Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS) and isoelectric focusing

Journal of Molecular Evolution

Volumn 56, Issue 3, 2003, Pages 317-329

  Creer, Simon ^a   Malhotra, Anita ^a   Thorpe, Roger S ^a   Stöcklin, Reto ^b   Favreau, Philippe ^b   Chou, Wen Hao ^c  

^a BANGOR UNIVERSITY   (United Kingdom)

^b ATHERIS LABORATORIES   (Switzerland)

^c NATIONAL MUSEUM OF NATURAL SCIENCE   (Taiwan)

Author keywords

Geographic variation; MALDI TOF mass spectrometry; Phospholipase A2; Taiwan; Trimeresurus stejnegeri; Venom

Indexed keywords

ISOENZYME; PHOSPHOLIPASE A2; SNAKE VENOM;

ARTICLE; CONTROLLED STUDY; FEMALE; GEOGRAPHICAL VARIATION (SPECIES); GEOGRAPHY; ISOELECTRIC FOCUSING; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PACIFIC ISLANDS; PHYLOGENY; TAIWAN;

ANIMALS; CROTALID VENOMS; CYTOCHROME B GROUP; EVOLUTION, MOLECULAR; ISOELECTRIC FOCUSING; MITOCHONDRIA; PHYLOGENY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TAIWAN; VARIATION (GENETICS); VIPERIDAE;

ANIMALIA; SERPENTES; TRIMERESURUS; TRIMERESURUS STEJNEGERI;

EID: 0037372230     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-002-2403-4     Document Type: Article

References (77)

