Abstract
The nucleotide sequences of 13 cDNAs encoding group II phospholipases A2 (PLA2 S), which are from viperidae snake venoms and from mammalian sources, were aligned and analyzed by phylogenetic trees constructed using various components of the sequences. The evolutionary trees derived from the combined sequences of the untranslated (5′ and 3′) region and the signal peptide region of cDNAs were in accord with the consequences from taxonomy. In contrast, the evolutionary trees from the mature protein-coding region sequences of cDNAs and from the amino acid sequences showed random patterns. These observations indicated that the mature protein-coding region has evolved through a process differently from the untranslated and signal peptide regions. The trees built from the nucleotide differences at each of three positions of codons in the mature protein-coding region suggested that snakevenom-gland PLA2 genes have evolved via a process different from mammalian PLA2 genes. The occurrence of accelerated evolution has been recently discovered in Trimeresurus flavoviridis venom-gland group II PLA2 isozyme genes (Nakashima et al. 1993, Proc Natl Acad Sci USA 90:5964–5968), so the present phylogenetic analysis together with the estimation of nucleotide divergence of cDNAs provides further evidence that snakevenom-group II PLA2 isozyme genes have evolved by accelerated evolution to gain diverse physiological activities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Boffa GA, Boffa MC, Winchenne JJ (1976) A phospholipase A2 with anticoagulant activity. I. Isolation from Vipera berus venom and properties. Biocim Biophys Acta 429:828–838
Bouchier C, Boulain J-C, Bon C, Ménez A (1991) Analysis of cDNAs encoding the two subunits of crotoxin, a phospholipase A2 neurotoxin from rattlesnake venom: the acidic non enzymatic subunit derives from a phospholipase A2-like precursor. Biochim Biophys Acta 1088:401–408
Davidson FF, Dennis EA (1990) Evolutionary relationships and implication for the regulation of phospholipases A2 from snake venom to human secreted forms. J Mol Evol 31:228–238
Dijkstra BW, Kalk KH, Hol WGJ, Drenth J (1981) Structure of bovine pancreatic phospholipase A2 at 1.7 Å resolution. J Mol Biol 147: 97–123
Dijkstra BW, Renetseder R, Kalk KH, Hol WGJ, Drenth J (1983) Structure of porcine pancreatic phospholipase A2 at 2.6 Å resolution and comparison with bovine phospholipase A2. J Mol Biol 168:163–179
Dufton MJ, Hider RC (1983) Classification of phospholipases A2 according to sequence. Evolutionary and pharmacological implications. Eur J Biochem 137:545–551
Felsenstein J (1985) Confidence limits of phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fletcher JE, Rapuano BE, Condrea E, Yang C-C, Rosenberg P (1981) Relationship between catalysis and toxicological properties of three phospholipases A2 from elapid snake venoms. Toxicol Appl Pharmacol 59:375–388
Francis B, Gutierrez JM, Lomonte B, Kaizer II (1991) Myotoxin II from Bothrops asper (Terciopelo) venom is a lysine-49 phospholipase A2. Arch Biochem Biophys 284:352–359
Gojobori T, Ishii K, Nei M (1982) Estimations of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. J Mol Evol 18:414–423
Gutierrez JM, Lomonte MB, Cerdas L (1986) Isolation and partial characterization of a myotoxin from the venom of the snake Bothrops nummifer. Toxicon 24:885–894
Halpert J, Eaker D, Karlsson E (1976) The role of phospholipase activity in the action of a presynaptic neurotoxin from the venom of Notechis scutatus scutatus (Australian tiger snake). FEBS lett 61: 72–76
Higgins DG, Fuches R, Bleasby A (1992) CLUSTAL V: a new multiple sequence alignment program. Comput Appl Biosci 8:189–191
Ishizaki J, Ohara O, Nakamura E, Tamaki M, Ono T, Kanda A, Yoshida N, Teraoka H, Tojo H, Okamoto M (1989) cDNA cloning and sequence determination of rat membrane-associated phospholipase A2. Biochem Biophys Res Commun 162:1030–1036
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–123
Kihara H, Uchikawa R, Hattori S, Ohno M (1992) Myotoxicity and physiological effects of three Trimeresurus flavoviridis phospholipases A2. Biochem Int 28:895–903
Kimura M (1969) The rate of molecular evolution considered from the standpoint of population genetics. Proc Natl Acad Sci USA 63: 1181–1188
Kimura M (1983) The neutral theory of molecular evolution. Cambridge Univ Press, Cambridge, U.K.
