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Molecular evolution of toxin genes in Elapidae snakes

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Abstract

The venom of the sea krait, Laticauda semifasciata, consists primarily of two toxic proteins, phospholipase A2 (PLA2) and a three-finger-structure toxin. We have cloned both toxic protein genes, including the upstream region. PLA2 genes contain three types of inserted sequences: an AG-rich region, a chicken repeat 1-like long interspersed nucleotide element sequence and an intron II 3′ side repeat sequence. The molecular divergence of L. semifasciata PLA2 genes was defined on the basis of the inserted sequences and their sequence homology. The length of intron I in the three-finger-structure toxin genes differs from species to species. The alignment analysis of intron I of the three-finger-structure toxin genes revealed that the intron I sequence of the ancestral gene comprised ten genetic regions. A hypothetical evolutionary process for the three-finger-structure toxin genes has also been developed.

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Abbreviations

APLA2 :

Acidic phospholipase A2

amdC:

Ammodytoxin C

b-btx:

β-Bungarotoxin

Bm:

Bungarus multicinctus

CR1:

Chicken repeat 1

Etx:

Erabutoxin

Etxa:

Erabutoxin a

Etxb:

Erabutoxin b

Etxc:

Erabutoxin c

Gg:

Gallus gallus

LINE:

Long interspersed nucleotide elements

Ls:

Laticauda semifasciata

MAR:

Matrix attached region

nAChR:

Nicotinic acetylcholine receptor

PLA2 :

Phospholipase A2

Ps:

Platemys spixii

SINE:

Short interspersed nucleotide elements

snoRNA:

Small nucleolar RNA

TBP:

TATA box binding protein

Tf:

Trimeresurus flavoviridis

Tg:

Trimeresurus gramineus

Va:

Vipera ammodytes

References

  1. Menez A., (2003) The Subtle Beast, Snakes, From Myth To Medicine. Taylor & Francis Group, London

    Google Scholar 

  2. Ernst C.H., Zug G.R., (1996) Snakes in question. Smithsonian Institution Press, Washington D.C.

    Google Scholar 

  3. Ohno M., Menez R., Ogawa T., Danse J.M., Shimohigashi Y., Fromen C., Ducancel F., Zinn-Justin S., Le Du M.H., Boulain J.C., Tamiya T., Menez A., (1998) Molecular evolution of snake toxins: is the functional diversity of snake toxins associated with a mechanism of accelerated evolution? Prog. Nucleic Acids Res. Mol. Biol. 59: 307–364

    Article  CAS  Google Scholar 

  4. Kini R.M., (1997) Phospholipase A2: a complex multifunctional protein puzzle. In: Kini R.M. (Ed.), Venom phospholipase A2 enzymes: structure, function and mechanism, John Wiley & Sons, Chichester pp. 1–28

    Google Scholar 

  5. Huang P., Mackessy S.P., (2004) Biochemical characterization of phospholipase A2 (trimorphin) from the venom of the Sonoran Lyre Snake Trimorphodon biscutatus lambda (family Colubridae) Toxicon 44: 27–36

    Article  CAS  Google Scholar 

  6. Ho I.C., Arm J.P., Bingham C.O. III, Choi A., Austen K.F., Glimcher L.H., (2001) A novel group of phospholipase A2s preferentially expressed in type 2 helper T cells J. Biol. Chem. 276:18321–18326

    Article  CAS  Google Scholar 

  7. Valentin E., Lambeau G., (2000) Increasing molecular diversity of secreted phospholipases A2 and their receptors and binding proteins Biochim. Biophys. Acta, 1488: 59–70

    CAS  Google Scholar 

  8. Dennis E.A., (1997) The growing phospholipase A2 superfamily of signal transduction enzymes Trends Biochem. Sci. 22: 1–2

    Article  CAS  Google Scholar 

  9. Six D.A., Dennis E.A., (2000) The expanding superfamily of phospholipase A2 enzymes: classification and characterization Biochim. Biophys. Acta 1488: 1–19

    CAS  Google Scholar 

  10. Siew J.P., Khan A.M., Tan P.T., Koh J.L., Seah S.H., Koo C.Y., Chai S.C., Armugam A., Brusic V., Jeyaseelan K., (2004) Systematic analysis of snake neurotoxins’ functional classification using a data warehousing approach Bioinformatics 20: 3466–3480

