A combined strategy of neuropeptide prediction and tandem mass spectrometry identifies evolutionarily conserved ancient neuropeptides in the sea anemone Nematostella vectensis

English version

Autoři: Eisuke Hayakawa ^aff001; Hiroshi Watanabe ^aff002; Gerben Menschaert ^aff004; Thomas W. Holstein ^aff003; Geert Baggerman ^aff005; Liliane Schoofs ^aff001
Působiště autorů: Research Group of Functional Genomics and Proteomics, KU Leuven, Leuven, Belgium ^aff001; Evolutionary Neurobiology Unit, Okinawa Institute of Science & Technology, Okinawa, Japan ^aff002; Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany ^aff003; Faculty of Bioscience Engineering, Laboratory for Bioinformatics and Computational Genomics, Ghent University, Ghent, Belgium ^aff004; CFP/Ceproma, University Antwerpen, Antwerpen, Belgium ^aff005; VITO, Applied Bio & molecular Systems (ABS), Mol, Belgium ^aff006
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0215185

Souhrn

Neuropeptides are a class of bioactive peptides shown to be involved in various physiological processes, including metabolism, development, and reproduction. Although neuropeptide candidates have been predicted from genomic and transcriptomic data, comprehensive characterization of neuropeptide repertoires remains a challenge owing to their small size and variable sequences. De novo prediction of neuropeptides from genome or transcriptome data is difficult and usually only efficient for those peptides that have identified orthologs in other animal species. Recent peptidomics technology has enabled systematic structural identification of neuropeptides by using the combination of liquid chromatography and tandem mass spectrometry. However, reliable identification of naturally occurring peptides using a conventional tandem mass spectrometry approach, scanning spectra against a protein database, remains difficult because a large search space must be scanned due to the absence of a cleavage enzyme specification. We developed a pipeline consisting of in silico prediction of candidate neuropeptides followed by peptide-spectrum matching. This approach enables highly sensitive and reliable neuropeptide identification, as the search space for peptide-spectrum matching is highly reduced. Nematostella vectensis is a basal eumetazoan with one of the most ancient nervous systems. We scanned the Nematostella protein database for sequences displaying structural hallmarks typical of eumetazoan neuropeptide precursors, including amino- and carboxyterminal motifs and associated modifications. Peptide-spectrum matching was performed against a dataset of peptides that are cleaved in silico from these putative peptide precursors. The dozens of newly identified neuropeptides display structural similarities to bilaterian neuropeptides including tachykinin, myoinhibitory peptide, and neuromedin-U/pyrokinin, suggesting these neuropeptides occurred in the eumetazoan ancestor of all animal species.

Klíčová slova:

Database searching – Protein extraction – Sequence databases – Sequence motif analysis – Sequence similarity searching – Signal peptides – Animal evolution – Amidation

Zdroje

1. Van Bael S, Watteyne J, Boonen K, De Haes W, Menschaert G, Ringstad N, et al. Mass spectrometric evidence for neuropeptide-amidating enzymes in Caenorhabditis elegans. J Biol Chem. 2018;293: 6052–6063. doi: 10.1074/jbc.RA117.000731 29487130

2. Fricker LD. Neuropeptide-processing enzymes: applications for drug discovery. AAPS J. 2005;7: E449–55. doi: 10.1208/aapsj070244 16353923

3. Hook V, Funkelstein L, Lu D, Bark S, Wegrzyn J, Hwang S-R. Proteases for processing proneuropeptides into peptide neurotransmitters and hormones. Annu Rev Pharmacol Toxicol. 2008;48: 393–423. doi: 10.1146/annurev.pharmtox.48.113006.094812 18184105

4. Hökfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M. Neuropeptides—an overview. Neuropharmacology. 2000;39: 1337–56. doi: 10.1016/s0028-3908(00)00010-1 10818251

5. Emeson RB. Hypothalamic peptidyl-glycine alpha-amidating monooxygenase: preliminary characterization. J Neurosci. 1984;4: 2604–13. https://doi.org/10.1523/JNEUROSCI.04-10-02604.1984 6491725

