Discovery by proteogenomics and characterization of an RF-amide neuropeptide from cone snail venom

Journal of Proteomics

Volumn 114, Issue , 2015, Pages 38-47

  Robinson, Samuel D ^a   Safavi Hemami, Helena ^b   Raghuraman, Shrinivasan ^b   Imperial, Julita S ^b   Papenfuss, Anthony T ^c   Teichert, Russell W ^b   Purcell, Anthony W ^d   Olivera, Baldomero M ^b   Norton, Raymond S ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF UTAH   (United States)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Calcium imaging; Conotoxin; Neuropeptide; Proteogenomics; RF amide; Venom

Indexed keywords

CALCIUM; CONOTOXIN; CYSTEINE; NEUROHORMONE; NEUROPEPTIDE; RF AMIDE NEUROPEPTIDE; SNAIL VENOM; UNCLASSIFIED DRUG; CONORFAMIDE; MOLLUSC VENOM;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENOMICS; MARINE SNAIL; MOUSE; NERVE CELL; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEOGENOMICS; PROTEOMICS; PROTON NUCLEAR MAGNETIC RESONANCE; SPINAL GANGLION; TANDEM MASS SPECTROMETRY; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CONUS (SNAIL); CYTOLOGY; DRUG EFFECTS; GENETIC ASSOCIATION STUDY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; PROCEDURES;

GASTROPODA;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CONOTOXINS; CONUS SNAIL; GENETIC ASSOCIATION STUDIES; GENOMICS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MOLLUSK VENOMS; NEURONS; NEUROPEPTIDES; PROTEOMICS;

EID: 84911905927     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.11.003     Document Type: Article