1. Aird SD, Thirkhill LJ, Seebart CS, Kaiser II (1989) Venoms and morphology of western diamondback/mojave rattlesnake hybrids. J Herp 23:131-141
2. Anderson SG, Gutiérrez JM, Ownby CL (1993) Comparison of the immunogenicity and antigenic composition of ten Central American snake venoms. Toxicon 31:1051-1059
3. Bairoch A, Apweiler R (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res 28:45-48 (http://www/expasy.ch/sprot)
4. Bonilla CA, Faith MR, Minton SAJ (1973) L-amino acid oxidase, phosphodiesterase, total protein and other properties of juvenile timber rattlesnake (C. h. horridus) venom at different stages of growth. Toxicon 11:301-303
5. Bowersox SS, Luther R (1998) Pharmacotherapeutic potential of omega-conotoxin MVIIA (SNX-111), an N-type neuronal calcium channel blocker found in the venom of Conus magus. Toxicon 36:1651-1658
6. Campbell JA, Solorzano A (1992) The distribution, variation, and natural history of the middle american montane pitviper, Porthidium godmani. In: Campbell JA, Brodie ED (eds) Biology of the pitvipers. Sylva, Tyler, TX, pp 223-250
7. Chijiwa T, Deshimaru M, Nobuhisa I, Nakai M, Ogawa T, Oda N, Nakashima K-I, Fukumaki Y, Shimohigashi Y, Hattori S, Ohno M (2000) Regional evolution of venom gland phospholipase A2 isozymes of Trimeresurus flavoviridis snakes in the southwestern islands of Japan. Biochem J 347:491-499
8. Chippaux JP, Goyffon M (1998) Venoms, antivenoms and immunotherapy. Toxicon 36:823-846
9. Chippaux JP, Boche J, Courtois B (1982) Electrophoretic patterns of the venoms from a litter of Bitis gabonica snakes. Toxicon 20:521-523
10. Chippaux JP, Williams V, White J (1991) Snake venom variability: methods of study, results and interpretation. Toxicon 29:1279-1303
11. Chuman Y, Nobuhisa I, Ogawa T, Deshimaru M, Chijiwa T, Tan N-H, Fukumaki Y, Shimohigashi Y, Ducancel F, Boulain J-C, Menéz A, Ohno M (2000) Regional and accelerated molecular evolution in group I snake venom gland phospholipase A2 isozymes. Toxicon 38:449-462
12. Conticello SG, Gilad Y, Avidan N, Ben-Asher E, Levy Z, Fainzilber M (2001) Mechanisms for evolving hypervariability: The case of the conopeptides. Mol Biol Evol 18:120-131
13. Creer S, Malhotra A, Thorpe RS, Chou W-H (2001) Multiple causation of phylogeographical pattern as revealed by nested clade analysis of the bamboo viper (Trimeresurus stejnegeri) within Taiwan. Mol Ecol 10:1967-1981
14. Creer S, Chou W-H, Malhotra A, Thorpe RS (2002) Offshore insular variation in the diet of the Taiwanese bamboo viper Trimeresurus stejnegeri (Schmidt). Zool Sci 19:907-913
15. Creer S, Malhotra A, Thorpe RS, Chou W-H (2003) Cryptic genetic diversity in the bamboo viper (Trimeresurus stejnegeri) within Taiwan. In: Schuett G, Höggren M, Greene H (eds) Biology of the vipers. Eagle Mountain Publishing (in press)
16. Daltry JC, Ponnudurai G, Shin CK, Tan NH, Thorpe RS, Wüster W (1996a) Electrophoretic profiles and biological activities: Intraspecific variation in the venom of the Malayan Pitviper (Calloselasma rhodostoma). Toxicon 34:67-79
17. Daltry JC, Wüster W, Thorpe RS (1996b) Diet and snake venom evolution. Nature 379:537-540
18. Daltry JC, Wüster W, Thorpe RS (1997) The role of ecology in determining venom variation in the Malayan pitviper, Calloselasma rhodostoma. In: Thorpe RS, Wüster W, Malhotra A (eds) Venomous snakes, ecology, evolution and snakebite. Symposia of the Zoological Society of London, pp 155-171
19. 2 enzymes: Structure, function and mechanism. John Wiley and Sons, New York, pp 29-72
20. Deshimaru M, Ogawa T, Nakashima KI, Nobuhisu I, Chijiwa T, Shimohigashi Y, Fukumaki Y, Niwa M, Yamashina I, Hattori S, Ohno M (1996) Accelerated evolution of crotaline snake-venom gland serine proteases. FEBS Lett 397:83-88
21. Duda TFJ, Palumbi SR (1999) Molecular genetics of ecological diversification: Duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc Natl Acad Sci USA 96:6820-6823
22. Escoubas P, Chamot-Rooke J, Stöcklin R, Whiteley BJ, Corzo G, Genet R, Nakajima T (1999) A comparison of matrix-assisted laser desorption/ionisation time-of-flight and liquid chromatography electrospray ionisation mass spectrometry methods for the analysis of crude tarantula venoms in the Pterinochilus group. Rapid Commun Mass Spectrom 13:1861-1868
23. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1-15
24. Feng B, Wu WJ, Qian R, Wang KY, Zhou YC (1996) Purification and characterisation of phospholipase A(2) from the venom of snake Trimeresurus stejnegeri Schmidt. Acta Biochim Biophys Sinica 28:201-205
25. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM (1989) Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64-71
26. 2 isozyme from Trimeresurus gramineus (green habu snake) venom. Toxicon 30:1331-1341
27. 2 isozymes from Trimeresurus gramineus (Green Habu Snake) venom. Toxicon 31:957-967
28. Glenn JL, Straight RC (1989) Intergradation of two different venom populations of the Mojave rattlesnake (Crotalus scutulatus scutulatus) in Arizona. Toxicon 27:411-418
29. Gregory-Dwyer VM, Egen NB, Bosisio AB, Righetti PG, Russell FE (1986) An isoelectric focusing study of seasonal variation in rattlesnake venom proteins. Toxicon 24:995-1000
30. 2 enzymes: Structure, function and mechanism. John Wiley and Sons, New York, pp 73-96
31. Harris JB (1985) Phospholipases in snake venoms and their effects on nerve and muscle. Pharm Theor 31:79-102
32. Harris JB (1997) Toxic phospholipases in snake venom: An introductory review. In: Thorpe RS, Wüster W, Malhotra A (eds) Venomous snakes, ecology, evolution and snakebite. Symposia of the Zoological Society of London, pp 235-250
33. Harris JB, MacDonell CA (1981) Phospholipase A2 activity of notexin and its role in muscle damage. Toxicon 19:419-430
34. Huang J (1984) Change of sea-level since the late Pleistocene in China. In: Whyte RO (ed) The evolution of the east Asian environment. Center of Asian Studies, University of Hong Kong, Hong Kong, pp 309-319
35. Jones MJ (1976) Variations of venom proteins in Agkistrodon snakes from North America. Copeia 3:558-562
36. King RB (1993) Microgeographic, historical, and size-correlated variation in water snake diet composition. J Herp 27:90-94
37. Kini RM (1997) Phospholipase A2-A complex multifunctional protein puzzle. In: Kini RM (ed) Venom phospholipase A2 enzymes: Structure, function and mechanism. John Wiley and Sons, New York, pp 1-28
38. Kuo TP, Wu CS (1972) Clinico pathological studies on snakebite in Taiwan. Snake 4:1-22
39. Legendre P, Fortin M-J (1989) Spatial pattern and ecological analysis. Vegetatio 80:107-138
40. Manly BJF (1991) Randomisation and Monte Carlo methods in biology. Chapman and Hall, London
41. Mao S (1993) Common terrestrial venomous snakes of Taiwan. Special Publication Number 5. National Museum of Natural Science, Taiwan
42. Marsh NA, Whaler BC (1984) The Gaboon viper (Bitis gabonica): Its biology, venom components and toxinology. Toxicon 22:669-694
43. McDiarmid RW, Campbell JA, Tourė TSA (1999) Snake species of the world. A taxonomic and geographic reference. Herpetologists League, Washington, DC
44. Mebs D (2001) Toxicity in animals. Trends in evolution. Toxicon 39:87-96
45. Meier J, Stocker KF (1995) Biology and distribution of venomous snakes of medical importance and the composition of snake venoms. In: Meier J, White J (eds) Handbook of clinical toxicology of animal venoms and poisons. CRC Press, Boca Raton, FL, pp 367-412
46. Metzgar D, Wills C (2000) Evidence for the adaptive evolution of mutation rates. Cell 101:581-584
47. Mirgorodskaya E, Krogh TN, Roepstorff P (2000) Characterisation of protein glycolysation by MALDI-TOFMS. In: Chapman JR (ed) Methods in molecular biology, Vol 146. Protein and peptide analysis: New mass spectrometric applications. Humana Press, Totowa, NJ, pp 273-292
48. Monteiro RQ, Carlini CR, Guimaraes JA, Bon C, Zingali RB (1997) Distinct Bothrojaracin isoforms produced by individual Jararaca (Bothrops jararaca) snakes. Toxicon 35:649-657
49. Nakai M, Nakashima K, Ogawa T, Shimohigashi Y, Hattori S, Chang C-C, Ohno M (1995) Purification and primary structure of a myotoxic lysine-49 phospholipase A(2) with low lipolytic-activity from Trimeresurus gramineus venom. Toxicon 33:1469-1478
50. Nakashima K, Ogawa T, Oda N, Shimohigashi Y, Hattori M, Sakaki Y, Kihora H, Ohno M (1994) Darwinian evolution of Trimeresurus flavoviridis venom gland phospholipase A(2) isozymes. Pure Appl Chem 66:715-720
51. Nakashima K-I, 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 crotaline snake venom gland phospholipase A2 isozyme genes. Proc Natl Acad Sci USA 92:5605-5609
52. Oda N, Sakai H, Shieh TC, Nakamura H, Sakamoto S, Kihara H, Chang C-C, Ohno M (1987) Purification and characterization of phospholipase A2 from Trimeresurus gramineus venom. J Biochem 102:1441-1449
53. 2 from the venom of Trimeresurus gramineus (green Habu snake). Toxicon 29:157-166
54. 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 A (2) isozymes for acquisition of diverse physiological functions. Toxicon 34:1229-1236
