Annotation of a New Low Voltage Activated Calcium Channel of Trichoplax adhaerens (Phylum Placozoa)

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Abstract

Studying the voltage-gated calcium channels sheds light on the formation of systems responsible for the coupling of sensors and actuators in a living cell. A homologue of 2090 aa lUNKth in the Trichoplax sp. H2 scaffold and an incomplete protein of 1510 aa lUNKth in the Trichoplax adhaerens scaffold were identified on the basis of the data on the voltage-gated calcium channel TCav3 (2063 aa) from the Trichoplax adhaerens cells. The incomplete hypothetical protein is annotated as Cav3-channel. An EEDD selective filter was found for all 3 proteins and the calcium channel core structure consisting of 24 trans-membrane α-helices was reconstructed. However, the studied proteins demonstrated significant variations in their cytoplasmic domains that indicates the different specialization of Cav3-channels in the signal transduction. So part of the AID motive (alpha-interacting domain) and the adjacent potential sensor from the annotated channel have homologies in 25 species of bony fish, and the corresponding region from both other channels in 41 species of bony fish and in 4 species of snakes was found. Significantly, a highly conserved IIS1-S2 loop with the IEHHNQP sequence was identified lower from the AID motif of bony fish, like in Trichoplax, while the homologous IEHHEQP sequence was revealed in snakes, which differs in the negative residue of glutamic acid that is also present in the corresponding proteins of the rat and human. A modular mechanism for the evolution of Cav3-channels by insertions and merging of protein domains that perform various regulatory functions is suggested based on the analysis of primary transcripts and mature proteins.

About the authors

A. V Kuznetsov

Federal Research Center “A.O. Kovalevsky Institute of Biology of the Southern Seas”, Russian Academy of Sciences; Institute of Radio-electronics and Information Security, Sevastopol State University

Email: kuznet@ibss-ras.ru
prosp. Nakhimova 2, Sevastopol, 299011 Russia; Universitetskaya ul. 33, Sevastopol, 299053 Russia

L. E Kartashov

Department of Instrumental Systems and Automation of Technological Processes, Sevastopol State University

