Spatial Models of Piezoproteins and Networks of Protein-Protein Interactions in Trichoplax Animals (Placozoa)
- Authors: Kuznetsov A.V.1,2,3, Grishin I.Y.3, Vtyurina D.N.4
-
Affiliations:
- Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences
- Sevastopol State University
- Branch of the Lomonosov Moscow State University
- Semenov Federal Research Center for Chemical Physics, Russian Academy of Sciences
- Issue: Vol 57, No 5 (2023)
- Pages: 895-897
- Section: БИОИНФОРМАТИКА
- URL: https://innoscience.ru/0026-8984/article/view/655389
- DOI: https://doi.org/10.31857/S0026898423050075
- EDN: https://elibrary.ru/PNKHJR
- ID: 655389
Cite item
Abstract
The marine free-living organism Trichoplax (phylum Placozoa) resembles the unicellular amoeba in shape and type of movement. Trichoplax diverged from the main evolutionary tree in the Neoproterozoic Era and is one of the simplest models of a multicellular animal, as well as a strong example of the ensemble of interacting cells in an organism during its development and movement. Two orthologs of mouse Piezo1 protein (6B3R) were found in two Trichoplax haplotypes H1 and H2 as a result of a search for similar sequences in the NCBI databases. Spatial models of the corresponding proteins, XP_002112008.1 and RDD46920.1, were created based on the structural alignment using a 6KG7 (mouse Piezo2) template. The analysis of domain structures was performed, and a limited graph of protein‒protein interactions of the hypothetical mechanosensor XP_002112008.1 was constructed. The possibility of signal transduction from the mechanoreceptor to membrane complexes, cytoplasm and cell nucleus was shown. It is assumed that mechanosensory receptors of Trichoplax are involved in the perception of force stimuli between neighboring cells and the environment. Based on the obtained data, we propose to use the primitive Trichoplax organism as the simplest multicellular model for mechanical and morphogenetic movements.
About the authors
A. V. Kuznetsov
Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences; Sevastopol State University; Branch of the Lomonosov Moscow State University
Email: vtyurinad@gmail.com
Russia, 299011, Sevastopol; Russia, 299053, Sevastopol; Russia, 299001, Sevastopol
I. Yu. Grishin
Branch of the Lomonosov Moscow State University
Email: vtyurinad@gmail.com
Russia, 299001, Sevastopol
D. N. Vtyurina
Semenov Federal Research Center for Chemical Physics, Russian Academy of Sciences
Author for correspondence.
Email: vtyurinad@gmail.com
Russia, 119991, Moscow
References
- Niethammer P. (2021) Components and mechanisms of nuclear mechanotransduction. Annu. Rev. Cell Dev. Biol. 37, 233‒256. https://doi.org/10.1146/annurev-cellbio-120319-030049
- Fajardo-Cavazos P., Nicholson W.L. (2021) Mechanotransduction in prokaryotes: a possible mechanism of spaceflight adaptation. Life (Basel). 11(1), 33. https://doi.org/10.3390/life11010033
- Jin P., Jan L.Y., Jan Y.N. (2020) Mechanosensitive ion channels: structural features relevant to mechanotransduction mechanisms. Annu. Rev. Neurosci. 43, 207‒229. https://doi.org/10.1146/annurev-neuro-070918-050509
- Marshall K.L., Lumpkin E.A. (2012) The molecular basis of mechanosensory transduction. Adv Exp. Med. Biol. 739, 142‒155. https://doi.org/10.1007/978-1-4614-1704-0_9
- Clapham D.E. (2007) Calcium signaling. Cell. 131(6), 1047‒1058. https://doi.org/10.1016/j.cell.2007.11.028
- Perozo E. (2006) Gating prokaryotic mechanosensitive channels. Nat. Rev. Mol. Cell Biol. 7(2), 109‒119. https://doi.org/10.1038/nrm1833
- Arnadóttir J., Chalfie M. (2010) Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111‒137. https://doi.org/10.1146/annurev.biophys.37.032807.125836
- Earley S., Santana L.F., Lederer W.J. (2021) The physiological sensor channels TRP and piezo: nobel prize in physiology or medicine. Physiol. Rev. 102(2), 1153‒1158. https://doi.org/10.1152/physrev.00057.2021