    Article  CAS  Google Scholar 

  11. Dufton M.J., (1984) Classification of elapid snake neurotoxins and cytotoxins according to chain length: evolutionary implications J. Mol. Evol. 20: 128–134

    Article  CAS  Google Scholar 

  12. Endo T., Tamiya N., (1991) Structure-function relationships of postsynaptic neurotoxins from snake venoms. In: Harvey A.L. (Ed.), Snake toxins. Pergamon Press, New York, pp. 165–222

    Google Scholar 

  13. Tsetlin V., (1999) Snake venom α-neurotoxins and other ‚three-finger’ proteins Eur. J. Biochem. 264:281–286

    Article  CAS  Google Scholar 

  14. Phui Yee J.S., Nanling G., Afifiyan F., Donghui M., Siew L.P., Armugam A., Jeyaseelan K., (2004) Snake postsynaptic neurotoxins: gene structure, phylogeny and applications in research and therapy Biochimie 86: 137–149

    Article  CAS  Google Scholar 

  15. Fry B.G., Wuster W., Kini R.M., Brusic V., Khan A., Venkataraman D., Rooney A.P., (2003) Molecular evolution and phylogeny of elapid snake venom three-finger toxins J. Mol. Evol., 57: 110–129

    Article  CAS  Google Scholar 

  16. Fujimi T.J., Nakajyo T., Nishimura E., Ogura E., Tsuchiya T., Tamiya T., (2003) Molecular evolution and diversification of snake toxin genes, revealed by analysis of intron sequences Gene 313: 111–118

    Article  CAS  Google Scholar 

  17. Ducancel F., Bouchier C., Tamiya T., Boulain J.-C., Menez A., (1991) Cloning and expression of cDNAs encoding snake toxins. In: Harvey A.L. (Ed.), Snake toxin. Pergamon Press, New York, pp. 385–414

    Google Scholar 

  18. Fruchart-Gaillard C., Gilquin B., Antil-Delbeke S., Le Novere N., Tamiya T., Corringer P.J., Changeux J.P., Menez A., Servent D., (2002) Experimentally based model of a complex between a snake toxin and the alpha 7 nicotinic receptor Proc. Natl. Acad. Sci. USA 99: 3216–3221

    Article  CAS  Google Scholar 

  19. Antil-Delbeke S., Gaillard C., Tamiya T., Corringer P.J., Changeux J.P., Servent D., Menez A., (2000) Molecular determinants by which a long chain toxin from snake venom interacts with the neuronal α7-nicotinic acetylcholine receptor J. Biol. Chem. 275: 29594–29601

    Article  CAS  Google Scholar 

  20. Pillet L., Tremeau O., Ducancel F., Drevet P., Zinn-Justin S., Pinkasfeld S., Boulain J.C., Menez A., (1993) Genetic engineering of snake toxins. Role of invariant residues in the structural and functional properties of a curaremimetic toxin, as probed by site-directed mutagenesis J. Biol. Chem., 268: 909–916

    CAS  Google Scholar 

  21. Tsai I.H., Wang Y.M., (1998) Effect of site directed mutagenesis on the activity of recombinant trimucrotoxin, a neurotoxic phospholipase from Trimeresurus mucrosquamatus venom Toxicon 36: 1591–1597

    Article  CAS  Google Scholar 

  22. Nakashima K., Ogawa T., Oda N., Hattori M., Sakaki Y., Kihara H., Ohno M., (1993) Accelerated evolution of Trimeresurus flavoviridis venom gland phospholipase A2 isozymes Proc. Natl. Acad. Sci. USA, 90: 5964–5968

    Article  CAS  Google Scholar 

  23. Ohno M., Ogawa T., Oda-Ueda N., Chijiwa T., Hattori S., (2002) Accelerated and regional evolution of snake venom gland isozymes In: Menez A. (Ed.), Perspectives in molecular toxinology, John Wiley & Sons, Chichester pp. 388–419

    Google Scholar 

  24. Gong N., Armugam A., Jeyaseelan K., (2000) Molecular cloning, characterization and evolution of the gene encoding a new group of short-chain α-neurotoxins in an Australian elapid, Pseudonaja textiles FEBS Lett. 473: 303–310

