Identification and molecular characterization of three new K +-channel specific toxins from the Chinese scorpion Mesobuthus martensii Karsch revealing intronic number polymorphism and alternative splicing in duplicated genes

Peptides

Volumn 34, Issue 2, 2012, Pages 311-323

  Zeng, Xian Chun ^a   Zhang, Lei ^a   Nie, Yao ^a   Luo, Xuesong ^a  

^a CHINA UNIVERSITY OF GEOSCIENCES   (China)

Author keywords

KTx22; Alternative splicing; Genomic organization; Intron; K + channel specific toxins; Mesobuthus martensii Karsch; Scorpion

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL TOXIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; EXON; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE INSERTION; GENETIC ANALYSIS; GENETIC CODE; GENETIC POLYMORPHISM; INTRON; INTRONIC NUMBER POLYMORPHISM; MESOBUTHUS MARTENSII; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; SCORPION; SEQUENCE ANALYSIS; TRANSCRIPTOMICS;

5' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CHINA; CLONING, MOLECULAR; DNA COPY NUMBER VARIATIONS; EXONS; GENE LIBRARY; GENES, DUPLICATE; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; PEPTIDES; POTASSIUM CHANNEL BLOCKERS; PROTEIN ISOFORMS; SCORPION VENOMS; SCORPIONS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

MESOBUTHUS MARTENSII; SCORPIONES;

EID: 84862779036     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2011.12.012     Document Type: Article

References (71)

