Bioinformatic prediction of Trichoplax adhaerens regulatory peptides

General and Comparative Endocrinology

Volumn 212, Issue , 2015, Pages 145-155

  Nikitin, Mikhail ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Neuronal precursors; Placozoa; T. adhaerens

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN RECEPTOR; GRANULIN; HORMONE PRECURSOR; INSULIN; INSULIN RECEPTOR; MEMBRANE RECEPTOR; RECEPTOR PROTEIN; REGULATOR PROTEIN; TEMPTIN; UNCLASSIFIED DRUG; AMIDE; INSULIN DERIVATIVE; NEUROPEPTIDE; PEPTIDE FRAGMENT; PROTEOME;

ANIMAL GENETICS; ARTICLE; BIOINFORMATICS; CELL GROWTH; EXPRESSED SEQUENCE TAG; GENE; GENE IDENTIFICATION; GENE STRUCTURE; GENETIC TRANSCRIPTION; HORMONE ACTION; IMMUNOREACTIVITY; MOLECULAR EVOLUTION; NONHUMAN; PLACOZOA; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; TRICHOPLAX ADHAERENS; TRINS 2 GENE; TRINS 3 GENE; TRINS 4 GENE; TRINS 5 GENE; AMINO ACID SEQUENCE; ANIMAL; BIOLOGY; CLASSIFICATION; EVOLUTION; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; PROCEDURES;

AMIDES; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; COMPUTATIONAL BIOLOGY; GENOME; INSULINS; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; PEPTIDE FRAGMENTS; PLACOZOA; PROTEOME;

EID: 84936070817     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2014.03.049     Document Type: Article

References (66)