    Article  CAS  Google Scholar 

  25. Kordis D., Gubensek F., (1996) Ammodytoxin C gene helps to elucidate the irregular structure of Crotalinae group II phospholipase A2 genes Eur. J. Biochem., 240:83–90

    Article  CAS  Google Scholar 

  26. Fuse N., Tsuchiya T., Nonomura Y., Menez A., Tamiya T., (1990) Structure of the snake short-chain neurotoxin, erabutoxin c, precursor gene Eur. J. Biochem. 193:629–633

    Article  CAS  Google Scholar 

  27. Ohno M., Chijiwa T., Oda-Ueda N., Ogawa T., Hattori S., (2003) Molecular evolution of myotoxic phospholipases A2 from snake venom Toxicon 42: 841–854

    Article  CAS  Google Scholar 

  28. Nakashima K., Nobuhisa I., Deshimaru M., Ogawa T., Shimohigashi Y., Fukumaki Y., Hattori M., Sakaki Y., Hattori S., Ohno M., (1995) Structures of genes encoding TATA box-binding proteins from Trimeresurus gramineus and T. flavoviridis snakes Gene 152:209–213

    Article  CAS  Google Scholar 

  29. Nakashima K., Nobuhisa I., Ogawa T., Hattori M., Sakaki Y., Kihara H., Ohno M., (1994) Polymorphisms of Trimeresurus flavoviridis venom gland phospholipase A2 isozyme genes Biosci. Biotechnol. Biochem. 58: 1510–1511

    Article  CAS  Google Scholar 

  30. Nakashima K., Nobuhisa I., Deshimaru M., Nakai M., Ogawa T., Shimohigashi Y., Fukumaki Y., Hattori M., Sakaki Y., Hattori S., Ohno M., (1995) Accelerated evolution in the protein-coding regions is universal in crotalinae snake venom gland phospholipase A2 isozyme genes Proc. Natl. Acad. Sci. USA 92: 5605–5609

    Article  CAS  Google Scholar 

  31. Nobuhisa I., Nakashima K., Deshimaru M., Ogawa T., Shimohigashi Y., Fukumaki Y., Sakaki Y., Hattori S., Kihara H., Ohno M., (1996) Accelerated evolution of Trimeresurus okinavensis venom gland phospholipase A2 isozyme-encoding genes Gene 172:267–272

    Article  CAS  Google Scholar 

  32. Ogawa T., Oda N., Nakashima K., Sasaki H., Hattori M., Sakaki Y., Kihara H., Ohno M., (1992) Unusually high conservation of untranslated sequences in cDNAs for Trimeresurus flavoviridis phospholipase A2 isozymes Proc. Natl. Acad. Sci. USA 89:8557–8561

    Article  CAS  Google Scholar 

  33. Ogawa T., Nakashima K., Oda N., Shimohigashi Y., Ohno M., Hattori S., Hattori M., Sakaki Y., Kihara H., (1995) Trimeresurus flavoviridis venom gland phospholipase A2 isozymes genes have evolved via accelerated substitutions J. Mol. Recognit. 8: 40–46

    Article  CAS  Google Scholar 

  34. Ogawa T., Kitajima M., Nakashima K., Sakaki Y., Ohno M., (1995) Molecular evolution of group II phospholipases A2 J. Mol. Evol. 41: 867–877

    Article  CAS  Google Scholar 

  35. Ogawa T., Nakashima K., Nobuhisa I., Deshimaru M., Shimohigashi Y., Fukumaki Y., Sakaki Y., Hattori S., Ohno M., (1996) Accelerated evolution of snake venom phospholipase A2 isozymes for acquisition of diverse physiological functions Toxicon 34:1229–1236

    Article  CAS  Google Scholar 

  36. Kordis D., Gubensek F., (1997) Bov-B long interspersed repeated DNA (LINE) sequences are present in Vipera ammodytes phospholipase A2 genes and in genomes of Viperidae snakes Eur. J. Biochem. 246: 772–779

    Article  CAS  Google Scholar 

  37. Kordis D., Gubensek F., (1998) The Bov-B lines found in Vipera ammodytes toxic PLA2 genes are widespread in snake genomes Toxicon 36: 1585–1590

    Article  CAS  Google Scholar 

  38. Kordis D., Gubensek F., (1998) Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes Proc. Natl. Acad. Sci. USA 95:10704–10709