6. Harada M, Fukasawa KM, Fukasawa K, Nagatsu T. Inhibitory action of proline-containing peptides on Xaa-Pro-dipeptidylaminopeptidase. Biochim Biophys Acta. 1982;705: 288–90. doi: 10.1016/0167-4838(82)90191-1 6126216

7. Conlon JM, Larhammar D. The evolution of neuroendocrine peptides. Gen Comp Endocrinol. 2005;142: 53–9. doi: 10.1016/j.ygcen.2004.11.016 15862548

8. Baggerman G, Cerstiaens A, De Loof A, Schoofs L. Peptidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem. 2002;277: 40368–74. doi: 10.1074/jbc.M206257200 12171930

9. Clynen E, Baggerman G, Veelaert D, Cerstiaens A, Van der Horst D, Harthoorn L, et al. Peptidomics of the pars intercerebralis-corpus cardiacum complex of the migratory locust, Locusta migratoria. Eur J Biochem. 2001;268: 1929–39. doi: 10.1046/j.1432-1327.2001.02067.x 11277915

10. Fricker LD, Lim J, Pan H, Che F-Y. Peptidomics: identification and quantification of endogenous peptides in neuroendocrine tissues. Mass Spectrom Rev. 2006;25: 327–44. doi: 10.1002/mas.20079 16404746

11. De Haes W, Van Sinay E, Detienne G, Temmerman L, Schoofs L, Boonen K. Functional neuropeptidomics in invertebrates. Biochim Biophys Acta. 2014; doi: 10.1016/j.bbapap.2014.12.011 25528324

12. Dallas DC, Guerrero A, Parker EA, Robinson RC, Gan J, German JB, et al. Current peptidomics: Applications, purification, identification, quantification and functional analysis. Proteomics. 2014; doi: 10.1002/pmic.201400310 25429922

13. Pauls D, Chen J, Reiher W, Vanselow JT, Schlosser A, Kahnt J, et al. Peptidomics and processing of regulatory peptides in the fruit fly Drosophila. EuPA Open Proteomics. 2014;3: 114–127. doi: 10.1016/j.euprot.2014.02.007

14. Hayakawa E, Menschaert G, De Bock P-J, Luyten W, Gevaert K, Baggerman G, et al. Improving the identification rate of endogenous peptides using electron transfer dissociation and collision-induced dissociation. J Proteome Res. 2013;12: 5410–21. doi: 10.1021/pr400446z 24032530

15. Hummon AB, Richmond TA, Verleyen P, Baggerman G, Huybrechts J, Ewing MA, et al. From the genome to the proteome: uncovering peptides in the Apis brain. Science. 2006;314: 647–9. doi: 10.1126/science.1124128 17068263

16. Christie AE. Prediction of the peptidomes of Tigriopus californicus and Lepeophtheirus salmonis (Copepoda, Crustacea). Gen Comp Endocrinol. 2014;201: 87–106. doi: 10.1016/j.ygcen.2014.02.015 24613138

17. Hauser F, Neupert S, Williamson M, Predel R, Tanaka Y, Grimmelikhuijzen CJP. Genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp Nasonia vitripennis. J Proteome Res. 2010;9: 5296–310. doi: 10.1021/pr100570j 20695486

18. Dircksen H, Neupert S, Predel R, Verleyen P, Huybrechts J, Strauss J, et al. Genomics, transcriptomics, and peptidomics of Daphnia pulex neuropeptides and protein hormones. J Proteome Res. 2011;10: 4478–504. doi: 10.1021/pr200284e 21830762

19. Jékely G. Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci U S A. 2013;110: 8702–7. doi: 10.1073/pnas.1221833110 23637342

20. De Loof A, Schoofs L. Homologies between the amino acid sequences of some vertebrate peptide hormones and peptides isolated from invertebrate sources. Comp Biochem Physiol B. 1990;95: 459–68. doi: 10.1016/0305-0491(90)90003-c 2184989

