Comparative venom gland transcriptome surveys of the saw-scaled vipers (Viperidae: Echis) reveal substantial intra-family gene diversity and novel venom transcripts

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Casewell, Nicholas R ^a   Harrison, Robert A ^b   Wüster, Wolfgang ^a   Wagstaff, Simon C ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACID LIPASE; AMINO ACID OXIDASE; C TYPE LECTIN; COMPLEMENTARY DNA; CYSTEINE RICH SECRETORY PROTEIN; DIPEPTIDYL PEPTIDASE; DIPEPTIDYL PEPTIDASE III; DISINTEGRIN; GROWTH FACTOR; HYALURONIDASE; LECTIN; LEVO AMINO ACID OXIDASE; LYSOSOMAL ACID LIPASE; MEMBRANE METALLOENDOPEPTIDASE; METALLOPROTEINASE; PHOSPHOLIPASE A2 GROUP II; SECRETORY PROTEIN; SERINE PROTEINASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; VENOM GLAND TRANSCRIPTOME; MESSENGER RNA; VIPER VENOM;

ARTICLE; CONTROLLED STUDY; DNA LIBRARY; ECHIS CARINATUS SOCHUREKI; ECHIS OCELLATUS; ECHIS PYRAMIDUM LEAKEYI; ECHIS VENOM; EVOLUTIONARY ADAPTATION; EXPRESSED SEQUENCE TAG; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE INSERTION; GENETIC IDENTIFICATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; NONHUMAN; PREY; SAW SCALED VIPER; SNAKE; ADAPTATION; ANIMAL; COMPARATIVE STUDY; ENZYMOLOGY; GENETIC DATABASE; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SECRETION;

ECHIS; ECHIS CARINATUS; ECHIS CARINATUS SOCHUREKI; ECHIS COLORATUS; ECHIS OCELLATUS; ECHIS PYRAMIDUM LEAKEYI; VERTEBRATA; VIPERIDAE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DATABASES, GENETIC; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENETIC VARIATION; HUMANS; RNA, MESSENGER; VIPER VENOMS; VIPERIDAE;

EID: 71949086303     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-564     Document Type: Article

References (88)

