Probing peptide libraries from Conus achatinus using mass spectrometry and cDNA sequencing: Identification of δ and ω-conotoxins

Journal of Mass Spectrometry

Volumn 43, Issue 6, 2008, Pages 791-805

  Gowd, Konkallu Hanumae ^a   Dewan, Kalyan Kumar ^b   Iengar, Prathima ^b   Krishnan, Kozhalmannom S ^a,c   Balaram, Padmanabhan ^b  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

cDNA library; Conus peptide library; MALDI MS; MALDI MS MS; RT PCR

Indexed keywords

CLASSIFICATION (OF INFORMATION); DESORPTION; FORECASTING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH PRESSURE LIQUID CHROMATOGRAPHY; IONIZATION; LASERS; LIBRARIES; MASS SPECTROMETERS; MASS SPECTROMETRY; MATRIX ALGEBRA; PEPTIDES; POLYPEPTIDES; PROTEINS; PULSED LASER DEPOSITION; SPECTROMETERS; SPECTROMETRY; SPECTRUM ANALYSIS;

C TERMINUS; CONOTOXINS; CYS RESIDUES; DISULFIDE BONDS; INDIVIDUAL COMPONENTS; MALDI-MS; MATRIX-ASSISTED LASER DESORPTION/IONIZATION (MALDI) MASS SPECTROMETRY; MATRIX-ASSISTED LASER-DESORPTION/IONIZATION (MALDI); PEPTIDE LIBRARIES; PEPTIDE MIXTURES; PEPTIDE SEQUENCING; PROLINE (PRO); RETENTION TIMES; REVERSE-PHASE HPLC (RP-HPLC); SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY (MS/MS); TRYPSIN DIGESTION;

AMINES;

COMPLEMENTARY DNA; CYSTEINE; DELTA CONOTOXIN; MARINE TOXIN; OMEGA CONOTOXIN; PEPTIDE LIBRARY; TRYPSIN;

ALKYLATION; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; DNA SEQUENCE; MARINE SNAIL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REDUCTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CONOTOXINS; CONUS SNAIL; DNA, COMPLEMENTARY; MOLECULAR SEQUENCE DATA; OMEGA-CONOTOXINS; PEPTIDE LIBRARY; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

GASTROPODA;

EID: 46849122906     PISSN: 10765174     EISSN: 10969888     Source Type: Journal    
DOI: 10.1002/jms.1377     Document Type: Article

References (51)