21. Anctil M, Grimmelikhuijzen CJP. Excitatory action of the native neuropertide Antho-RFamide on muscles in the pennatulid Renilla köllikeri. Gen Pharmacol Vasc Syst. 1989;20: 381–384. doi: 10.1016/0306-3623(89)90277-2

22. Fujisawa T, Hayakawa E. Peptide signaling in Hydra. Int J Dev Biol. 2012;56: 543–50. doi: 10.1387/ijdb.113477tf 22689368

23. Grimmelikhuijzen CJ, Graff D. Isolation of pyroGlu-Gly-Arg-Phe-NH2 (Antho-RFamide), a neuropeptide from sea anemones. Proc Natl Acad Sci U S A. 1986;83: 9817–21. doi: 10.1073/pnas.83.24.9817 2879288

24. McFarlane ID, Anderson PA, Grimmelikhuijzen CJ. Effects of three anthozoan neuropeptides, Antho-RWamide I, Antho-RWamide II and Antho-RFamide, on slow muscles from sea anemones. J Exp Biol. 1991;156: 419–31. Available: http://www.ncbi.nlm.nih.gov/pubmed/1675657 1675657

25. Takahashi T, Muneoka Y, Lohmann J, Lopez de Haro MS, Solleder G, Bosch TC, et al. Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families. Proc Natl Acad Sci U S A. 1997;94: 1241–6. doi: 10.1073/pnas.94.4.1241 9037037

26. Takahashi T, Hayakawa E, Koizumi O, Fujisawa T. Neuropeptides and their functions in Hydra. Acta Biol Hung. 2008;59 Suppl: 227–35. doi: 10.1556/ABiol.59.2008.Suppl.32 18652396

27. Yum S, Takahashi T, Koizumi O, Ariura Y, Kobayakawa Y, Mohri S, et al. A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Commun. 1998;248: 584–90. doi: 10.1006/bbrc.1998.8831 9703970

28. Watanabe H, Fujisawa T, Holstein TW. Cnidarians and the evolutionary origin of the nervous system. Dev Growth Differ. 2009;51: 167–83. doi: 10.1111/j.1440-169X.2009.01103.x 19379274

29. Anctil M. Chemical transmission in the sea anemone Nematostella vectensis: A genomic perspective. Comp Biochem Physiol Part D Genomics Proteomics. Elsevier Inc.; 2009;4: 268–89. doi: 10.1016/j.cbd.2009.07.001 20403752

30. Hand C, Uhlinger KR. The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull. 1992;182: 169–176. doi: 10.2307/1542110 29303672

31. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science. 2007;317: 86–94. doi: 10.1126/science.1139158 17615350

32. Grimmelikhuijzen CJ, Rinehart KL, Spencer AN. Isolation of the neuropeptide less than Glu-Trp-Leu-Lys-Gly-Arg-Phe-NH2 (Pol-RFamide II) from the hydromedusa Polyorchis penicillatus. Biochem Biophys Res Commun. 1992;183: 375–82. doi: 10.1016/0006-291x(92)90491-3 1550547

33. Darmer D, Schmutzler C, Diekhoff D, Grimmelikhuijzen CJ. Primary structure of the precursor for the sea anemone neuropeptide Antho-RFamide (less than Glu-Gly-Arg-Phe-NH2). Proc Natl Acad Sci U S A. 1991;88: 2555–9. doi: 10.1073/pnas.88.6.2555 1706527

34. Leviev I, Grimmelikhuijzen CJ. Molecular cloning of a preprohormone from sea anemones containing numerous copies of a metamorphosis-inducing neuropeptide: a likely role for dipeptidyl aminopeptidase in neuropeptide precursor processing. Proc Natl Acad Sci U S A. 1995;92: 11647–51. doi: 10.1073/pnas.92.25.11647 8524821