1. B. Billen, F. Bosmans, and J. Tytgat Animal peptides targeting voltage-activated sodium channels Curr Pharm Des 14 24 2008 2492 2502
2. T.S. Camargos, R. Restano-Cassulini, L.D. Possani, S. Peigneur, J. Tytgat, C.A. Schwartz, E.M. Alves, S.M. de Freitas, and E.F. Schwartz The new kappa-KTx 2 5 from the scorpion Opisthacanthus cayaporum Peptides 32 7 2011 1509 1517
3. C.I. Castillo-Davis, S.L. Mekhedov, D.L. Hartl, E.V. Koonin, and F.A. Kondrashov Selection for short introns in highly expressed genes Nat Genet 31 2002 415 418 (Pubitemid 35154453)
4. B.Y.W. Chung, C. Simons, A.E. Firth, C.M. Brown, and R.P. Hellens Effect of 5′UTR introns on gene expression in Arabidopsis thaliana BMC Genomics 7 2006 120
5. C.T. Cologna, S. Peigneur, J.C. Rosa, H.S. Selistre-de-Araujo, W.A. Varanda, J. Tytgat, and E.C. Arantes Purification and characterization of Ts15 the first member of a new α-KTX subfamily from the venom of the Brazilian scorpion Tityus serrulatus Toxicon 58 1 2011 54 61
6. G. Corzo, P. Escoubas, E. Villegas, K.J. Barnham, W. He, R.S. Norton, and T. Nakajima Characterization of unique amphipathic antimicrobial peptides from venom of the scorpion Pandinus imperator Biochem J 359 2001 35 45 (Pubitemid 32939205)
7. J. Coulombe-Huntington, and J. Majewski Characterization of intron loss events in mammals Genome Res 17 2007 23 32 (Pubitemid 46041662)
8. L. Dai, J.J. Wu, Y.H. Gu, Z.D. Lan, M.H. Ling, and C.W. Chi Genomic organization of three novel toxins from the scorpion Buthus martensi Karsch that are active on potassium channels Biochem J 346 2000 805 809 (Pubitemid 30171044)
9. A. Dabo, G. Golou, M.S. Traoré, N. Diarra, M. Goyffon, and O. Doumbo Scorpion envenoming in the North of Mali (West Africa): epidemiological, clinical and therapeutic aspects Toxicon 58 2 2011 154 158
10. M.L. Delabre, P. Pasero, M. Marilley, and P.E. Bougis Promoter structure and intron-exon organization of a scorpion alpha-toxin gene Biochemistry-US 34 1995 6729 6736
11. S. Dutertre, and R.J. Lewis Use of venom peptides to probe ion channel structure and function J Biol Chem 285 18 2010 13315 13320
12. G.P. Espino-Solis, G. Estrada, T. Olamendi-Portugal, E. Villegas, F. Zamudio, S. Cestele, L.D. Possani, and G. Corzo Isolation and molecular cloning of beta-neurotoxins from the venom of the scorpion Centruroides suffusus suffusus Toxicon 57 5 2011 739 746
13. S. Fan, Z. Sun, D. Jiang, C. Dai, Y. Ma, Z. Zhao, H. Liu, Y. Wu, Z. Cao, and W. Li BmKCT toxin inhibits glioma proliferation and tumor metastasis Cancer Lett 291 2 2010 158 166
14. O. Froy, T. Sagiv, M. Poreh, D. Urbach, N. Zilberberg, and M. Gurevitz Dynamic diversification from a putative common ancestor of scorpion toxins affecting sodium, potassium, and chloride channels J Mol Evol 48 2 1999 Feb 187 196 (Pubitemid 29066455)
15. B.I. García-Gómez, F.I. Coronas, R. Restano-Cassulini, R.R. Rodríguez, and L.D. Possani Biochemical and molecular characterization of the venom from the Cuban scorpion Rhopalurus junceus Toxicon 58 1 2011 18 27
16. B.I. García-Gómez, T.C. Olamendi-Portugal, J. Paniagua, J. van der Walt, K. Dyason, and L.D. Possani Heterologous expression of a gene that codes for Pg8, a scorpion toxin of Parabuthus granulatus, capable of generating protecting antibodies in mice Toxicon 53 7-8 2009 770 778
17. C. Goudet, C.W. Chi, and J. Tytgat An overview of toxins and genes from the venom of the Asian scorpion Buthus martensii Karsch Toxicon 40 2002 1239 1258 (Pubitemid 35239894)
18. S. Han, H. Yi, S.J. Yin, Z.Y. Chen, H. Liu, Z.J. Cao, Y.L. Wu, and W.X. Li Molecular basis of a potent peptide inhibitor designed for Kv1.3 channel, a therapeutic target of autoimmune disease J Biol Chem 283 2008 19058 19065
19. T.E. Heinen, and A.B. da Veiga Arthropod venoms and cancer Toxicon 57 15 March (4) 2011 497 511