ul. Gogolya 12-14, Sevastopol, 299007 Russia

References

  1. Schulze F. E. Trichoplax adhaerens, nov. gen., nov.spec. Zool. Anzeiger, 6, 92–97 (1883).
  2. Schulze F. E. Uber Trichoplax adhaerens. Physik Abh. Kgl. Akad. Wiss. (Berlin), 1, 1–23 (1891).
  3. 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., and Rokhsar D. S. The Trichoplax genome and the nature of placozoans. Nature, 454 (7207), 955–960 (2008). doi: 10.1038/nature07191
  4. Dellaporta S. L., Xu A., Sagasser S., Jakob W., Moreno M. A., Buss L. W., and Schierwater B. Mitochondrial genome of Trichoplax adhaerens supports placozoa as the basal lower metazoan phylum. Proc. Natl. Acad. Sci. USA, 103 (23), 8751–8756 (2006).doi: 10.1073/pnas.0602076103
  5. Signorovitch A. Y., Buss L. W., and Dellaporta S. L. Comparative genomics of large mitochondria in placozoans. PLoS Genet., 3 (1), e13 (2007). doi: 10.1371/journal.pgen.0030013
  6. Senatore A., Raiss H., and Le P. Physiology and Evolution of Voltage-Gated Calcium Channels in Early Diverging Animal Phyla: Cnidaria, Placozoa, Porifera and Ctenophora. Front. Physiol., 7, 481 (2016). doi: 10.3389/fphys.2016.00481
  7. Ertel E. A., Campbell K. P., Harpold M. M., Hofmann F., Mori Y., Perez-Reyes E., Schwartz A.,Snutch T. P., Tanabe T., Birnbaumer L., Tsien R. W., and Catterall W. A. Nomenclature of voltage-gated calcium channels. Neuron, 25 (3), 533–535 (2000). doi: 10.1016/s0896-6273(00)81057-0
  8. Rang H. P., Ritter J. M., Flower R. J., and Henderson G. Rang & Dale's Pharmacology, 8th Edition (Churchill Livingstone, 2014).
  9. Smith C. L., Abdallah S., Wong Y. Y., Le P., Harracksingh A. N., Artinian L., Tamvacakis A. N., Rehder V., Reese T. S., and Senatore A. Evolutionary insights into T-type Ca2+ channel structure, function, and ion selectivity from the Trichoplax adhaerens homologue. J. Gen. Physiol., 149 (4), 483–510 (2017). doi: 10.1085/jgp.201611683
  10. Strong M., Chandy K. G., and Gutman G. A. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol. Biol. & Evolution, 10 (1), 221–242 (1993). doi: 10.1093/oxfordjournals. molbev.a039986
  11. Ishibashi K., Suzuki M., and Imai M.. Molecular Cloning of a Novel Form (Two-Repeat) Protein Related to Voltage-Gated Sodium and Calcium Channels. Biochem. Biophys. Res. Commun., 270 (2), 370–376 (2000). doi: 10.1006/bbrc.2000.2435
  12. Rahman T., Cai X., Brailoiu G. C., Abood M. E., Brailoiu E., and Patel S. Two-pore channels provide insight into the evolution of voltage-gated Ca2+ and Na+ channels. Science Signaling, 7 (352), ra109 (2014). doi: 10.1126/scisignal.2005450
  13. Warnier M., Gackiere F., Roudbaraki M., and Mariot P. Expression and Role of T-type Calcium Channels during Neuroendocrine Differentiation. J. Cell Signal., 1 (2), 113 (2016). doi: 10.4172/2576-1471.1000113
  14. Kapustin Y., Souvorov A., Tatusova T., and Lipman D. Splign: algorithms for computing spliced alignments with identification of paralogs. Biol. Direct, 3 (20), 1–13 (2008). doi: 10.1186/1745-6150-3-20
  15. Stothard P. The Sequence Manipulation Suite: JavaScript Programs for Analyzing and Formatting Protein and DNA Sequences. BioTechniques, 28, 1102–1104 (2000). doi: 10.2144/00286ir01
  16. Kyte J. and Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol., 157 (1), 105–132 (1982). doi: 10.1016/0022-2836(82)90515-0
  17. Kelley L. A. and Sternberg M. J. E. Protein structure prediction on the Web: A case study using the Phyre server. Nature Protocols, 4 (3), 363–371 (2009). doi: 10.1038/nprot.2009
  18. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., MUNK E. C., and Ferrin T. E. UCSF Chimera--a Visualization System for Exploratory Research and Analysis. J. Comput. Chem.,25 (13), 1605–1612 (2004). doi: 10.1002/jcc.20084