    Article  CAS  Google Scholar 

  39. Kordis D., Gubensek F., (1999) Horizontal transfer of non-LTR retrotransposons in vertebrates Genetica 107: 121–128

    Article  CAS  Google Scholar 

  40. Kordis D., Gubensek F., (1999) Molecular evolution of Bov-B LINEs in vertebrates Gene 238: 171–178

    Article  CAS  Google Scholar 

  41. Krizaj I., Dolly J.O., Gubensek F., (1994) Identification of the neuronal acceptor in bovine cortex for ammodytoxin C, a presynaptically neurotoxic phospholipase A2 Biochemistry 33: 13938–13945

    Article  CAS  Google Scholar 

  42. Burch J.B., Davis D.L., Haas N.B., (1993) Chicken repeat 1 elements contain a pol-like open reading frame and belong to the non-long terminal repeat class of retrotransposons Proc. Natl. Acad. Sci. USA 90: 8199–8203

    Article  CAS  Google Scholar 

  43. Nobuhisa I., Ogawa T., Deshimaru M., Chijiwa T., Nakashima K.I., Chuman Y., Shimohigashi Y., Fukumaki Y., Hattori S., Ohno M., (1998) Retrotransposable CR1-like elements in crotalinae snake genomes Toxicon 36:915–920

    Article  CAS  Google Scholar 

  44. Fujimi T.J., Tsuchiya T., Tamiya T., (2002) A comparative analysis of invaded sequences from group IA phospholipase A2 genes provides evidence about the divergence period of genes groups and snake families Toxicon 40: 873–884

    Article  CAS  Google Scholar 

  45. Fujimi T.J., Kariya Y., Tsuchiya T., Tamiya T., (2002) Nucleotide sequence of phospholipase A2 gene expressed in snake pancreas reveals the molecular evolution of toxic phospholipase A2 genes Gene 292: 225–231

    Article  CAS  Google Scholar 

  46. Tamiya N., Yagi T., (1985) Non-divergence theory of evolution: sequence comparison of some proteins from snakes and bacteria J. Biochem. (Tokyo) 98: 289–303

    CAS  Google Scholar 

  47. Jeyaseelan K., Armugam A., Donghui M., Tan N.H., (2000) Structure and phylogeny of the venom group I phospholipase A2 gene Mol. Biol. Evol. 17: 1010–1021

    CAS  Google Scholar 

  48. Kordis D., Gubensek F., (2000) Adaptive evolution of animal toxin multigene families Gene 261: 43–52

    Article  CAS  Google Scholar 

  49. Vandergon T.L., Reitman M., (1994) Evolution of chicken repeat 1 (CR1) elements: evidence for ancient subfamilies and multiple progenitors Mol. Biol. Evol. 11: 886–898

    CAS  Google Scholar 

  50. Deshimaru M., Ogawa T., Nakashima K., Nobuhisa I., Chijiwa T., Shimohigashi Y., Fukumaki Y., Niwa M., Yamashina I., Hattori S., Ohno M., (1996) Accelerated evolution of crotalinae snake venom gland serine proteases FEBS Lett. 397: 83–88

    Article  CAS  Google Scholar 

  51. Hahn B.S., Yang K.Y., Park E.M., Chang I.M., Kim Y.S., (1996) Purification and molecular cloning of calobin, a thrombin-like enzyme from Agkistrodon caliginosus (Korean viper) J. Biochem. (Tokyo) 119: 835–843

    CAS  Google Scholar 

  52. Serrano S.M., Hagiwara Y., Murayama N., Higuchi S., Mentele R., Sampaio C.A., Camargo A.C., Fink E., (1998) Purification and characterization of a kinin-releasing and fibrinogen-clotting serine proteinase (KN-BJ) from the venom of Bothrops jararaca, and molecular cloning and sequence analysis of its cDNA Eur. J. Biochem. 251: 845–853

    Article  CAS  Google Scholar 

  53. Zhang Y., Wisner A., Xiong Y., Bon C., (1995) A novel plasminogen activator from snake venom. Purification, characterization, and molecular cloning J. Biol. Chem. 270: 10246–10255