20. C.A. Hernández-Aponte, J. Silva-Sanchez, V. Quintero- Hernández, A. Rodríguez-Romero, C. Balderas, L.D. Possani, and G.B. Gurrola Vejovine, a new antibiotic from the scorpion venom of Vaejovis mexicanus Toxicon 57 1 2011 84 92
21. H. Huang, and L.O. Trussell KCNQ5 channels control resting properties and release probability of a synapse Nat Neurosci 14 12 July (7) 2011 840 847
22. B. Jouirou, A. Mosbah, V. Visan, S. Grissmer, S. M'Barek, Z. Fajloun, J. Van Rietschoten, C. Devaux, H. Rochat, G. Lippens, M. El Ayeb, M. De Waard, K. Mabrouk, and J.M. Sabatier Cobatoxin 1 from Centruroides noxius scorpion venom: chemical synthesis, three-dimensional structure in solution, pharmacology and docking on K+ channels Biochem J 377 Pt (1) 2004 37 49 (Pubitemid 38114430)
23. P.D. Koeberle, Y. Wang, and L.C. Schlichter Kv1 1 and Kv1.3 channels contribute to the degeneration of retinal ganglion cells after optic nerve transection in vivo Cell Death Differ 17 1 2010 134 144
24. Y.V. Korolkova, S.A. Kozlov, A.V. Lipkin, K.A. Pluzhnikov, J.K. Hadley, and A.K. Filippov An ERG channel inhibitor from the scorpion Buthus eupeus J Biol Chem 276 2001 9868 9876
25. B.A. Knutson, and S. Hahn Yeast Rrn7 and human TAF1B are TFIIB-related RNA polymerase I general transcription factors Science 333 16 September (6049) 2011 1637 1640
26. C. Legros, E. Feyfant, F. Sampieri, H. Rochat, P.E. Bougis, and M.F. Martin-Eauclaire Influence of a NH2-terminal extension on the activity of KTX2, a K+ channel blocker purified from Androctonus australis scorpion venom FEBS Lett 417 1997 123 129 (Pubitemid 27490487)
27. Y. Ma, Y. Zhao, R. Zhao, W. Zhang, Y. He, Y. Wu, Z. Cao, L. Guo, and W. Li Molecular diversity of toxic components from the scorpion Heterometrus petersii venom revealed by proteomic and transcriptome analysis Proteomics 10 13 2010 2471 2485
28. +-channel blocker from scorpion venom Biochem Biophys Res Commun 360 2007 728 734 (Pubitemid 47077384)
29. C. McCloskey, S. Jones, S. Amisten, R.T. Snowden, L.K. Kaczmarek, D. Erlinge, A.H. Goodall, I.D. Forsythe, and M.P. Mahaut-Smith Kv1.3 is the exclusive voltage-gated K+ channel of platelets and megakaryocytes: roles in membrane potential Ca2+ signalling and platelet count J Physiol 588 Pt (9) 2010 1399 1406
30. A.R. Meki, and A.T. Nassar Rochat II A bradykinin-potentiating petide (peptide K12) isolated from the venom of Egyptian scorpion Buthus occitanus Peptides 16 1995 1359 1369
31. D. Morgenstern, B.H. Rohde, G.F. King, T. Tal, D. Sher, and E. Zlotkin The tale of a resting gland: transcriptome of a replete venom gland from the scorpion Hottentotta judaicus Toxicon 57 5 2011 695 703
32. G.M. Nicholson, A. Graudins, H.I. Wilson, M. Little, and K.W. Broady Arachnid toxicology in Australia: from clinical toxicology to potential applications Toxicon 48 2006 872 898 (Pubitemid 44738995)
33. K. Noble, R. Floyd, A. Shmygol, A. Shmygol, A. Mobasheri, and S. Wray Distribution, expression and functional effects of small conductance Ca-activated potassium (SK) channels in rat myometrium Cell Calcium 47 1 2010 47 54
34. R.S. Norton, and S.I. McDonough Peptides targeting voltage-gated calcium channels Curr Pharm Des 14 24 2008 2480 2491
35. A. Nott, S.H. Meislin, and M.J. Moore A quantitative analysis of intron effects on mammalian gene expression RNA 9 2003 607 617 (Pubitemid 36505458)
36. A. Peretz, L. Pell, Y. Gofman, Y. Haitin, L. Shamgar, E. Patrich, P. Kornilov, O. Gourgy-Hacohen, N. Ben-Tal, and B. Attali Targeting the voltage sensor of Kv7 2 voltage-gated K+ channels with a new gating-modifier Proc Natl Acad Sci USA 107 35 2010 15637 15642
37. A.M. Pimenta, R. Stocklin, P. Favreau, P.E. Bougis, and M.F. Martin-Eauclaire Moving pieces in a proteomic puzzle: mass fingerprinting of toxic fractions from the venom of Tityus serrulatus (Scorpiones Buthidae) Rapid Commun Mass Spectrom 15 2001 1562 1572 (Pubitemid 32834979)