1. Biemann K. Mass spectrometry of peptides and proteins. Annual Review of Biochemistry 1992; 61: 977.
2. McLafferty FW, Fridriksson EK, Horn DM, Lewis MA, Zubarev RA. Biomolecule mass spectrometry. Science 1999; 284: 1289.
3. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 2003; 422: 198.
4. Domon B, Aebersold R. Mass spectrometry and protein analysis. Science 2006; 312: 212.
5. Quinton L, Demeure K, Dobson R, Gilles N, Gabelica V, Pauw ED. New method for characterizing highly disulfide-bridged peptides in complex mixtures: application to toxin identification from crude venoms. Journal of Proteome Research 2007; 6: 3216.
6. Jakubowski JA, Sweedler JV. Sequencing and mass profiling highly modified conotoxins using global reduction/alkylation followed by mass spectrometry. Analytical Chemistry 2004; 76: 6541.
7. Neitz S, Jurgens M, Kellmann M, Schulz-Knappe P, Schrader M. Screening for disulfide-rich peptides in biological sources by carboxyamidomethylation in combination with differential matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Communications in Mass Spectrometry 2001; 15: 1586.
8. Legros C, Celerier ML, Henry M, Guette C. Nanospray analysis of the venom of the tarantula Theraphosa leblondi: a powerful method for direct venom mass fingerprinting and toxin sequencing. Rapid Communications in Mass Spectrometry 2004; 18: 1024.
9. Jakubowski JA, Keays DA, Kelley WP, Sandall DW, Bingham JP, Livett BG, Gayler KR, Sweedler JV. Determining sequences and post-translational modifications of novel conotoxins in Conus victoriae using cDNA sequencing and mass spectrometry. Journal of Mass Spectrometry 2004; 39: 548.
10. Jakubowski JA, Kelley WP, Sweedler JV. Screening for post-translational modifications in conotoxins using liquid chromatography/mass spectrometry: an important component of conotoxin discovery. Toxicon 2006; 47: 688.
11. Terlau H, Olivera BM. Conus venoms: a rich source of novel ion channel- targeted peptides. Physiological Reviews 2004; 84: 41.
12. Olivera BM, Hillyard DR, Marsh M, Yoshikami D. Combinatorial peptide libraries in drug design: lessons from venomous cone snails. Trends in Biotechnology 1995; 13: 422.
13. Myers RA, Cruz LJ, Rivier JE, Olivera BM. Conus peptides as chemical probes for receptors and ion channels. Chemical Reviews 1993; 93: 1923.
14. Olivera BM, Rivier J, Clark C, Ramilo CA, Corpuz GP, Abogadie FC, Mena EE, Woodward SR, Hillyard DR, Cruz LJ. Diversity of Conus neuropeptides. Science 1990; 249: 257.
15. Olivera BM. Conus venom peptides, receptor and ion channel targets and drug design: 50 million years of neuropharmacology (EE Just Lecture, 1996). Molecular Biology of the Cell 1997; 8: 2101.
16. Sudarslal S, Majumdar S, Ramasamy P, Dhawan R, Pal PP, Ramaswami M, Lala AK, Sikdar SK, Sarma SP, Krishnan KS, Balaram P. Sodium channel modulating activity in a δ-conotoxin from an Indian marine snail. FEBS Letters 2003; 553: 209.
17. Sudarslal S, Singaravadivelan G, Ramasamy P, Ananda K, Sarma SP, Sikdar SK, Krishnan KS, Balaram P. A novel 13 residue acyclic peptide from the marine snail, Conus monile, targets potassium channels. Biochemical and Biophysical Research Communications 2004; 317: 682.
18. Gowd KH, Sabareesh V, Sudarslal S, Iengar P, Franklin B, Fernando A, Dewan K, Ramaswami M, Sarma SP, Sikdar SK, Balaram P, Krishnan KS. Novel peptides of therapeutic promise from Indian conidae. Annals of the New York Academy of Sciences 2005; 1056: 462.
19. Sabareesh V, Gowd KH, Ramasamy P, Sudarslal S, Krishnan KS, Sikdar SK, Balaram P. Characterization of contryphans from Conus loroisii and Conus amadis that target calcium channels. Peptides 2006; 27: 2647.
20. Mandal AK, Ramasamy MR, Sabareesh V, Openshaw ME, Krishnan KS, Balaram P. Sequencing of T-superfamily conotoxins from Conus virgo: pyroglutamic acid identification and disulfide arrangement by MALDI mass spectrometry. Journal of the American Society for Mass Spectrometry 2007; 18: 1396.
21. Turner RJ, Freeman SE. Factors affecting the muscle depolarization due to Conus achatinus toxin. Toxicon 1974; 12: 49.
22. Liu L, Chew G, Hawrot E, Chi C, Wang C. Two potent α3/5 conotoxins from piscivorous Conus achatinus. Acta biochimica et biophysica Sinica (Shanghai) 2007; 39: 438.
23. Lu BS, Yu F, Zhao D, Huang PT, Huang CF. Conopeptides from Conus striatus and Conus textile by cDNA cloning. Peptides 1999; 20: 1139.