Kini RM, Kawabata S, Iwanaga S (1986) Comparison of amino terminal region of three isoenzymes of phospholipases A2 (TFV PL-Ia, TFV PL-Ib, TFV PL-X) from Trimeresurus flavoviridis (habu snake) venom and the complete amino acid sequences of the basic phospholipase, TFV PL-X. Toxicon 24:1117–1129
Kramer RM, Hession C, Johansen B, Hayes G, McGray P, Chow EP, Tizard R, Pepinsky RB (1989) Structure and properties of a human nonpancreatic phospholipase A2. J Biol Chem 264:5768–5775
Liu S-Y, Yoshizumi K, Oda N, Ohno M, Tokunaga F, Iwanaga S, Kihara H (1990) Purification and amino acid sequence of basic protein II, a lysine-49-phospholipase A2 with low activity, from Trimeresurus flavoviridis venom. J Biochem (Tokyo) 107:400–408
Maraganore JM, Merutka G, Cho W, Welches W, Kézdy FJ, Heinrikson RL (1984) A new class of phospholipase A2 with lysine in place of aspartate 49. Functional consequences for calcium and substrate binding. J Biol Chem 259:13839–13843
Maraganore JM, Heinrikson RL (1986) The lysine-49 phospholipase A2 from the venom of Agkistrodon piscivorus piscivorus. Relation of structure and function to other phospholipases A2. J Biol Chem 261:4797–4804
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
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
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Nei M, Jin L (1989) Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol 6: 290–300
Oda N, Ogawa T, Ohno M, Sasaki H, Sakaki Y, Kihara H (1990) Cloning and sequence analysis of cDNA for Trimeresurus flavoviridis phospholipase A2, and consequent revision of the amino acid sequence. J Biochem (Tokyo) 108:816–821
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
Ohta T (1991) Role of diversifying selection and gene conversion in evolution of major histocompatibility complex loci. Proc Natl Acad Sci USA 88:6716–6720
Ohta T, Basten CJ (1992) Gene conversion generates hypervariability at the variable regions of kallikreins and their inhibitors. Mol Phyl Evol 1:87–90
Ohta T (1993) Amino acid substitution at the Adh locus of Drosophila is facilitated by small population size. Proc Natl Acad Sci USA 90:4548–4551
Pungercar J, Kordis D, Strukelj B, Liang N-S, Gubensek F (1991) Cloning and nucleotide sequence of a cDNA encoding ammodytoxin A, the most toxic phospholipase A2 from the venom of longnosed viper (Vipera ammodytes). Toxicon 29:269–273
Renetseder R, Brunie S, Dijkstra BW, Drenth J, Sigler PB (1985) A comparison of the crystal structures of phospholipases A2 from bovine pancreas and Crotalus atrox venom. J Biol Chem 260: 11627–11634
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scott DL, Achari A, Vidal JC, Sigler PB (1992) Crystallographic and biochemical studies of the (inactive) Lys-49 phospholipase A2 from the venom of Agkistrodon piscivorus piscivorus. J Biol Chem 267: 22645–22657
Seilhamer JJ, Pruzanski W, Vadas P, Plant S, Miller JA, Kloss J, Johnson LK (1989) Cloning and recombinant expression of phospholipase A2 present in rheumatoid arthritic synovial fluid. J Biol Chem 264:5335–5338
Tanaka S, Mohori N, Kihara H, Ohno M (1986) Amino acid sequence of Trimeresurus flavoviridis phospholipase A2. J Biochem (Tokyo) 99:281–289
Vishwanath BS, Kini RM, Gowda TV (1987) Characterization of three edema-inducing phospholipase A2 enzymes from habu (Trimeresurus flavoviridis) venom and their interaction with the alkaloid aristolochic acid. Toxicon 25:501–515
Wery J-P, Schevitz RW, Clawson DK, Bobbitt JL, Dow ER, Gamboa G, Goodson T, Jr, Hermann RB, Kramer RM, McClure DB, Mihelich ED, Putnam LE, Sharp JD, Stark DH, Teater C, Warrick W, Jones ND (1991) Structure of recombinant human rheumatoid arthritic synovial fluid phospholipase A2 at 2.2Å resolution. Nature 352:79–82
Yoshizumi K, Liu S-Y, Miyata T, Saita S, Ohno M, Iwanaga S, Kihara H (1990) Purification and amino acid sequence of basic protein I, a lysine-49-phospholipase A2 with low activity, from the venom of Trimeresurus flavoviridis (habu snake). Toxicon 28:43–54
Author information
Authors and Affiliations
Additional information
Correspondence to: M. Ohno
Rights and permissions
About this article
Cite this article
Ogawa, T., Kitajima, M., Nakashima, Ki. et al. Molecular evolution of group II phospholipases A2 . J Mol Evol 41, 867–877 (1995). https://doi.org/10.1007/BF00173166
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00173166