38. V. Quintero-Hernández, E. Ortiz, M.R. Rendon, E.F. Schwartz, B. Becerril, G. Corzo, and L.D. Possani Scorpion and spider venom peptides: gene cloning and peptide expression Toxicon 58 8 2011 644 663
39. Q. Remijsen, F. Verdonck, and J. Willems Parabutoporin, a cationic amphipathic peptide from scorpion venom: much more than an antibiotic Toxicon 55 2-3 2010 180 185
40. I. Rjeibi, K. Mabrouk, H. Mosrati, C. Berenguer, H. Mejdoub, C. Villard, D. Laffitte, D. Bertin, L. Ouafik, J. Luis, M. Elayeb, and N. Srairi-Abid Purification, synthesis and characterization of AaCtx, the first chlorotoxin-like peptide from Androctonus australis scorpion venom Peptides 32 4 2011 656 663
41. +-channels Toxicon 43 2004 865 875 (Pubitemid 38781021)
42. R.C. Rodríguez de la Vega, E.F. Schwartz, and L.D. Possani Mining on scorpion venom biodiversity Toxicon 56 7 2010 1155 1161
43. R. Romi-Lebrun, B. Lebrun, M.F. Martin-Eauclaire, M. Ishiguro, P. Escoubas, F.Q. Wu, M. Hisada, O. Pongs, and T. Nakajima Purification, characterization, and synthesis of three novel toxins from the Chinese scorpion Buthus martensi, which act on K+ channels Biochemistry 36 4 November (44) 1997 13473 13482 (Pubitemid 27481593)
44. A.H. Rowe, Y. Xiao, J. Scales, K.D. Linse, M.P. Rowe, T.R. Cummins, and H.H. Zakon Isolation and characterization of CvIV4: a pain inducing α-scorpion toxin PLoS One 6 8 2011 e23520
45. E.F. Schwartz, E. Diego-Garcia, R.C. Rodríguez de la Vega, and L.D. Possani Transcriptome analysis of the venom gland of the Mexican scorpion Hadrurus gertschi (Arachnida: Scorpiones) BMC Genomics 8 2007 119 125
46. J.J. Smith, J.M. Hill, M.J. Little, G.M. Nicholson, G.F. King, and P.F. Alewood Unique scorpion toxin with a putative ancestral fold provides insight into evolution of the inhibitor cystine knot motif Proc Natl Acad Sci USA 108 26 2011 10478 10483
47. Z. Takacs, M. Toups, A. Kollewe, E. Johnson, L.G. Cuello, G. Driessens, M. Biancalana, A. Koide, C.G. Ponte, E. Perozo, T.F. Gajewski, G. Suarez-Kurtz, S. Koide, and S.A. Goldstein A designer ligand specific for Kv1.3 channels from a scorpion neurotoxin-based library Proc Natl Acad Sci USA 106 52 2009 Dec 29 22211 22216
48. Y. Takashima, T. Ohtsuka, A. González, H. Miyachi, and R. Kageyama Intronic delay is essential for oscillatory expression in the segmentation clock Proc Natl Acad Sci USA 108 8 2001 3301 3305
49. J. Tao, J. Shi, L. Yan, Y. Chen, Y.H. Duan, P. Ye, Q. Feng, J.W. Zhang, X.Q. Shu, and Y.H. Ji Enhancement effects of martentoxin on glioma BK channel and BK channel (α+β1) subtypes PLoS One 6 3 2011 e15896
50. C.A. Tegla, C. Cudrici, M. Rozycka, K. Soloviova, T. Ito, A.K. Singh, A. Khan, P. Azimzadeh, M. Andrian-Albescu, A. Khan, F. Niculescu, V. Rus, S.I. Judge, and H. Rus C5b-9-activated, K(v)1 3 channels mediate oligodendrocyte cell cycle activation and dedifferentiation Exp Mol Pathol 91 1 2011 335 345
51. R. Tuteja Type I signal peptidase: an overview Arch Biochem Biophys 441 2005 107 111 (Pubitemid 41557688)
52. J. Tytgat, K.G. Chandy, M.L. Garcia, G.A. Gutman, M.F. Martin-Eauclaire, and J.J. van der Walt A unified nomenclature for short-chain peptides isolated from scorpion venoms: alpha-KTx molecular subfamilies Trends Pharmacol Sci 20 1999 444 447 (Pubitemid 29528214)
53. N. Villalonga, M. David, J. Bielanska, R. Vicente, N. Comes, C. Valenzuela, and A. Felipe Immunomodulation of voltage-dependent K+ channels in macrophages: molecular and biophysical consequences J Gen Physiol 135 2 2010 135 147
54. Y. Wang, L. Wang, Y. Cui, Y.B. Song, Y.F. Liu, R. Zhang, C.F. Wu, and J.H. Zhang Purification, characterization and functional expression of a new peptide with an analgesic effect from Chinese scorpion Buthus martensii Karsch (BmK AGP-SYPU1) Biomed Chromatogr 25 7 2011 801 807