1. Aird SD. Ophidian envenomation strategies and the role of purines. Toxicon 2002, 40:335-393. 10.1016/S0041-0101(01)00232-X, 11738231.
2. Chippaux JP, Williams V, White J. Snake venom variability: methods of study, results and interpretation. Toxicon 1991, 29:1279-1303. 10.1016/0041-0101(91)90116-9, 1814005.
3. Gutiérrez JM, Lomonte B, Leün G, Alape-Girün A, Flores-Díaz M, Sanz L, Angulo Y, Calvete JJ. Snake venomics and antivenomics: proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J Proteomics 2009, 72:165-182. 10.1016/j.jprot.2009.01.008, 19344652.
4. Sasa M. Diet and snake venom evolution: can local selection alone explain intraspecific venom variation?. Toxicon 1999, 37:249-252. 10.1016/S0041-0101(98)00121-4, 10078860.
5. Sasa M. Reply. Toxicon 1999, 37:259-260.
6. Mebs D. Toxicity in animals. Trends in evolution?. Toxicon 2001, 39:87-96. 10.1016/S0041-0101(00)00155-0, 10936625.
7. Daltry JC, Wüster W, Thorpe RS. Diet and snake venom evolution. Nature 1996, 379:537-540. 10.1038/379537a0, 8596631.
8. Kordiš D, Gubenšek F. Adaptive evolution of animal toxin multigene families. Gene 2000, 261:43-52. 10.1016/S0378-1119(00)00490-X, 11164036.
9. Jorge da Silva N, Aird SD. Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comp Biochem Physiol 2001, 128C:425-456.
10. Barlow A, Pook CE, Harrison RA, Wüster W. Co-evolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc R Soc B 2009, 276:2443-2449. 10.1098/rspb.2009.0048, 19364745.
11. Creer S, Malhotra A, Thorpe RS, Stõcklin R, Favreau P, Chou WH. 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. J Mol Evol 2003, 56:317-329. 10.1007/s00239-002-2403-4, 12612835.
12. Sanz L, Gibbs HL, Mackessy SP, Calvete JJ. Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J Proteome Res 2006, 5:2098-2112. 10.1021/pr0602500, 16944921.
13. Warrell DA. Snake venoms in science and clinical medicine. 1. Russell's viper: biology, venom and treatment of bites. Trans R Soc Trop Med Hyg 1989, 83:732-740. 10.1016/0035-9203(89)90311-8, 2533418.
14. Prasad NB, Uma B, Bhat SKG, Gowda TV. Comparative characterization of Russell's viper (Daboia/Vipera russelli) venoms from different regions of Indian peninsula. Biochim Biophys Acta 1999, 1428:121-136.
15. Shashidharamurthy R, Jagadeesha DK, Girish KS, Kemparaju K. Variation in biochemical and pharmacological properties of Indian cobra (Naja naja) venom due to geographical distribution. Mol Cell Biochem 229:93-101. 10.1023/A:1017972511272, 11936852.
16. Theakston RDG, Phillips RE, Warrell DA, Galigedera Y, Abeysekera DT, Dissanayake P, Hutton RA, Aloysius DJ. Failure of India (Haffkine) antivenom in treatment of Vipera russelli pulchella (Russell's viper) envenoming in Sri Lanka. Toxicon 1989, 27:82.
17. Galán JA, Sánchez EE, Rodríguez-Acosta A, Pérez JC. Neutralization of venoms from two Southern Pacific rattlesnakes (Crotalus helleri) with commercial antivenoms and endothermic animal sera. Toxicon 2004, 43:791-799. 10.1016/j.toxicon.2004.03.009, 15284013.
18. Visser LE, Kyei-Faried S, Belcher DW, Geelhoed DW, Schagen van Leeuwen J, van Roosmalen J. Failure of a new antivenom to treat Echis ocellatus snake bite in rural Ghana: the importance of quality surveillance. Trans R Soc Trop Med Hyg 2008, 102:445-450. 10.1016/j.trstmh.2007.11.006, 18190937.
19. Warrell DA, Davidson NM, Greenwood BM, Ormerod LD, Pope HM, Watkins BJ, Prentice CRM. Poisoning by bites of the saw-scaled or carpet viper (Echis carinatus) in Nigeria. QJM 1977, 46:33-62.
20. Warrell DA. Clinical toxicology of snakebite in Africa, the Middle East/Arabian Peninsula and Asia. Handbook of clinical toxicology of animal venoms and poisons 1995, 433-595. Boca Raton, Florida: CRC Press, Meier J, White J.
21. Habib AG, Gebi UI, Onyemelukwe GC. Snake bite in Nigeria. Afr J Med Med Sci 2001, 30:171-178.
22. Gillissen A, Theakston RDG, Barth J, May B, Krieg M, Warrell DA. Neurotoxicity, haemostatic disturbances and haemolytic anaemia after a bite by a Tunisian saw-scaled or carpet viper (Echis 'pyramidum'-complex): Failure of antivenom treatment. Toxicon 1994, 32:937-944. 10.1016/0041-0101(94)90372-7, 7985198.
23. Kochar DK, Tanwar PD, Norris RL, Sabir M, Nayak KC, Agrawal TD, Purohit VP, Kochar A, Simpson ID. Rediscovery of severe saw-scaled viper (Echis sochureki) envenoming in the Thar Desert region of Rajasthan, India. Wilderness Enviro Med 2007, 18:75-85.
24. Warrell DA. Unscrupulous marketing of snake bite antivenoms in Africa and Papua New Guinea: choosing the right product-'What's in a name?'. Trans Royal Soc Trop Med Hygiene 2008, 102(5):397-399.
25. Pook CE, Joger U, Stümpel N, Wüster W. When continents collide: phylogeny, historical biogeography and systematics of the medically important viper genus Echis (Squamata: Serpentes: Viperidae). Mol Phylogenet Evol 2009, doi:10.1016/j.ympev.2009.08.002.
26. Wagstaff SC, Harrison RA. Venom gland EST analysis of the saw-scaled viper, Echis ocellatus, reveals novel α9β1 integrin-binding motifs in venom metalloproteinases and a new group of putative toxins, renin-like aspartic proteases. Gene 2006, 377:21-32. 10.1016/j.gene.2006.03.008, 16713134.