    Article  CAS  Google Scholar 

  54. Nishida S., Kim H.S., Tamiya N., (1982) Amino acid sequences of three phospholipases A I, III and IV from the venom of the sea snake Laticauda semifasciataBiochem. J. 207: 589–594

    CAS  Google Scholar 

  55. Yoshida H., Kudo T., Shinkai W., Tamiya N., (1979) Phospholipase A of sea snake Laticauda semifasciata venom. Isolation and properties of novel forms lacking tryptophan J Biochem (Tokyo) 85:379–388

    CAS  Google Scholar 

  56. Harvey A.L., Tamiya N., (1980) Role of phospholipase A activity in the neuromuscular paralysis produced by some components isolated from the venom of the seasnake, Laticauda semifasciata Toxicon 18: 65–69

    Article  CAS  Google Scholar 

  57. Fujimi T.J., Yasuoka S., Ogura E., Tsuchiya T., Tamiya T., (2004) Comparative analysis of gene expression mechanisms between group IA and IB phospholipase A2 genes from sea snake Laticauda semifasciata Gene 332: 179–190

    Article  CAS  Google Scholar 

  58. Iijima N., Fujikawa Y., Tateishi Y., Takashima Y., Uchiyama S., Esaka M., (2001) Cloning and expression of group IB phospholipase A2 isoforms in the red sea bream, Pagrus major Lipids 36: 499–506

    Article  CAS  Google Scholar 

  59. Ohara O., Tamaki M., Nakamura E., Tsuruta Y., Fujii Y., Shin M., Teraoka H., Okamoto M., (1986) Dog and rat pancreatic phospholipases A2: complete amino acid sequences deduced from complementary DNAs J. Biochem. (Tokyo) 99: 733–739

    CAS  Google Scholar 

  60. Seilhamer J.J., Plant S., Pruzanski W., Schilling J., Stefanski E., Vadas P., Johnson L.K., (1989) Multiple forms of phospholipase A2 in arthritic synovial fluid J. Biochem. (Tokyo) 106: 38–42

    CAS  Google Scholar 

  61. Servent D., Winckler-Dietrich V., Hu H.Y., Kessler P., Drevet P., Bertrand D., Menez A., (1997) Only snake curaremimetic toxins with a fifth disulfide bond have high affinity for the neuronal α7 nicotinic receptor J. Biol. Chem. 272: 24279–24286

    Article  CAS  Google Scholar 

  62. Feofanov A.V., Sharonov G.V., Dubinnyi M.A., Astapova M.V., Kudelina I.A., Dubovskii P.V., Rodionov D.I., Utkin Y.N., Arseniev A.S., (2004) Comparative study of structure and activity of cytotoxins from venom of the cobras Naja oxiana, Naja kaouthia, and Naja haje Biochemistry (Mosc.) 69:1148–1157

    Article  CAS  Google Scholar 

  63. Feofanov A.V., Sharonov G.V., Astapova M.V., Rodionov D.I., Utkin Y.N., Arseniev A.S., (2005) Cancer cell injury by cytotoxins from cobra venom is mediated through lysosomal damage Biochem. J. 390: 11–18

    Article  CAS  Google Scholar 

  64. Gasanov S.E., Alsarraj M.A., Gasanov N.E., Rael E.D., (1997) Cobra venom cytotoxin free of phospholipase A2 and its effect on model membranes and T leukemia cells J. Membr. Biol. 155: 133–142

    Article  CAS  Google Scholar 

  65. Marchot P., Bourne Y., Prowse C.N., Bougis P.E., Taylor P., (1998) Inhibition of mouse acetylcholinesterase by fasciculin: crystal structure of the complex and mutagenesis of fasciculin Toxicon 36: 1613–1622

    Article  CAS  Google Scholar 

  66. Dajas F., Bolioli B., Castello M.E., Silveira R., (1987) Rat striatal acetylcholinesterase inhibition by fasciculin (a polypeptide from green mamba snake venom) Neurosci. Lett. 77: 87–91

    Article  CAS  Google Scholar 

  67. Karlsson E., Mbugua P.M., Rodriguez-Ithurralde D., (1984) Fasciculins, anticholinesterase toxins from the venom of the green mamba Dendroaspis angusticeps J. Physiol. (Paris) 79: 232–240

    CAS  Google Scholar 

  68. Grant G.A., Chiappinelli V.A., (1985) κ-Bungarotoxin: complete amino acid sequence of a neuronal nicotinic receptor probe Biochemistry 24: 1532–1537

