., Clapham D.E. An introduction to TRP channels. Annu Rev Physiol., 2006, vol. 68, pp. 619-647, doi: 10.1146/annurev.physiol.68.040204.100431.
7. Venkatachalam K., Montell C. TRP channels. Annu Rev Biochem., 2007, vol. 76, pp. 387-417, doi: 10.1146/annurev.biochem.75.103004.142819.
8. Himmel N.J., Cox D.N. Transient receptor potential channels: current perspectives on evolution, structure, function and nomenclature. Proc Biol Sci., 2020, vol. 287, no. 1933, p. 20201309, doi: 10.1098/rspb.2020.1309.
9. Ishimaru Y., Matsunami H. ransient receptor potential (TRP) channels and taste sensation. J Dent Res., 2009, vol. 88, no. 3, pp. 212-218, doi: 10.1177/0022034508330212.
10. Chung M.K., Jung S.J., Oh S.B. Role of TRP channels in pain sensation. Adv Exp Med Biol., 2011, vol. 704, pp. 615-636, doi: 10.1007/978-94-007-0265-3_33.
11. Julius D. TRP channels and pain. Annu Rev Cell Dev Biol., 2013, vol. 29, pp. 355-384, doi: 10.1146/annurev-cellbio-101011-155833.
12. Sun S., Dong X. Trp channels and itch. Semin Immunopathol., 2016, vol. 38, no. 3, pp. 293-307, doi: 10.1007/s00281-015-0530-4.
13. Kadowaki T. Evolutionary dynamics of metazoan TRP channels. Pflugers Arch., 2015, vol. 467, no. 10, pp. 2043-2053, doi: 10.1007/s00424-015-1705-5.
14. Himmel N.J., Letcher J.M., Sakurai A., Gray T.R., Benson M.N., Cox D.N. Drosophila menthol sensitivity and the Precambrian origins of transient receptor potential-dependent chemosensation. Philos Trans R Soc Lond B Biol Sci., 2019, vol. 374, no. 1785, p. 20190369, doi: 10.1098/rstb.2019.0369.
15. Schierwater B., DeSalle R. Placozoa. Curr Biol., 2018, vol. 28, no. 3, pp. R97-R98, doi: 10.1016/j.cub.2017.11.042.
16. Neff E.P. What is a lab animal? Lab Anim (NY), 2018, vol. 47, no. 9, pp. 223-227, doi: 10.1038/s41684-018-0135-3.
17. Kuznetsov A.V., Halaimova A.V., Ufimtseva M.A., Chelebieva E.S. Blocking a chemical communication between Trichoplax organisms leads to their disorderly movement. International Journal of Parallel, Emergent and Distributed Systems, 2020, vol. 35, no. 4, pp. 473-482, doi: 10.1080/17445760.2020.1753188.
18. Kuznetsov A.V., Vainer V.I., Volkova Y.M., Kartashov L.E. Motility disorders and disintegration into separate cells of Trichoplax sp. H2 in the presence of Zn2+ ions and L-cysteine molecules: A systems approach. Biosystems, 2021, vol. 206, p. 104444, doi: 10.1016/j.biosystems.2021.104444.
19. Armon S., Bull M.S., Aranda-Diaz A., Prakash M. Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity. Proc Natl Acad Sci USA, 2018, vol. 115, no. 44, pp. E10333-E10341, doi: 10.1073/pnas.1802934115.
20. Smith C.L., Reese T.S., Govezensky T., Barrio R.A. Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system. Proc Natl Acad Sci USA, 2019, vol. 116, no. 18, pp. 8901-8908, doi: 10.1073/pnas.1815655116.
21. Kuznetsov A.V. Computer models of piezoproteins and networks of protein-protein interactions in Trichoplax (Placozoa) animals. IV International Black Sea Scientific and Practical Conference of Moscow State University "Problems of Informatics, Control and Artificial Intelligence", May 17-27, 2022, Sevastopol, Russia. (In Russ.)
22. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol., 1990, vol. 215, no. 3, pp. 403-410, doi: 10.1016/S0022-2836(05)80360-2.
23. Marchler-Bauer A., Bryant S.H. CD-Search: protein domain annotations on the fly. Nucleic Acids Res., 2004, vol. 32, pp. W327-331, doi: 10.1093/nar/gkh454.
24. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res., 2011, vol. 39, pp. D225-259, doi: 10.1093/nar/gkq1189.
25. Marchler-Bauer A., Derbyshire M.K., Gonzales N.R. et al. CDD: NCBI's conserved domain database. Nucleic Acids Res., 2015, vol. 43, pp. D222-226, doi: 10.1093/nar/gku1221.
26. Marchler-Bauer A., Bo Y., Han L., He J., Lanczycki C.J. et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res., 2017, vol. 45, no. D1, pp. D200-D203, doi: 10.1093/nar/gkw1129.
27. Papadopoulos J.S., Agarwala R. COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics, 2007, vol. 23, no. 9, pp. 1073-1079, doi: 10.1093/bioinformatics/btm076.
28. Kelley L.A., Mezulis S., Yates C.M., Wass M.N., Sternberg M.J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc., 2015, vol. 10, no. 6, pp. 845-858, doi: 10.1038/nprot.2015.053.
29. Bitencourt-Ferreira G., de Azevedo W.F. Jr. Docking with SwissDock. Methods Mol Biol., 2019, vol. 2053, pp. 189-202, doi: 10.1007/978-1-4939-9752-7_12.
30. Sayle R., Milner-White E.J. RasMol: Biomolecular graphics for all. Trends Biochem Sci., 1995, vol. 20, no. 9, p. 374, doi: 10.1016/s0968-0004(00)89080-5.
31. Cotton R. Learning R: A Step-by-Step Function Guide to Data Analysis. O'Reilly Media; 1st edition, 2013, 400 p.
32. Kamm K., Osigus H.J., Stadler P.F., DeSalle R., Schierwater B. Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction. Sci Rep., 2018, vol. 8, no. 1, p. 11168, doi: 10.1038/s41598-018-29400-y.
33. Liang X., Madrid J., Gartner R., Verbavatz J.M., Schiklenk C., Wilsch-Brauninger M., Bogdanova A., Stenger F., Voigt A., Howard J. A NOMPC-dependent membrane-microtubule connector is a candidate for the gating spring in fly mechanoreceptors. Curr Biol., 2013, vol. 23, no. 9, pp. 755-763, doi: 10.1016/j.cub.2013.03.065.
34. Liang X., Madrid J., Howard J. The microtubule-based cytoskeleton is a component of a mechanical signaling pathway in fly campaniform receptors. Biophys J., 2014, vol. 107, no. 12, pp. 2767-2774, doi: 10.1016/j.bpj.2014.10.052.
35. Zanini D., Gopfert M.C. Mechanosensation: tethered ion channels. Curr Biol., 2013, vol. 23, no. 9, pp. R349-51, doi: 10.1016/j.cub.2013.03.045.
36. Gillespie P.G., Walker R.G. Molecular basis of mechanosensory transduction. Nature, 2001, vol. 413, no. 6852, pp. 194-202, doi: 10.1038/35093011.
37. Howard J., Bechstedt S. Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol., 2004, vol. 14, no. 6, pp. R224-226, doi: 10.1016/j.cub.2004.02.050.
38. Sotomayor M., Corey D.P., Schulten K. In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure, 2005, vol. 13, no. 4, pp. 669-682, doi: 10.1016/j.str.2005.03.001.
39. Lee G., Abdi K., Jiang Y., Michaely P., Bennett V., Marszalek P.E. Nanospring behaviour of ankyrin repeats. Nature, 2006, vol. 440, no. 7081, pp.246-249, doi: 10.1038/nature04437.
40. Zhang W., Yan Z., Jan L.Y., Jan Y.N. Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. Proc Natl Acad Sci USA, 2013, vol. 110, no. 33, pp. 13612-13617, doi: 10.1073/pnas.1312477110.
41. Montell C. Drosophila visual transduction. Trends Neurosci., 2012, vol. 35, no. 6, pp. 356-363, doi: 10.1016/j.tins.2012.03.004.
42. Zhang K., Julius D., Cheng Y. Structural snapshots of TRPV1 reveal mechanism of polymodal functionality. Cell, 2021, vol. 184, no. 20, pp. 5138-5150.e12, doi: 10.1016/j.cell.2021.08.012.
43. Oteiza P., Baldwin M.W. Evolution of sensory systems. Curr Opin Neurobiol., 2021, vol. 71, pp. 52-59, doi: 10.1016/j.conb.2021.08.005.