55. H.F. Wang, L. Feng, and D.K. Niu Relationship between mRNA stability and intron presence Biochem Res Commun 354 2007 203 208 (Pubitemid 46123220)
56. J. Wang, V. Yarov-Yarovoy, R. Kahn, D. Gordon, M. Gurevitz, T. Scheuer, and W.A. Catterall Mapping the receptor site for α-scorpion toxins on a Na+ channel voltage sensor Proc Natl Acad Sci USA 108 37 2011 15426 15431
57. H. Weinberger, Y. Moran, D. Gordon, M. Turkov, R. Kahn, and M. Gurevitz Positions under positive selection - key for selectivity and potency of scorpion α-toxins Mol Biol Evol 27 5 2010 1025 1034
58. X.C. Zeng, G. Corzo, and R. Hahin Scorpion venom peptides without disulfide bridges IUBMB Life 57 January (1) 2005 13 21 (Pubitemid 40637696)
59. X.C. Zeng, W.X. Li, F. Peng, and Z.H. Zhu Cloning and characterization of a novel cDNA sequence encoding the precursor of a navel venom peptide (Bmkbpp) related to a bradykinin-potentiating peptide from Chinese scorpion Buthus martensii Karsch IUBMB Life 49 2000 207 210 (Pubitemid 30350867)
60. X.C. Zeng, W.X. Li, S.X. Wang, S.Y. Zhu, and F. Luo Precursor of a novel scorpion venom peptide (BmKn1) with no disulfide bridge from Buthus martensii Karsch IUBMB Life 51 2001 117 120 (Pubitemid 32645809)
61. X.C. Zeng, W.X. Li, S.Y. Zhu, F. Peng, Z.H. Zhu, and H. Liu Molecular cloning and sequence analysis of cDNAs encoding a beta-toxin-like peptide and two MkTx I homologues from scorpion Buthus martensii Karsch Toxicon 39 2001 225 232
62. X.C. Zeng, W.X. Li, S.Y. Zhu, F. Peng, Z.H. Zhu, and K.L. Wu Cloning and characterization of a cDNA sequence encoding the precursor of a chlorotoxin-like peptide from the Chinese scorpion Buthus martensii Karsch Toxicon 38 2000 1009 1014 (Pubitemid 30116743)
63. X.C. Zeng, F. Luo, and W.X. Li Characterization of a novel cDNA encoding a short venom peptide derived from venom gland of scorpion Buthus martensii Karsch: trans-splicing may play an important role in the diversification of scorpion venom peptides Peptides 27 2006 675 681
64. X.C. Zeng, L. Feng, and W.X. Li Molecular dissection of venom from Chinese scorpion Mesobuthus martensii: identification and characterization of four novel disulfide-bridged venom peptides Peptides 27 7 2006 1745 1754
65. + channel toxins: a new subfamily of venom peptides (alpha-KTx-14) and genomic analysis of a member Biochimie 83 2001 883 889 (Pubitemid 33039799)
66. X.C. Zeng, S.X. Wang, and W.X. Li Identification of BmKAPi, a novel type of scorpion venom peptide with peculiar disulfide bridge pattern from Buthus martensii Karsch Toxicon 40 2002 1719 1722
67. X.C. Zeng, S. Wang, Y. Nie, L. Zhang, and X. Luo Characterization of BmKbpp, a multifunctional peptide from the Chinese scorpion Mesobuthus martensii Karsch: gaining insight into a new mechanism for the functional diversification of scorpion venom peptides Peptides 2011 10.1016/j.peptides.2011.11.012 http://www.sciencedirect.com/science/article/pii/S0196978111004840
68. X.C. Zeng, S.X. Wang, Y. Zhu, S.Y. Zhu, and W.X. Li Identification and functional characterization of novel scorpion venom peptides with no disulfide bridge from Buthus martenssi Karsch Peptides 25 2004 143 150 (Pubitemid 38520043)
69. Y. Zhao, X. Cai, T. Ye, J. Huo, C. Liu, S. Zhang, and P. Cao Analgesic-antitumor peptide inhibits proliferation and migration of SHG-44 human malignant glioma cells Cell Biochem 112 9 2011 2424 2434
70. K.F. Zoccal, S. Bitencourt Cda, A. Secatto, C.A. Sorgi, C. Bordon Kde, S.V. Sampaio, E.C. Arantes, and L.H. Faccioli Tityus serrulatus venom and toxins Ts1, Ts2 and Ts6 induce macrophage activation and production of immune mediators Toxicon 57 7-8 2011 1101 1108
71. S. Zhu, S. Peigneur, B. Gao, L. Luo, D. Jin, Y. Zhao, and J. Tytgat Molecular diversity and functional evolution of scorpion potassium channel toxins Mol Cell Proteomics 10 2 2011 M110