  19. Kamm K., Osigus H. J., Stadler P. F., DeSalle R., and Schierwater B. Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction. Sci Rep., 8 (1), 11168 (2018). doi: 10.1038/s41598-018-29400-y
  20. Kelley L. A., Mezulis S., Yates C. M., Wass M. N., and Sternberg M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10 (6), 845–858 (2015). doi: 10.1038/nprot.2015.053
  21. Berrou L., Dodier Y., Raybaud A., Tousignant A., Dafi O., Pelletier J. N., and Parent L. The C-terminal Residues in the Alpha-interacting Domain (AID) Helix Anchor CaVβ Subunit Interaction and Modulation of CaV2.3 Channels. J. Biol. Chem., 280 (1), 494–505 (2005). doi: 10.1074/jbc.M410859200
  22. Findeisen F., Campiglio M., Jo H., Abderemane-Ali F., Rumpf C. H., Pope L., Rossen N. D., Flucher B. E., DeGrado W. F., and Minor D. L., Jr. Stapled Voltage- Gated Calcium Channel (CaV) α-Interaction Domain (AID) Peptides Act As Selective Protein-Protein Interaction Inhibitors of CaV Function. ACS Chem. Neurosci., 8 (6), 1313–1326 (2017). DOI: 10.1021/ acschemneuro.6b00454
  23. Cloues R. K., Cibulsky S. M., and Sather W. A. Ion Interactions in the High-Affinity Binding Locus of a Voltage-Gated Ca2+ Channel. J. Gen. Physiol., 116 (4), 569–586 (2000). doi: 10.1085/jgp.116.4.569
  24. Cibulsky S. M. and Sather W. A. The Eeee Locus Is the Sole High-Affinity Ca2+ Binding Structure in the Pore of a Voltage-Gated Ca2+ Channel: Block by Ca2+ Entering from the Intracellular Pore Entrance. J. Gen. Physiol., 116 (3), 349–362 (2000). DOI: 10.1085/ jgp.116.3.349
  25. Catterall W. A. Ion Channel Voltage Sensors: Structure, Function, and Pathophysiology. Neuron, 67 (6), 915–928 (2010). doi: 10.1016/j.neuron.2010.08.021
  26. Jensen M. O., Jogini V., Borhani D. W., Leffler A. E., Dror R. O., Shaw D. E. Mechanism of Voltage Gating in Potassium Channels. Science, 336 (6078), 229–233 (2012). doi: 10.1126/science.1216533
  27. Tuluc P., Yarov-Yarovoy V., Benedetti B., and Flucher B. E. Molecular Interactions in the Voltage Sensor Controlling Gating Properties of CaV Calcium Channels. Structure, 24 (2), 261–271 (2015). doi: 10.1016/j.str.2015.11.011
  28. Basic Neurochemistry: Principles of Molecular, Cellular, and Medical Neurobiology. Ed. by S. Brady, G. Siegel, and R. W. Albers, 8th Edition (Elsevier, 2011). 1120 pages. ISBN-10: 0125468075.
  29. Catterall W. A., Striessnig J., Snutch T. P., and Perez-Reyes E. International Union of Pharmacology. XL. Compendium of Voltage-Gated Ion Channels: Calcium Channels. Pharmacol. Rev., 55 (4), 579–581 (2003). doi: 10.1124/pr.55.4.8
  30. Noda M., Shimizu S., Tanabe T., Takai T., Kayano T., Ikeda T., Takahashi H., Nakayama H., Kanaoka Y., and Minamino N. Primary structure of ElectrophoUNK electricus sodium channel deduced from cDNA sequence. Nature, 312 (5990), 121–127 (1984). doi: 10.1038/312121a0
  31. Akaike N., Kostyuk P. G., and Osipchuk Y. V. Dihydropyridine-sensitive low-threshold calcium channels in isolated rat hypothalamic neurones. J. Physiol. (Lond.) 412, 181–195 (1989). doi: 10.1113/jphysiol. 1989.sp017610
  32. Senatore A., Reese T. S., and Smith C. L. Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses. J. Exp. Biol., 220 (18), 3381–3390 (2017). doi: 10.1242/jeb.162396
  33. Enyeart J. J., Mlinar B., and Enyeart J. A. T-type Ca2+ channels are required for adrenocorticotropin-stimulated cortisol production by bovine adrenal zona fasciculata cells. Mol. Endocrinol., 7, 1031–1040 (1993).
  34. Loirand G., Mironneau C., Mironneau J., and Pacaud P. Two types of calcium currents in single smooth muscle cells from rat portal vein. J. Physiol., 412, 333–349 (1989). doi: 10.1113/jphysiol.1989.sp017619
  35. Huguenard J. R. Low-threshold calcium currents in central nervous system neurons. Annu. Rev. Physiol., 58, 329–348 (1996). doi: 10.1146/annurev.ph.58.030196.001553