- Du G., Chen W., Li L., Zhang Q. (2022) The potential role of mechanosensitive ion channels in substrate stiffness-regulated Ca2+ response in chondrocytes. Connect. Tissue Res. 63(5), 453‒462. https://doi.org/10.1080/03008207.2021.2007902
- Coste B., Mathur J., Schmidt M., Earley T.J., Ranade S., Petrus M.J., Dubin A.E., Patapoutian A. (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science. 330(6000), 55‒60. https://doi.org/10.1126/science.1193270
- Fang X.Z., Zhou T., Xu J.Q., Wang Y.X., Sun M.M., He Y.J., Pan S.W., Xiong W., Peng Z.K., Gao X.H., Shang Y. (2021) Structure, kinetic properties and biological function of mechanosensitive Piezo channels. Cell Biosci. 11(1), 13. https://doi.org/10.1186/s13578-020-00522-z
- Barzegari A., Omidi Y., Ostadrahimi A., Gueguen V., Meddahi-Pellé A., Nouri M., Pavon-Djavid G. (2020) The role of Piezo proteins and cellular mechanosensing in tuning the fate of transplanted stem cells. Cell Tissue Res. 381(1), 1‒12. https://doi.org/10.1007/s00441-020-03191-z
- Ge J., Li W., Zhao Q., Li N., Chen M., Zhi P., Li R., Gao N., Xiao B., Yang M. (2015) Architecture of the mammalian mechanosensitive Piezo1 channel. Nature. 527(7576), 64‒69. https://doi.org/10.1038/nature15247
- Coste B., Xiao B., Santos J.S., Syeda R., Grandl J., Spencer K.S., Kim S.E., Schmidt M., Mathur J., Dubin A.E., Montal M., Patapoutian A. (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature. 483(7388), 176‒181. https://doi.org/10.1038/nature10812
- Coste B., Murthy S.E., Mathur J., Schmidt M., Mechioukhi Y., Delmas P., Patapoutian A. (2015) Piezo1 ion channel pore properties are dictated by C-terminal region. Nat. Commun. 6, 7223. https://doi.org/10.1038/ncomms8223
- Syeda R., Florendo M.N., Cox C.D., Kefauver J.M., Santos J.S., Martinac B., Patapoutian A. (2016) Piezo1 channels are inherently mechanosensitive. Cell Rep. 17(7), 1739‒1746. https://doi.org/10.1016/j.celrep.2016.10.033
- Syed T., Schierwater B. (2002) The evolution of the Placozoa: a new morphological model. Palaeobiodiversity and Palaeoenvironments. 82(1), 315‒324. https://doi.org/10.1007/BF03043791
- Srivastava M., Begovic E., Chapman J., Putnam N.H., Hellsten U., Kawashima T., Kuo A., Mitros T., Salamov A., Carpenter M.L., Signorovitch A.Y., Moreno M.A., Kamm K., Grimwood J., Schmutz J., Shapiro H., Grigoriev I.V., Buss L.W., Schierwater B., Dellaporta S.L., Rokhsar D.S. (2008) The Trichoplax genome and the nature of placozoans. Nature. 454(7207), 955‒960. https://doi.org/10.1038/nature07191
- Kamm K., Osigus H.J., Stadler P.F., DeSalle R., Schierwater B. (2018) Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction. Sci. Rep. 8(1), 11168. https://doi.org/10.1038/s41598-018-29400-y
- Smith C.L., Varoqueaux F., Kittelmann M., Azzam R.N., Cooper B., Winters C.A., Eitel M., Fasshauer D., Reese T.S. (2014) Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens. Curr. Biol. 24(14), 1565‒1572. https://doi.org/10.1016/j.cub.2014.05.046
- Wenderoth H. (1990) Cytoplasmic vibrations due to flagellar beating in Trichoplax adhaerens F. E. Schulze (Placozoa). Z. Naturforsch. 45, 715‒722. https://doi.org/10.1515/znc-1990-0624
- Armon S., Bull M.S., Aranda-Diaz A., Prakash M. (2018) Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity. Proc. Natl. Acad. Sci. USA. 115(44), E10333‒E10341. https://doi.org/10.1073/pnas.1802934115
- Kuznetsov A.V., Halaimova A.V., Ufimtseva M.A., Chelebieva E.S. (2020) Blocking a chemical communication between Trichoplax organisms leads to their disorderly movement. Int. J. Parallel Emergent Distributed Systems. 35(4), 473‒482. https://doi.org/10.1080/17445760.2020.1753188
- Kuznetsov A.V., Vainer V.I., Volkova Y.M., Kartashov L.E. (2021) 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. 206, 104444. https://doi.org/10.1016/j.biosystems.2021.104444