24. Kauferstein S, Melaun C, Mebs D. Direct cDNA cloning of novel conopeptides precursors of the O-superfamily. Peptides 2005; 26: 361.
25. Jiang H, Xu CQ, Wang CZ, Fan CX, Zhao TY, Chen JS, Chi CW. Two novel O-superfamily conotoxins from Conus vexillum. Toxicon 2006; 15: 425.
26. Luo S, Zhangsun D, Lin Q, Xie L, Wu Y, Zhu X. Sequence diversity of O-superfamily conopeptides from Conus marmoreus native to Hainan. Peptides 2006; 27: 3058.
27. Luo S, Zhangsun D, Feng J, Wu Y, Zhu X, Hu Y. Diversity of the O- superfamily conotoxins from Conus miles. Journal of Peptide Science 2007; 13: 44.
28. Chomczynski P, Sacchi N. Single step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 1987; 163: 156.
29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of Molecular Biology 1990; 215: 403.
30. Altschul SF, Madden TL, Schärfer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997; 25: 3389.
31. Thompson JD, Plewnial F, Thierry JC, Poch O. Rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acid Research 2000; 28: 2919.
32. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, Gasteiger E, Martin MJ, Michoud K, O'Donovan C, Phan I, Pilbout S, Schneider M. The swiss-prot protein knowledge base and its supplement TrEMBL. Nucleic Acids Research 2003; 31: 365.
33. Cohen SL, Chait BT. Influence of matrix solution conditions on the MALDI-MS analysis of peptides and proteins. Analytical Chemistry 1996; 68: 31.
34. Buczek O, Bulaj G, Olivera BM. Conotoxins and the posttranslational modification of secreted gene products. Cellular and Molecular Life Sciences 2005; 62: 3067.
35. Prigge ST, Mains RE, Eipper BA, Amzel LM. New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cellular and Molecular Life Sciences 2000; 57: 1236.
36. Biemann K. Sequencing of peptides by tandem mass spectrometry and high-energy collision-induced dissociation. Methods in Enzymology 1990; 193: 455.
37. Jakubowski JA, Kelley WP, Sweedler JV, Gilly WF, Schulz JR. Intraspecific variation of venom injected by fish-hunting Conus snails. Journal of Experimental Biology 2005; 208: 2873.
38. Bulaj G, DeLaCruz R, Azimi-Zonooz A, West P, Watkins M, Yoshikami D, Olivera BM. δ-Conotoxin structure/function through a cladistic analysis. Biochemistry 2001; 40: 13201.
39. McCleskey EW, Fox AP, Feldman DH, Cruz LJ, Olivera BM, Tsien RW, Yoshikami D. ω-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proceedings of the National Academy of Sciences of the United States of America 1987; 84: 4327.
40. Hodgkin AL, Huxley AF. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. Journal of Physiology 1952; 116: 440.
41. Clay JR. Axonal excitability revisited. Progress in Biophysics and Molecular Biology 2005; 88: 59.
42. Terlau H, Schon KJ, Grilley M, Stocker M, Stuhmer W, Olivera BM. Strategy for rapid immobilization of prey by a fish-hunting marine snail. Nature 1996; 381: 148.
43. Leipold E, Hansel A, Olivera BM, Terlau H, Heinemann SH. Molecular interaction of δ-conotoxins with voltage-gated sodium channels. FEBS Letters 2005; 579: 3881.
44. 1B subunit controls reversibility of ω-conotoxin GVIA and MVIIA block. Journal of Biological Chemistry 2001; 276: 15728.
45. Olivera BM, Rivier J, Scott JK, Hillyard DR, Cruz LJ. Conotoxins. Journal of Biological Chemistry 1991; 266: 22067.
46. Kim J, Takahashi M, Ogura A, Kohno T, Kudo Y, Sato K. Hydroxyl group of Tyr13 is essential for the activity of ω-conotoxin GVIA, a peptide toxin for the N-type calcium channel. Journal of Biological Chemistry 1994; 269: 23876.
47. Flinn JP, Pallaghy PK, Lew M, Murphy R, Angus JA, Norton RS. Role of key functional groups in ω-conotoxin GVIA: synthesis structure and functional assay of selected peptide analogues. European Journal of Biochemistry 1999; 262: 447.
48. Price-Carter M, Gray WR, Goldenberg DP. Folding of ω-conotoxins. 2 influence of precursor sequences and protein disulfide isomerase. Biochemistry 1996; 35: 15547.
49. Chivian E, Roberts CM, Bernstein AS. The threat to cone snails. Science 2003; 302: 391.
50. Duda TF Jr, Bingham JP, Livett BG, Kohn AJ, Massilia GR, Schulz JR, Down J, Sandall D, Sweedler JV. How much at risk are cone snails? Science 2004; 303: 955.
51. Nelson L. Venomous snails: one slip, and you're dead. Nature 2004; 429: 798.