35. Moosler A, Rinehart KL, Grimmelikhuijzen CJ. Isolation of four novel neuropeptides, the hydra-RFamides I-IV, from Hydra magnipapillata. Biochem Biophys Res Commun. 1996;229: 596–602. doi: 10.1006/bbrc.1996.1849 8954943

36. Darmer D, Hauser F, Nothacker HP, Bosch TC, Williamson M, Grimmelikhuijzen CJ. Three different prohormones yield a variety of Hydra-RFamide (Arg-Phe-NH2) neuropeptides in Hydra magnipapillata. Biochem J. 1998;332 (Pt 2: 403–12. doi: 10.1042/bj3320403 9601069

37. Hayakawa E, Takahashi T, Nishimiya-Fujisawa C, Fujisawa T. A novel neuropeptide (FRamide) family identified by a peptidomic approach in Hydra magnipapillata. FEBS J. 2007;274: 5438–48. doi: 10.1111/j.1742-4658.2007.06071.x 17894820

38. Gajewski M, Leitz T, Schloßherr J, Plickert G. LWamides from Cnidaria constitute a novel family of neuropeptides with morphogenetic activity. Roux’s Arch Dev Biol. 1996;205: 232–242. doi: 10.1007/BF00365801 28306026

39. Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TC, Kobayakawa Y, et al. A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development. 2000;127: 997–1005. doi: 10.1016/S1095-6433(99)90367-7 10662639

40. Zhou A, Webb G, Zhu X, Steiner DF. Proteolytic processing in the secretory pathway. J Biol Chem. 1999;274: 20745–8. doi: 10.1074/jbc.274.30.20745 10409610

41. Fälth M, Sköld K, Svensson M, Nilsson A, Fenyö D, Andren PE. Neuropeptidomics strategies for specific and sensitive identification of endogenous peptides. Mol Cell Proteomics. 2007;6: 1188–97. doi: 10.1074/mcp.M700016-MCP200 17401030

42. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8: 785–6. doi: 10.1038/nmeth.1701 21959131

43. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, et al. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol. 2009;330: 186–99. doi: 10.1016/j.ydbio.2009.02.004 19217898

44. Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, et al. Unexpected complexity of the Wnt gene family in a sea anemone. Nature. 2005;433: 156–60. doi: 10.1038/nature03158 15650739

45. Yum S, Takahashi T, Hatta M, Fujisawa T. The structure and expression of a preprohormone of a neuropeptide, Hym-176 in Hydra magnipapillata. FEBS Lett. 1998;439: 31–4. doi: 10.1016/s0014-5793(98)01314-3 9849871

46. Schmutzler C, Darmer D, Diekhoff D, Grimmelikhuijzen CJ. Identification of a novel type of processing sites in the precursor for the sea anemone neuropeptide Antho-RFamide (<Glu-Gly-Arg-Phe-NH2) from Anthopleura elegantissima. J Biol Chem. 1992;267: 22534–41. Available: http://www.ncbi.nlm.nih.gov/pubmed/1429603 1429603

47. Reinscheid RK, Grimmelikhuijzen CJ. Primary structure of the precursor for the anthozoan neuropeptide antho-RFamide from Renilla köllikeri: evidence for unusual processing enzymes. J Neurochem. 1994;62: 1214–22. doi: 10.1046/j.1471-4159.1994.62031214.x 7906718

48. Lundquist CT, Clottens FL, Holman GM, Nichols R, Nachman RJ, Nässel DR. Callitachykinin I and II, two novel myotropic peptides isolated from the blowfly, Calliphora vomitoria, that have resemblances to tachykinins. Peptides. 1994;15: 761–8. doi: 10.1016/0196-9781(94)90027-2 7984492

49. Neupert S, Russell WK, Russell DH, López JD, Predel R, Nachman RJ. Neuropeptides in Heteroptera: identification of allatotropin-related peptide and tachykinin-related peptides using MALDI-TOF mass spectrometry. Peptides. 2009;30: 483–8. doi: 10.1016/j.peptides.2008.11.009 19084564