- Ueda T., Koya S., Maruyama Y.K. (1999) Dynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence. Biosystems. 54(1–2), 65‒70. https://doi.org/10.1016/s0303-2647(99)00066-0
- Smith C.L., Reese T.S., Govezensky T., Barrio R.A. (2019) Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system. Proc. Natl. Acad. Sci. USA. 116(18), 8901‒8908. https://doi.org/10.1073/pnas.1815655116
- Velankar S., Burley S.K., Kurisu G., Hoch J.C., Markley J.L. (2021) The protein data bank archive. Methods Mol. Biol. 2305, 3‒21. https://doi.org/10.1007/978-1-0716-1406-8_1
- Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215(3), 403‒410. https://doi.org/10.1016/S0022-2836(05)80360-2
- Kelley L.A., Mezulis S., Yates C.M., Wass M.N., Sternberg M.J. (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10(6), 845‒858. https://doi.org/10.1038/nprot.2015.053
- Sayle R.A., Milner-White E.J. (1995) RASMOL: biomolecular graphics for all. Trends Biochem. Sci. 20(9), 374. https://doi.org/10.1016/s0968-0004(00)89080-5
- Mistry J., Chuguransky S., Williams L., Qureshi M., Salazar G.A., Sonnhammer E.L.L., Tosatto S.C.E., Paladin L., Raj S., Richardson L.J., Finn R.D., Bateman A. (2021) Pfam: the protein families database in 2021. Nucleic Acids Res. 49(D1), D412‒D419. https://doi.org/10.1093/nar/gkaa913
- Szklarczyk D., Gable A.L., Nastou K.C., Lyon D., Kirsch R., Pyysalo S., Doncheva N.T., Legeay M., Fang T., Bork P., Jensen L.J., von Mering C. (2021) The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 49(D1), D605‒D612. https://doi.org/10.1093/nar/gkaa1074
- Guo Y.R., MacKinnon R. (2017) Structure-based membrane dome mechanism for Piezo mechanosensitivity. Elife. 6, e33660. https://doi.org/10.7554/eLife.33660
- Wang L., Zhou H., Zhang M., Liu W., Deng T., Zhao Q., Li Y., Lei J., Li X., Xiao B. (2019) Structure and mechanogating of the mammalian tactile channel PIEZO2. Nature. 573(7773), 225‒229. https://doi.org/10.1038/s41586-019-1505-8
- Grigorov M.G. (2005) Global properties of biological networks. Drug Discov. Today. 10(5), 365‒372. https://doi.org/10.1016/S1359-6446(05)03369-6
- Ranade S.S., Syeda R., Patapoutian A. (2015) Mechanically activated ion channels. Neuron. 87(6), 1162‒1179. https://doi.org/10.1016/j.neuron.2015.08.032
- Фадеева М.В., Курченко В.М., Кузнецов А.В. (2022) Описание семейства катионных TRPА1-каналов Trichoplax adhaerens. Актуальные вопросы биологической физики и химии. БФФХ-2022: материалы XVII Междунар. науч. конф. г. Севастополь, РФ, 2022. с. 201‒202.
- Фадеева М.В., Сергеева Е.В., Рыбакова К.А., Кузнецов А.В. (2022) Характеристика семейства катионных TRPA1-каналов Trichoplax sp. H2 (Placozoa). Актуальные вопр. биол. физики и химии. 7(3), 493‒450.
- Scheres B., van der Putten W.H. (2017) The plant perceptron connects environment to development. Nature. 543(7645), 337‒345. https://doi.org/10.1038/nature22010
- Timsit Y., Grégoire S.P. (2021) Towards the idea of molecular brains. Int. J. Mol. Sci. 22(21), 11868. https://doi.org/10.3390/ijms222111868
- Cox C.D., Bavi N., Martinac B. (2019) Biophysical principles of ion-channel-mediated mechanosensory transduction. Cell Rep. 29(1), 1‒12. https://doi.org/10.1016/j.celrep.2019.08.075
- Lewis A.H., Grandl J. (2021) Piezo1 ion channels inherently function as independent mechanotransducers. Elife. 10, e70988. https://doi.org/10.7554/eLife.70988
- Yang X., Lin C., Chen X., Li S., Li X., Xiao B. (2022) Structure deformation and curvature sensing of PIEZO1 in lipid membranes. Nature. 604(7905), 377‒383. https://doi.org/10.1038/s41586-022-04574-8
- Young M., Lewis A.H., Grandl J. (2022) Physics of mechanotransduction by Piezo ion channels. J. Gen. Physiol. 154(7), e202113044. https://doi.org/10.1085/jgp.202113044
Supplementary files