1. Aleshin V.V., Petrov N.B. Molecular evidence of regression in evolution of metazoa. Zh. Obsh. Biol. 2002, 63:195-208.
2. Alié A., Manuel M. The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol. Biol. 2010, 10:34.
3. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
4. Anctil M. Chemical transmission in the sea anemone Nematostella vectensis: A genomic perspective. Comp. Biochem. Phys. D 2009, 4:268-289.
5. Baldwin G.S., Patel O., Shulkes A. Evolution of gastrointestinal hormones: the cholecystokinin/gastrin family. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:77-88.
6. Bateman A., Bennett H.P. Granulins: the structure and function of an emerging family of growth factors. J. Endocrinol. 1998, 158:145-151.
7. Bjerknes M., Cheng H. Neurogenin 3 and the enteroendocrine cell lineage in the adult mouse small intestinal epithelium. Dev. Biol. 2006, 300:722-735.
8. Chan S.J., Steiner D.F. Insulin through the ages: phylogeny of a growth promoting and metabolic regulatory hormone. Am. Zool. 2000, 40:213-222.
9. Christie A.E., Nolan D.H., Garcia Z.A., McCoole M.D., Harmon S.M., Congdon-Jones B., Ohno P., Hartline N., Congdon C.B., Baer K.N., Lenz P.H. Bioinformatic prediction of arthropod/nematode-like peptides in non-arthropod, non-nematode members of the Ecdysozoa. Gen. Comp. Endocr. 2011, 170:480-486.
10. Clynen E., Reumer A., Baggerman G., Mertens I., Schoofs L. Neuropeptide biology in Drosophila. Adv. Exp. Med. Biol. 2010, 692:192-210.
11. Cummins S.F., Nichols A.E., Amare A., Hummon A.B., Sweedler J.V., Nagle G.T. Characterization of Aplysia enticin and temptin, two novel water-borne protein pheromones that act in concert with attractin to stimulate mate attraction. J. Biol. Chem. 2004, 279:25614-25622.
12. Cummins S.F., Xie F., de Vries M.R., Annangudi S.P., Misra M., Degnan B.M., Sweedler J.V., Nagle G.T., Schein C.H. Aplysia temptin - the "glue" in the water-borne attractin pheromone complex. FEBS J. 2007, 274:5425-5437.
13. Delfino K.R., Southey B.R., Sweedler J.V., Rodriguez-Zas S.L. Genome-wide census and expression profiling of chicken neuropeptide and prohormone convertase genes. Neuropeptides 2010, 44:31-44.
14. Dellaporta S.L., Xu A., Sagasser S., Jakob W., Moreno M.A., Buss L.W., Schierwater B. Mitochondrial genome of Trichoplax adhaerens supports placozoa as the basal lower metazoan phylum. Proc. Natl. Acad. Sci. USA 2006, 103:8751-8756.
15. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
16. Eitel M., Schierwater B. The phylogeography of the Placozoa suggests a taxon-rich phylum in tropical and subtropical waters. Mol. Ecol. 2010, 19:2315-2327.
17. Eitel M., Osigus H.-J., DeSalle R., Schierwater B. Global diversity of the Placozoa. PLoS One 2013, 8:e57131.
18. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2:953-971. 10.1038/nprot.2007.131.
19. Grell K.G. Trichoplax adhaerens F.E. Schulze und die Entstehung der Metazoan. Naturwissenschaftliche Rundschau 1971, 24:160-161.
20. Grell K.G. Reproduction of Placozoa. Advances in Invertebrate Reproduction 1984, 541-546. Elsevier. W. Engels (Ed.).
21. Grell K.G., Benwitz G. Erganzende Untersuchungen zur Ultrastruktur von Trichoplax adhaerens F.E. Schulze (Placozoa). Zoomorphology 1981, 98:47-67.
22. Grimmelikhuijzen C.J.P., Hauser F. Mini-review: the evolution of neuropeptide signaling. Regul. Pept. 2012, 177(Suppl.):S6-9.
23. Guidi L., Eitel M., Cesarini E., Schierwater B., Balsamo M. Ultrastructural analyses support different morphological lineages in the phylum Placozoa Grell, 1971. J. Morphol. 2011, 272:371-378.
24. Hoff K.J., Stanke M. WebAUGUSTUS - a web service for training AUGUSTUS and predicting genes in eukaryotes. Nucleic Acids Res. 2013, 41:W123-W128.
25. Husson S.J., Mertens I., Janssen T., Lindemans M., Schoofs L. Neuropeptidergic signaling in the nematode Caenorhabditis elegans. Prog. Neurobiol. 2007, 82:33-55.
26. Jacobs D.K., Nakanishi N., Yuan D., Camara A., Nichols S.A., Hartenstein V. Evolution of sensory structures in basal metazoa. Integr. Comp. Biol. 2007, 47:712-723.
27. Jakob W., Sagasser S., Dellaporta S., Holland P., Kuhn K., Schierwater B. The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev. Genes Evol. 2004, 214:170-175.
28. Kawada T., Sekiguchi T., Sakai T., Aoyama M., Satake H. Neuropeptides, hormone peptides, and their receptors in Ciona intestinalis: an update. Zool. Sci. 2010, 27:134-153.
29. Li, C., 2008. Neuropeptides. WormBook 1-36. The C. elegans Research Community, WormBook, doi: , http://www.wormbook.org.
30. Li B., Predel R., Neupert S., Hauser F., Tanaka Y., Cazzamali G., Williamson M., Arakane Y., Verleyen P., Schoofs L., Schachtner J., Grimmelikhuijzen C.J.P., Park Y. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res. 2008, 18:113-122.
31. Martinelli C., Spring J. Distinct expression patterns of the two T-box homologues Brachyury and Tbx2/3 in the placozoan Trichoplax adhaerens. Dev. Genes Evol. 2003, 213:492-499.
32. Menschaert G., Vandekerckhove T.T.M., Baggerman G., Landuyt B., Sweedler J.V., Schoofs L., Luyten W., Van Criekinge W. A hybrid, de novo based, genome-wide database search approach applied to the sea urchin neuropeptidome. J. Proteome Res. 2010, 9:990-996.
33. Nothacker H.P., Grimmelikhuijzen C.J.P. Molecular cloning of a novel, putative G protein-coupled receptor from sea anemones structurally related to members of the FSH, TSH, LH/CG receptor family from mammals. Biochem. Biophys. Res. Commun. 1993, 197:1062-1069.
34. Novo M., Riesgo A., Fernández-Guerra A., Giribet G. Pheromone evolution, reproductive genes, and comparative transcriptomics in Mediterranean earthworms (Annelida, Oligochaeta, Hormogastridae). Mol. Biol. Evol. 2013, 30:1614-1629.