50. Anastasi A, Erspamer V. The isolation and amino acid sequence of eledoisin, the active endecapeptide of the posterior salivary glands of Eledone. Arch Biochem Biophys. 1963;101: 56–65. doi: 10.1016/0003-9861(63)90533-2 14012712

51. Chiwakata C, Brackmann B, Hunt N, Davidoff M, Schulze W, Ivell R. Tachykinin (substance-P) gene expression in Leydig cells of the human and mouse testis. Endocrinology. 1991;128: 2441–8. doi: 10.1210/endo-128-5-2441 1708336

52. Veenstra JA. Neuropeptide evolution: neurohormones and neuropeptides predicted from the genomes of Capitella teleta and Helobdella robusta. Gen Comp Endocrinol. 2011;171: 160–75. doi: 10.1016/j.ygcen.2011.01.005 21241702

53. Sato Y, Oguchi M, Menjo N, Imai K, Saito H, Ikeda M, et al. Precursor polyprotein for multiple neuropeptides secreted from the suboesophageal ganglion of the silkworm Bombyx mori: characterization of the cDNA encoding the diapause hormone precursor and identification of additional peptides. Proc Natl Acad Sci U S A. 1993;90: 3251–5. doi: 10.1073/pnas.90.8.3251 8475067

54. Duportets L, Gadenne C, Couillaud F. A cDNA, from Agrotis ipsilon that encodes the pheromone biosynthesis activating neuropeptide (PBAN) and other FXPRL peptides. Peptides. 1999;20: 899–905. doi: 10.1016/s0196-9781(99)00079-0 10503766

55. Hauser F, Williamson M, Cazzamali G, Grimmelikhuijzen CJP. Identifying neuropeptide and protein hormone receptors in Drosophila melanogaster by exploiting genomic data. Brief Funct Genomic Proteomic. 2006;4: 321–30. doi: 10.1093/bfgp/eli003 17202123

56. Mori K, Miyazato M, Ida T, Murakami N, Serino R, Ueta Y, et al. Identification of neuromedin S and its possible role in the mammalian circadian oscillator system. EMBO J. 2005;24: 325–35. doi: 10.1038/sj.emboj.7600526 15635449

57. Brighton PJ, Szekeres PG, Willars GB. Neuromedin U and its receptors: structure, function, and physiological roles. Pharmacol Rev. 2004;56: 231–48. doi: 10.1124/pr.56.2.3 15169928

58. Williamson M, Lenz C, Winther AM, Nässel DR, Grimmelikhuijzen CJ, Winther ME. Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin preprohormone from Drosophila melanogaster. Biochem Biophys Res Commun. 2001;281: 544–50. doi: 10.1006/bbrc.2001.4402 11181081

59. Yamanaka N, Hua Y-J, Roller L, Spalovská-Valachová I, Mizoguchi A, Kataoka H, et al. Bombyx prothoracicostatic peptides activate the sex peptide receptor to regulate ecdysteroid biosynthesis. Proc Natl Acad Sci U S A. 2010;107: 2060–5. doi: 10.1073/pnas.0907471107 20133850

60. Schoofs L, Holman GM, Hayes TK, Nachman RJ, De Loof A. Isolation, identification and synthesis of locustamyoinhibiting peptide (LOM-MIP), a novel biologically active neuropeptide from Locusta migratoria. Regul Pept. 1991;36: 111–9. Available: doi: 10.1016/0167-0115(91)90199-q 1796179

61. Fu Q, Tang LS, Marder E, Li L. Mass spectrometric characterization and physiological actions of VPNDWAHFRGSWamide, a novel B type allatostatin in the crab, Cancer borealis. J Neurochem. 2007;101: 1099–107. doi: 10.1111/j.1471-4159.2007.04482.x 17394556

62. Moroz LL, Edwards JR, Puthanveettil S V., Kohn AB, Ha T, Heyland A, et al. Neuronal transcriptome of Aplysia: Neuronal compartments and circuitry. Cell. 2006;127: 1453–1467. doi: 10.1016/j.cell.2006.09.052 17190607