References (39)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
2. Yates J.R., Eng J.K., McCormack A.L. Mining genomes: correlating tandem mass spectra of modified and unmodified peptides to sequences in nucleotide databases. Anal Chem 1995, 67:3202-3210.
3. Ansong C., Purvine S.O., Adkins J.N., Lipton M.S., Smith R.D. Proteogenomics: needs and roles to be filled by proteomics in genome annotation. Brief Funct Genomic Proteomic 2008, 7:50-62.
4. Terlau H., Olivera B.M. Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol Rev 2004, 84:41-68.
5. Lewis R.J., Dutertre S., Vetter I., Christie M.J. Conus venom peptide pharmacology. Pharmacol Rev 2012, 64:259-298.
6. Norton R.S., Olivera B.M. Conotoxins down under. Toxicon 2006, 48:780-798.
7. Robinson S.D., Safavi-Hemami H., McIntosh L.D., Purcell A.W., Norton R.S., Papenfuss A.T. Diversity of conotoxin gene superfamilies in the venomous snail, Conus victoriae. PLoS One 2014, 9:e87648.
8. Walker R., Papaioannou S., Holden-Dye L. A review of FMRFamide- and RFamide-like peptides in metazoa. Invertebr Neurosci 2009, 9:111-153.
9. Chevreux B., Pfisterer T., Drescher B., Driesel A.J., Müller W.E.G., Wetter T., et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 2004, 14:1147-1159.
10. 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.
11. Hopkins C., Grilley M., Miller C., Shon K.-J., Cruz L.J., Gray W.R., et al. A new family of Conus peptides targeted to the nicotinic acetylcholine receptor. J Biol Chem 1995, 270:22361-22367.
12. Zhang M.M., Wilson M.J., Gajewiak J., Rivier J.E., Bulaj G., Olivera B.M., et al. Pharmacological fractionation of tetrodotoxin-sensitive sodium currents in rat dorsal root ganglion neurons by μ-conotoxins. Br J Pharmacol 2013, 169:102-114.
13. McIntosh J.M., Yoshikami D., Mahe E., Nielsen D.B., Rivier J.E., Gray W.R., et al. A nicotinic acetylcholine receptor ligand of unique specificity, alpha-conotoxin ImI. J. Biol. Chem. 1994, 269:16733-16739.
14. Raghuraman S., Garcia A.J., Anderson T.M., Twede V.D., Curtice K.J., Chase K., et al. Defining modulatory inputs into CNS neuronal subclasses by functional pharmacological profiling. Proc Natl Acad Sci U S A 2014, 111:6449-6454.
15. Teichert R.W., Smith N.J., Raghuraman S., Yoshikami D., Light A.R., Olivera B.M. Functional profiling of neurons through cellular neuropharmacology. Proc Natl Acad Sci U S A 2012, 109:1388-1395.
16. Maillo M., Aguilar M.B., Lopéz-Vera E., Craig A.G., Bulaj G., Olivera B.M., et al. Conorfamide, a Conus venom peptide belonging to the RFamide family of neuropeptides. Toxicon 2002, 40:401-407.
17. Aguilar M.B., Luna-Ramírez K.S., Echeverría D., Falcón A., Olivera B.M., Heimer de la Cotera E.P., et al. Conorfamide-Sr2, a gamma-carboxyglutamate-containing FMRFamide-related peptide from the venom of Conus spurius with activity in mice and mollusks. Peptides 2008, 29:186-195.
18. Woodward S.R., Cruz L.J., Olivera B.M., Hillyard D.R. Constant and hypervariable regions in conotoxin propeptides. EMBO J 1990, 9:1015-1020.
19. Sandall D.W., Satkunanathan N., Keays D.A., Polidano M.A., Liping X., Pham V., et al. A novel α-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo. Biochemistry 2003, 42:6904-6911.
20. Kaas Q., Westermann J.C., Craik D.J. Conopeptide characterization and classifications: an analysis using ConoServer. Toxicon 2010, 55:1491-1509.
21. Dutertre S., A-H Jin, Kaas Q., Jones A., Alewood P.F., Lewis R.J. Deep venomics reveals the mechanism for expanded peptide diversity in cone snail venom. Mol Cell Proteomics 2012, 12:312-329.
22. 15N random coil NMR chemical shifts of the common amino acids: investigations of nearest-neighbor effects. J Biomol NMR 1995, 5:67-81.
23. Teichert R.W., Raghuraman S., Memon T., Cox J.L., Foulkes T., Rivier J.E., et al. Characterization of two neuronal subclasses through constellation pharmacology. Proc Natl Acad Sci U S A 2012, 109:12758-12763.
24. Teichert R.W., Memon T., Aman J.W., Olivera B.M. Using constellation pharmacology to define comprehensively a somatosensory neuronal subclass. Proc Natl Acad Sci U S A 2014, 111:2319-2324.
25. Findeisen M., Rathmann D., Beck-Sickinger A.G. RFamide peptides: structure, function, mechanisms and pharmaceutical potential. Pharmaceuticals 2011, 4:1248-1280.
26. Perry S.J., Yi-Kung Huang E., Cronk D., Bagust J., Sharma R., Walker R.J., et al. A human gene encoding morphine modulating peptides related to NPFF and FMRFamide. FEBS Lett 1997, 409:426-430.
27. Hinuma S., Habata Y., Fujii R., Kawamata Yuji, Hosoya M., Fukusumi S., et al. A prolactin-releasing peptide in the brain. Nature 1998, 393:272-276.
28. Hinuma S., Shintani Y., Fukusumi S., Iijima N., Matsumoto Y., Hosoya M., et al. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2000, 2:703-708.
29. Chartrel N., Dujardin C., Anouar Y., Leprince J., Decker A., Clerens S., et al. Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc Natl Acad Sci U S A 2003, 100:15247-15252.
30. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.-M., Le Poul E., et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001, 276:34631-34636.
31. Bonini J.A., Jones K.A., Adham N., Forray C., Artymyshyn R., Durkin M.M., et al. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J Biol Chem 2000, 275:39324-39331.
32. Elshourbagy N.A., Ames R.S., Fitzgerald L.R., Foley J.J., Chambers J.K., Szekeres P.G., et al. Receptor for the pain modulatory neuropeptides FF and AF is an orphan G protein-coupled receptor. J Biol Chem 2000, 275:25965-25971.
33. Jiang Y., Luo L., Gustafson E.L., Yadav D., Laverty M., Murgolo N., et al. Identification and characterization of a novel RF-amide peptide ligand for orphan G-protein-coupled receptor SP9155. J Biol Chem 2003, 278:27652-27657.
34. Askwith C.C., Cheng C., Ikuma M., Benson C., Price M.P., Welsh M.J. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 2000, 26:133-141.
35. Lingueglia E., Champigny G., Lazdunski M., Barbry P. Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature 1995, 378:730-733.
36. Sherwood N.M., Krueckl S.L., McRory J.E. The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr Rev 2000, 21:619-670.
37. Parker D.S., Raufman J.P., O'Donohue T.L., Bledsoe M., Yoshida H., Pisano J.J. Amino acid sequences of helospectins, new members of the glucagon superfamily, found in Gila monster venom. J Biol Chem 1984, 259:11751-11755.
38. Eng J., Kleinman W.A., Singh L., Singh G., Raufman J.P. Isolation and characterization of exendin-4, an exendin-3 analogue, from Heloderma suspectum venom. Further evidence for an exendin receptor on dispersed acini from guinea pig pancreas. J Biol Chem 1992, 267:7402-7405.
39. Eng J., Andrews P.C., Kleinman W.A., Singh L., Raufman J.P. Purification and structure of exendin-3, a new pancreatic secretagogue isolated from Heloderma horridum venom. J Biol Chem 1990, 265:20259-20262.