55. Rael ED, Johnson JD, Molina O, McCrystal HK (1992) Distribution of a Mojave toxin-like protein in rock rattlesnake (Crotalus lepidus) venom. In: Campbell JA, Brodie EDJ (eds) Biology of the pitvipers. Selva, Tyler, TX, pp 163-168
56. Raftery MJ (2000) Characterisation of a mutant recombinant S100 protein using electrospray ionisation mass spectrometry. In: Chapman JR (ed) Methods in molecular biology, Vol. 146. Protein and peptide analysis: New mass spectrometric applications. Humana Press, Totowa, NJ, pp 27-39
57. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223-225
58. Righetti PG, Drysdale JW (1976) Isoelectric focusing: Laboratory techniques in biochemistry and molecular biology. North Holland/Elsevier, Amsterdam
59. Rosche F, Schmidt J, Hoffman T, Pauly RP, McIntosh CHS, Pederson RA, Demuth HU (2000) Kinetic analysis of enzymatic and nonenzymatic degradation of peptides by MALDI-TOFMS. In: Chapman JR (ed) Methods in molecular biology, Vol 146. Protein and peptide analysis: New mass spectrometric applications. Humana Press, Totowa, NJ, pp 251-272
60. Sadahiro S, Omori-Satoh T (1980) Lack of a hemorrhagic principle in Habu snake venom, Trimeresurus flavoviridis, from the Okinawa Islands. Toxicon 18:366-368
61. Sasa M (1999) Diet and snake venom evolution: Can local selection alone explain intraspecific venom variation? Toxicon 32:249-252
62. Sasa M, Barrantes R (1998) Allozyme variation in populations of Bothrops asper (Serpentes: Viperidae) in Costa Rica. Herpetologica 54:462-469
63. Schenberg S (1958) Geographical pattern of crotamine distribution in the same rattlesnake subspecies. Science 129:1361-1363
64. Schwaner TD (1985) Population structure of black tiger snakes, Notechis ater niger, on offshore islands of south Australia. In: Grigg G, Shine R, Ehmann H (eds) Biology of Australasian Frogs and Reptiles. Royal Zoological Society of New South Wales, pp 35-46
65. Sokal RR, Rohlf FJ (1995) Biometry, 3rd ed. W.H. Freeman, San Francisco
66. Stöcklin R, Favreau P (2002) Proteomics of venom peptides. In: Ménez A (ed) Perspectives in molecular toxinology. John Wiley and Sons, Chichester, UK, (in press)
67. Stöcklin R, Mebs D, Boulain J-C, Panchaud P-A, Virelizier H, Gillard-Factor C (2000) Identification of snake species by toxin mass fingerprinting of their venoms. In: Chapman JR (ed) Methods in molecular biology, Vol 146. Protein and peptide analysis: New mass spectrometric applications. Humana Press, Totowa, NJ, pp 317-336
68. Thorpe RS, Brown M, Day M, Malhotra A, McGregor DP, Wüster W (1994) Testing ecological and phylogenetic hypotheses in microevolutionary studies. In: Eggleton P, Vane-Wright R (eds) Phylogenetics and ecology. Linnean Society of London, London, pp 189-206
69. Trikha M, Schmitmeier S, Markland FS (1994) Purification and characterisation of fibrolase isoforms from venom of individual southern copperhead (Agkistrodon contortix contortix) snakes. Toxicon 32:1521-1531
70. Tyler MI, Retson-Yip KV, Gibson MK, Barnett D, Howe E, Stöcklin R, Turnbull RK, Kuchel T, Mirtschin P (1997) Isolation and amino acid sequence of a new long-chain neurotoxin with two chromotographic isoforms (Ae e1 and Ae e2) from the venom of the Australian death adder (Acanthophis antarcticus). Toxicon 35:555-562
71. Warrell DA (1986) Tropical snake bite: Clinical studies in southeast Asia. In: Harris JB (ed) Natural toxins - Animal, plant and microbial. Clarendon Press, Oxford, pp 25-45
72. Warrell DA (1995) Clinical toxicology of snakebite in Asia. In: Meier J, White J (eds) Handbook of clinical toxicology of animal venoms and poisons. CRC Press, Boca Raton, FL, pp 496-594
73. Warrell DA (1997) Geographical and intraspecies variation in the clinical manifestations of envenoming by snakes. In: Thorpe RS, Wuster W, Malhotra A (eds) Venomous snakes, ecology, evolution and snakebite. Symposia of the Zoological Society of London, pp 189-203
74. Wilkinson JA, Glenn JL, Straight RC, Sites JW (1991) Distribution and genetic variation in venom A and B populations of the Mojave rattlesnake (Crotalus scutulatus scutulatus) in Arizona. Herpetologica 47:54-68
75. Williams V, White J (1997) Snake venom and snakebite in Australia. In: Thorpe RS, Wüster W, Malhotra A (eds) Venomous snakes, ecology, evolution and snakebite. Symposia of the Zoological Society of London, 70, pp 205-217
76. Williams V, White J, Schwaner TD, Sparrow A (1988) Variation in venom proteins from isolated populations of tiger snakes (Notechis ater niger, N. scutatus) in South Australia. Toxicon 26:1067-1075
77. Yu H-T (1995) Patterns of diversification and genetic population structure of small mammals in Taiwan. Biol J Linn Soc 55:69-89