63. Ahn S-J, Martin R, Rao S, Choi M-Y. Neuropeptides predicted from the transcriptome analysis of the gray garden slug Deroceras reticulatum. Peptides. 2017;93: 51–65. doi: 10.1016/j.peptides.2017.05.005 28502716

64. Conzelmann M, Williams EA, Tunaru S, Randel N, Shahidi R, Asadulina A, et al. Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. Proc Natl Acad Sci U S A. 2013;110: 8224–9. doi: 10.1073/pnas.1220285110 23569279

65. Predel R, Nachman RJ, Gäde G. Myostimulatory neuropeptides in cockroaches: structures, distribution, pharmacological activities, and mimetic analogs. J Insect Physiol. 2001;47: 311–24. doi: 10.1016/s0022-1910(00)00129-3 11166295

66. Clynen E, Schoofs L. Peptidomic survey of the locust neuroendocrine system. Insect Biochem Mol Biol. 2009;39: 491–507. doi: 10.1016/j.ibmb.2009.06.001 19524670

67. Lorenz MW, Kellner R, Hoffmann KH. A family of neuropeptides that inhibit juvenile hormone biosynthesis in the cricket, Gryllus bimaculatus. J Biol Chem. 1995;270: 21103–8. doi: 10.1074/jbc.270.36.21103 7673141

68. Jang Y-H, Chae H-S, Kim Y-J. Female-specific myoinhibitory peptide neurons regulate mating receptivity in Drosophila melanogaster. Nat Commun. 2017;8: 1630. doi: 10.1038/s41467-017-01794-9 29158481

69. Oh Y, Yoon S-E, Zhang Q, Chae H-S, Daubnerová I, Shafer OT, et al. A homeostatic sleep-stabilizing pathway in Drosophila composed of the sex peptide receptor and its ligand, the myoinhibitory peptide. PLoS Biol. 2014;12: e1001974. doi: 10.1371/journal.pbio.1001974 25333796

70. Peymen K, Watteyne J, Borghgraef C, Van Sinay E, Beets I, Schoofs L. Myoinhibitory peptide signaling modulates aversive gustatory learning in Caenorhabditis elegans. PLoS Genet. 2019;15: e1007945. doi: 10.1371/journal.pgen.1007945 30779740

71. Marlow HQ, Srivastava M, Matus DQ, Rokhsar D, Martindale MQ. Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev Neurobiol. 2009;69: 235–54. doi: 10.1002/dneu.20698 19170043

72. Koizumi O. Nerve ring of the hypostome in Hydra: is it an origin of the central nervous system of bilaterian animals? Brain Behav Evol. 2007;69: 151–9. doi: 10.1159/000095204 17230023

73. Watanabe H, Kuhn A, Fushiki M, Agata K, Özbek S, Fujisawa T, et al. Sequential actions of β-catenin and Bmp pattern the oral nerve net in Nematostella vectensis. Nat Commun. 2014;5: 5536. doi: 10.1038/ncomms6536 25534229

74. Petruzziello F, Fouillen L, Wadensten H, Kretz R, Andren PE, Rainer G, et al. Extensive characterization of Tupaia belangeri neuropeptidome using an integrated mass spectrometric approach. J Proteome Res. 2012;11: 886–96. doi: 10.1021/pr200709j 22070463

75. Zhang X, Petruzziello F, Zani F, Fouillen L, Andren PE, Solinas G, et al. High identification rates of endogenous neuropeptides from mouse brain. J Proteome Res. 2012;11: 2819–27. doi: 10.1021/pr3001699 22424378

76. Sasaki K, Osaki T, Minamino N. Large-scale identification of endogenous secretory peptides using electron transfer dissociation mass spectrometry. Mol Cell Proteomics. 2013;12: 700–9. doi: 10.1074/mcp.M112.017400 23250050