  36. Catterall W. A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol., 3 (8), a003947 (2011). doi: 10.1101/cshperspect.a003947
  37. Kiyonaka S., Wakamori M., Miki T., Uriu Y., NonakaM., Bito H., Beedle A. M., Mori E., Hara Y., De Waard M., Kanagawa M., Itakura M., Takahashi M., Campbell K. P., and Mori Y. RIM1 confers sustained activity and neurotransmitter vesicle the vesicular SNARE protein synaptobrevin (syb) was dispensable for dockinganchoring to presynaptic Ca2+ channels. Nat Neurosci., 10 (6), 691–701 (2007). doi: 10.1038/nn1904
  38. Smith C. L., Varoqueaux F., Kittelmann M., Azzam R. N., Cooper B., Winters C. A., Eitel M., Fasshauer D., and Reese T. S. Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens. Curr. Biol., 24 (14), 1565–1572 (2014). doi: 10.1016/j.cub.2014.05.046
  39. Yim Y. Y., Zurawski Z., and Hamm H. GPCR Regulation of Secretion. Pharmacol. Ther., 192, 124–140 (2018). doi: 10.1016/j.pharmthera.2018.07.005
  40. Zhang Y., Jiang X., Snutch T. P., and Tao J. Modulation of low-voltage-activated T-type Ca2+ channels. Biochim. Biophys. Acta, 1828 (7), 1550–1559 (2013). doi: 10.1016/j.bbamem.2012.08.032
  41. Кузнецов А. В., Кулешова О. Н., Пронозин А. Ю., Кривенко О. В. и Завьялова О. С. Действие прямоугольных электрических импульсов низкой частоты на трихоплакса (тип Placozoa). Морской биол. журн., 5 (2), 50–66 (2020). doi: 10.21072/mbj.2020.05.2.05
  42. Uversky V. N. Dancing Protein Clouds: The Strange Biology and Chaotic Physics of Intrinsically Disordered Proteins. J. Biol. Chem., 291, 6681–6688 (2016). doi: 10.1074/jbc.R115.685859
  43. Catterall W. A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Devel. Biol., 16 (16), 521–555 (2000). doi: 10.1146/annurev.cellbio. 16.1.521
  44. Opatowsky Y., Chen C. C., Campbell K. P., and Hirsch J. A. Structural Analysis of the Voltage-Dependent Calcium Channel Beta Subunit Functional Core in Complex with Alpha1 Interaction Domain. Neuron, 42, 387–399 (2004). doi: 10.1016/S0896-6273(04)00250-8
  45. Zhao Y., Huang G., Wu Q., Wu K., Li R., Lei J., Pan X., and Yan N. Cryo-EM structures of apo and antagonist-bound human Cav3.1. Nature, 576, 492–497 (2019). doi: 10.1038/s41586-019-1801-3
  46. Cardozo T. J. and Martinez-Ortiz W. Residue assignment correction to the voltage gated calcium Cav1.1 rabbit alpha 1 subunit PDB entries 3JBR & 5GJV. Cell Rep., 23, 1399–1408 (2018). doi: 10.2210/pdb6BYO/pdb
  47. Wu J. P., Yan Z., Li Z. Q., Zhou Q., and Yan N. Structure of the mammalian voltage-gated calcium channel Cav1.1 complex for ClassII map. Nature, 537, 191–196 (2016). doi: 10.2210/pdb5GJW/pdb
  48. Maki R., Roeder W., Traunecker A., Sidman C., Wabl M., Raschke W., and Tonegawa S. The Role of DNA Rearrangement and Alternative RNA Processing in the Expression of Immunoglobulin Delta Genes. Cell, 1981 24 (2), 353–365. doi: 10.1016/0092-8674(81)90325-1
  49. Schmucker D., Clemens J. C., Shu Huidy, Worby C. A., Xiao Jian, Muda M., Dixon J.E., and Zipursky S. L. Drosophila Dscam Is an Axon Guidance Receptor Exhibiting Extraordinary Molecular Diversity. Cell, 101 (6), 671–684 (2000). doi: 10.1016/S0092-8674(00)80878-8
  50. Leman J. K., Ulmschneider M. B., and Gray J. J. Computational modeling of membrane proteins. Proteins, 83 (1), 1–24 (2015). doi: 10.1002/prot.24703
  51. Martinez-Ortiz W., and Cardozo T. J. An Improved Method for Modeling Voltage-Gated Ion Channels at Atomic Accuracy Applied to Human Cav Channels. Cell Rep., 23 (5), 1399–1408 (2018). doi: 10.1016/j.celrep.2018.04.02452
  52. Sebe-Pedros A., Chomsky E., Pang K., Lara-Astiaso D., Gaiti F., Mukamel Z., Amit .I, Hejnol A., Degnan B. M., and Tanay A. Early metazoan cell type diversity and the evolution of multicellular gene regulation. Nat. Ecol. Evol., 2 (7), 1176–1188 (2018). doi: 10.1038/s41559-018-0575-6

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