35. Okshtein I.L. On the biology of Trichoplax sp. (Placozoa). Zool. Zh. 1987, 66:325-338.
36. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786. 10.1038/nmeth.1701.
37. Petrov N.B., Aleshin V.V. Conditionally neutral phylogenetic markers of major taxa: a new aspect of the evolution of macromolecules. Russ. J. Genet. 2002, 38:877-894.
38. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Quéinnec E., Da Silva C., Wincker P., Le Guyader H., Leys S., Jackson D.J., Schreiber F., Erpenbeck D., Morgenstern B., Wörheide G., Manuel M. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
39. Pick K.S., Philippe H., Schreiber F., Erpenbeck D., Jackson D.J., Wrede P., Wiens M., Alié A., Morgenstern B., Manuel M., Wörheide G. Improved phylogenomic taxon sampling noticeably affects non-bilaterian relationships. Mol. Biol. Evol. 2010, 27:1983-1987.
40. Reiher W., Shirras C., Kahnt J., Baumeister S., Isaac R.E., Wegener C. Peptidomics and peptide hormone processing in the Drosophila midgut. J. Proteome Res. 2011, 10:1881-1892.
41. Ringrose J.H., van den Toorn H.W.P., Eitel M., Post H., Neerincx P., Schierwater B., Maarten Altelaar A.F., Heck A.J.R. Deep proteome profiling of Trichoplax adhaerens reveals remarkable features at the origin of metazoan multicellularity. Nat. Commun. 2013, 4:1408.
42. Robitzki A., Schroder H.C., Ugarkovic D., Pfeifer K., Uhlenbruck G., Muller W.E. Demonstration of an endocrine signaling circuit for insulin in the sponge Geodia cydonium. EMBO J. 1989, 8:2905-2909.
43. Rozhnov S.V. Development of the trophic structure of Vendian and Early Paleozoic marine communities. J. Paleontol. 2009, 43:1364-1377.
44. Rozhnov S.V. From Vendian to Cambrian: the beginning of morphological disparity of modern metazoan phyla. Russ. J. Dev. Biol. 2010, 41:357-368.
45. Ruthmann A., Grell K.G., Benwitz B. DNA-content and fragmentation of the egg-nucleus of Trichoplax adhaerens. Z. Naturforsch. 1981, 60:564-567.
46. Ryan J.F., Pang K., Mullikin J.C., Martindale M.Q., Baxevanis A.D. The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. Evodevo 2010, 1:9.
47. Ryan J.F., Pang K., Schnitzler C.E., Nguyen A.-D., Moreland R.T., Simmons D.K., Koch B.J., Francis W.R., Havlak P., Smith S.A., Putnam N.H., Haddock S.H.D., Dunn C.W., Wolfsberg T.G., Mullikin J.C., Martindale M.Q., Baxevanis A.D. The genome of the Ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 2013, 342:1242592.
48. Sakarya O., Armstrong K.A., Adamska M., Adamski M., Wang I.-F., Tidor B., Degnan B.M., Oakley T.H., Kosik K.S. A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2007, 2:e506.
49. Schierwater B., Eitel M., Jakob W., Osigus H.-J., Hadrys H., Dellaporta S.L., Kolokotronis S.-O., DeSalle R. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "Urmetazoon" hypothesis. PLoS Biol. 2009, 7:e20.
50. Schuchert P. Trichoplax adhaerens (Phylum Placozoa) has cells that react with antibodies against the neuropeptide RFamide. Acta Zool. 1993, 74:115-117.
51. Seravin L.N. Orientation of invertebrates in three-dimensional space: 4. Reaction of turning from the dorsal side to the ventral one. Zool. Zh 1989, 68:18-28.
52. Signorovitch A.Y., Dellaporta S.L., Buss L.W. Molecular signatures for sex in the Placozoa. Proc. Natl. Acad. Sci. USA 2005, 102:15518-15522.
53. Skorokhod A., Gamulin V., Gundacker D., Kavsan V., Muller I.M., Muller W. Origin of insulin receptor-like tyrosine kinases in marine sponges. Biol. Bull. 1999, 197:198-206.
54. Smout M.J., Laha T., Mulvenna J., Sripa B., Suttiprapa S., Jones A., Brindley P.J., Loukas A. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog. 2009, 5:e1000611.
55. Sonmez K., Zaveri N.T., Kerman I.A., Burke S., Neal C.R., Xie X., Watson S.J., Toll L. Evolutionary sequence modeling for discovery of peptide hormones. PLoS Comput. Biol. 2009, 5:e1000258.
56. Southey B.R., Amare A., Zimmerman T.A., Rodriguez-Zas S.L., Sweedler J.V. NeuroPred: a tool to predict cleavage sites in neuropeptide precursors and provide the masses of the resulting peptides. Nucleic Acids Res. 2006, 34:W267-W272.
57. Sperling E.A., Vinther J. A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol. Dev. 2010, 12:201-209.
58. 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. The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955-960.
59. Stanke M., Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 2005, 33:W465-W467.
60. Sternini C., Anselmi L., Rozengurt E. Enteroendocrine cells: a site of "taste" in gastrointestinal chemosensing. Curr. Opin. Endocrinol. Diabetes Obes. 2008, 15:73-78.
61. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
62. Ueda T., Koya S., Maruyama Y.K. Dynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence. Biosystems 1999, 54:65-70.
63. Van Loy T., Vandersmissen H.P., Van Hiel M.B., Poels J., Verlinden H., Badisco L., Vassart G., Vanden Broeck J. Comparative genomics of leucine-rich repeats containing G protein-coupled receptors and their ligands. Gen. Comp. Endocr. 2008, 155:14-21.
64. Veenstra J.A. Neurohormones and neuropeptides encoded by the genome of Lottia gigantea, with reference to other mollusks and insects. Gen. Comp. Endocr. 2010, 167:86-103.
65. Veenstra J.A. Neuropeptide evolution: neurohormones and neuropeptides predicted from the genomes of Capitella teleta and Helobdella robusta. Gen. Comp. Endocr. 2011, 171:160-175.
66. Voigt O., Collins A.G., Pearse V.B., Pearse J.S., Ender A., Hadrys H., Schierwater B. Placozoa - no longer a phylum of one. Curr. Biol. 2004, 14:R944-R945.