    Article  CAS  Google Scholar 

  69. McLane K.E., Weaver W.R., Lei S., Chiappinelli V.A., Conti-Tronconi B.M., (1993) Homologous κ-neurotoxins exhibit residue-specific interactions with the α3 subunit of the nicotinic acetylcholine receptor: a comparison of the structural requirements for κ-bungarotoxin and kappa-flavitoxin binding. Biochemistry 32: 6988–6994

    Article  CAS  Google Scholar 

  70. Maeda N., Tamiya N., (1974) The primary structure of the toxin Laticauda semifasciata III, a weak and reversibly acting neurotoxin from the venom of a sea snake, Laticauda semifasciata Biochem. J. 141:389–400

    CAS  Google Scholar 

  71. Sato S., Tamiya N., (1971) The amino acid sequences of erabutoxins, neurotoxic proteins of sea-snake (Laticauda semifasciata) venom Biochem. J. 122: 453–461

    CAS  Google Scholar 

  72. Tamiya N., Abe H., (1972) The isolation, properties and amino acid sequence of erabutoxin c, a minor neurotoxic component of the venom of a sea snake Laticauda semifasciata Biochem. J. 130: 547–555

    CAS  Google Scholar 

  73. Tamiya T., Ohno S., Nishimura E., Fujimi T.J., Tsuchiya T., (1999) Complete nucleotide sequences of cDNAs encoding long chain α-neurotoxins from sea krait, Laticauda semifasciata Toxicon 37: 181–185

    Article  CAS  Google Scholar 

  74. Cockerill P.N., Garrard W.T., (1986) Chromosomal loop anchorage sites appear to be evolutionarily conserved FEBS Lett. 204: 5–7

    Article  CAS  Google Scholar 

  75. Liebich I., Bode J., Reuter I., Wingender E., (2002) Evaluation of sequence motifs found in scaffold/matrix-attached regions (S/MARs) Nucleic Acids Res. 30: 3433–3442

    Article  CAS  Google Scholar 

  76. Mirkovitch J., Mirault M.E., Laemmli U.K., (1984) Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold Cell 39: 223–232

    Article  CAS  Google Scholar 

  77. Tamiya N., (1973) Erabutoxins a, b and c in sea snake Laticauda semifasciata venom Toxicon 11: 95–97

    Article  CAS  Google Scholar 

  78. Chang L., Lin S., Huang H., Hsiao M., (1999) Genetic organization of α-bungarotoxins from Bungarus multicinctus (Taiwan banded krait): evidence showing that the production of α-bungarotoxin isotoxins is not derived from edited mRNAs Nucleic Acids Res. 27: 3970–3975

    Article  CAS  Google Scholar 

  79. Holth L.T., Chadee D.N., Spencer V.A., Samuel S.K., Safneck J.R., Davie J.R., (1998) Chromatin, nuclear matrix and the cytoskeleton: role of cell structure in neoplastic transformation (review) Int. J. Oncol. 13:827–837

    CAS  Google Scholar 

  80. Chang L.S., Hong E., (1997) Novel SnoRNAs from Naja naja atra (Taiwan cobra) and Bungarus multicinctus (Taiwan banded krait), form extended sequence complementarity to 5S rRNA Biochem. Biophys. Res. Commun. 236:782–784

    Article  CAS  Google Scholar 

  81. Chang L.S., Chou Y.C., Lin S.R., Wu B.N., Lin J., Hong E., Sun Y.J., Hsiao C.D., (1997) A novel neurotoxin, cobrotoxin b, from Naja naja atra (Taiwan cobra) venom: purification, characterization, and gene organization J. Biochem. (Tokyo) 122:1252–1259

    CAS  Google Scholar 

  82. Chang L.S., Lin J., Chou Y.C., Hong E., (1997) Genomic structures of cardiotoxin 4 and cobrotoxin from Naja naja atra (Taiwan cobra) Biochem. Biophys. Res. Commun. 239: 756–762

    Article  CAS  Google Scholar 

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Tamiya, T., Fujimi, T.J. Molecular evolution of toxin genes in Elapidae snakes. Mol Divers 10, 529–543 (2006). https://doi.org/10.1007/s11030-006-9049-x

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