77. Southey BR, Amare A, Zimmerman T a, Rodriguez-Zas SL, 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: W267–72. doi: 10.1093/nar/gkl161 16845008

78. Darmer D, Hauser F, Nothacker HP, Bosch TC, Williamson M, Grimmelikhuijzen CJ. Three different prohormones yield a variety of Hydra-RFamide (Arg-Phe-NH2) neuropeptides in Hydra magnipapillata. Biochem J. 1998;332 (Pt 2: 403–12. doi: 10.1042/bj3320403 9601069

79. Zhang X, Pan H, Peng B, Steiner DF, Pintar JE, Fricker LD. Neuropeptidomic analysis establishes a major role for prohormone convertase-2 in neuropeptide biosynthesis. J Neurochem. 2010;112: 1168–79. doi: 10.1111/j.1471-4159.2009.06530.x 19968759

80. Lim J, Berezniuk I, Che F-Y, Parikh R, Biswas R, Pan H, et al. Altered neuropeptide processing in prefrontal cortex of Cpe (fat/fat) mice: implications for neuropeptide discovery. J Neurochem. 2006;96: 1169–81. doi: 10.1111/j.1471-4159.2005.03614.x 16417576

81. Hoshino A, Lindberg I. Peptide Biosynthesis: Prohormone Convertases 1/3 and 2. Colloq Ser Neuropeptides. 2012;1: 1–112. doi: 10.4199/C00050ED1V01Y201112NPE001

82. Boonen K, Baggerman G, D’Hertog W, Husson SJ, Overbergh L, Mathieu C, et al. Neuropeptides of the islets of Langerhans: a peptidomics study. Gen Comp Endocrinol. 152: 231–41. doi: 10.1016/j.ygcen.2007.05.002 17559849

83. Van Camp KA, Baggerman G, Blust R, Husson SJ. Neuropeptidomic analysis of zebrafish brain. Methods Mol Biol. 2018;1719: 241–246. doi: 10.1007/978-1-4939-7537-2_16 29476516

84. Leung PS, Shaw C, Maule AG, Thim L, Johnston CF, Irvine GB. The primary structure of neuropeptide F (NPF) from the garden snail, Helix aspersa. Regul Pept. 1992;41: 71–81. doi: 10.1016/0167-0115(92)90515-v 1472263

85. Brown MR, Crim JW, Arata RC, Cai HN, Chun C, Shen P. Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family. Peptides. 1999;20: 1035–42. doi: 10.1016/s0196-9781(99)00097-2 10499420

86. Cupo A, Proux J. Biochemical characterization of a vasopressin-like neuropeptide in Locusta migratoria. Evidence of high molecular weight protein encoding vasopressin sequence. Neuropeptides. 1983;3: 309–18. doi: 10.1016/0143-4179(83)90048-3 6866218

87. Cruz LJ, de Santos V, Zafaralla GC, Ramilo CA, Zeikus R, Gray WR, et al. Invertebrate vasopressin/oxytocin homologs. Characterization of peptides from Conus geographus and Conus straitus venoms. J Biol Chem. 1987;262: 15821–4. 3680228

88. Schoofs L, Danger JM, Jegou S, Pelletier G, Huybrechts R, Vaudry H, et al. NPY-like peptides occur in the nervous system and midgut of the migratory locust, Locusta migratoria and in the brain of the grey fleshfly, Sarcophaga bullata. Peptides. 9: 1027–36. doi: 10.1016/0196-9781(88)90084-8 3244556

89. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science. 2007;317: 86–94. doi: 10.1126/science.1139158 17615350

90. Jékely G. Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci U S A. 2013;110: 8702–7. doi: 10.1073/pnas.1221833110 23637342

91. Mirabeau O, Joly J-S. Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci U S A. 2013;110: E2028–37. doi: 10.1073/pnas.1219956110 23671109

A combined strategy of neuropeptide prediction and tandem mass spectrometry identifies evolutionarily conserved ancient neuropeptides in the sea anemone Nematostella vectensis

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Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

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