27. Paine MJ, Desmond HP, Theakston RDG, Crampton JM. Gene expression in Echis carinatus (carpet viper) venom glands following milking. Toxicon 1992, 30:379-386. 10.1016/0041-0101(92)90534-C, 1626320.
28. Wagstaff SC, Sanz L, Juárez P, Harrison RA, Calvete JJ. Combined snake venomics and venom gland transcriptomic analysis of the ocellated carpet viper, Echis ocellatus. J Proteomics 2009, 71(6):609-623. 10.1016/j.jprot.2008.10.003, 19026773.
29. Harrison RA, Ibison F, Wilbraham D, Wagstaff SC. Identification of cDNAs encoding viper venom hyaluronidases: cross-generic sequence conservation of full-length and unusually short variant transcripts. Gene 2007, 392:22-33. 10.1016/j.gene.2006.10.026, 17210232.
30. Fox JW, Serrano SMT. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 2005, 45:969-985. 10.1016/j.toxicon.2005.02.012, 15922769.
31. Warrell DA, Pope HM, Prentice CRM. Disseminated intravascular coagulation caused by the carpet viper (Echis carinatus): Trial of Heparin. Brit J Haemat 1976, 33:335-342. 10.1111/j.1365-2141.1976.tb03549.x, 1276079.
32. Fox JW, Serrano SMT. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J 2008, 275:3016-3030. 10.1111/j.1742-4658.2008.06466.x, 18479462.
33. Huang TF, Holt JC, Lukasiewicz H, Niewiarowski S. Trigamin. A low molecular weight peptide inhibiting fibrinogen with platelet receptors expressed on glycoprotein IIb-IIIa complex. J Biol Chem 1987, 262:16157-16163.
34. Calvete JJ, Marcinkiewicz C, Monleün D, Esteve V, Celda B, Juárez P, Sanz L. Snake venom disintegrins: evolution of structure and function. Toxicon 2005, 45:1063-1074. 10.1016/j.toxicon.2005.02.024, 15922775.
35. Wagstaff SC, Favreau P, Cheneval O, Laing GD, Wilkinson MC, Miller RL, Stöcklin R, Harrison RA. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun 2008, 365(4):650-656. 10.1016/j.bbrc.2007.11.027, 18029259.
36. Shimokawa K, Jai LG, Wang XM, Fox JW. Expression, activation and processing of the recombinant snake venom metalloproteinase, pro-atrolysin E. Arch Biochem Biophys 1996, 335:283-294. 10.1006/abbi.1996.0509, 8914925.
37. Okuda D, Koike H, Morita T. A new gene structure of the disintegrin family: a subunit of dimeric disintegrin has a short coding region. Biochemistry 2002, 41:14248-14254. 10.1021/bi025876s, 12450389.
38. Francischetti IMB, My-Pharm V, Harrison J, Garfield MK, Ribeiro JMC. Bitis gabonica (Gaboon viper) snake venom gland: toward a catalog for the full-length transcripts (cDNA) and proteins. Gene 2004, 357:55-69.
39. Juárez P, Wagstaff SC, Sanz L, Harrison RA, Calvete JJ. Molecular cloning of Echis ocellatus disintegrins reveals non-venom secreted proteins and a pathway for the evolution of ocellatusin. J Mol Evol 2006, 63:183-193. 10.1007/s00239-005-0269-y, 16830094.
40. Markland FS. Snake venoms and the haemostatic system. Toxicon 1998, 36:1749-1800. 10.1016/S0041-0101(98)00126-3, 9839663.
41. Kini RM. Anticoagulant proteins from snake venoms: structure, function and mechanism. Biochem J 2006, 397:377-387. 1533313, 16831131, 10.1042/BJ20060302.
42. Peng M, Lu W, Beviglia V, Niewiarowski S, Kirby EP. Echicetin: a snake venom protein that inhibits binding of von Willebrand factor and alboaggregins to platelet glycoprotein Ib. Blood 1993, 81:2321-2328.
43. Polgár J, Magnenat EM, Peitsch MC, Wells TN, Saqi MS, Clemetson KJ. Amino acid sequence of the alpha subunit and computer modelling of the alpha and beta subunits of echicetin from the venom of Echis carinatus (saw-scaled viper). Biochem J 1997, 323:533-537. 1218352, 9163349.
44. Siigur E, Aaspõllu A, Trummal K, Tõnismägi K, Tammiste I, Kalkkinen N, Siigur J. Factor X activator from Vipera lebetina venom is synthesized from different genes. Biochim Biophys Acta Prot Proteomics 2004, 1702:41-51.
45. Bharati K, Hasson SS, Oliver J, Laing GD, Theakston RDG, Harrison RA. Molecular cloning of phospholipases A2 from venom glands of Echis carpet vipers. Toxicon 2003, 41:941-947. 10.1016/S0041-0101(02)00312-4, 12875867.
46. Kemparaju K, Prasad BN, Gowda VT. Purification of a basic phospholipase A2 from Indian saw-scaled viper (Echis carinatus) venom: characterization of antigenic, catalytic and pharmacological properties. Toxicon 1994, 32:1187-1196. 10.1016/0041-0101(94)90348-4, 7846689.
47. Kemparaju K, Krishnakanth TP, Gowda VT. Purification and characterization of a platelet aggregation inhibitor acidic phospholipase A2 from Indian saw-scaled viper (Echis carinatus) venom. Toxicon 1999, 37:1659-1671. 10.1016/S0041-0101(99)00104-X, 10519645.
48. Jasti J, Paramasivam M, Srinivasan A, Singh TP. Structure of an acidic phospholipase A2 from Indian saw-scaled viper (Echis carinatus) at 2.6 Å resolution reveals a novel intermolecular interaction. Acta Cryst 2004, D60:66-72.
49. Zhou X, Tan TC, Valiyaveettil S, Go ML, Kini RM, Velazquez-Campoy A, Sivaraman J. Structural characterization of myotoxic Ecarpholin S from Echis carinatus venom. Biophysical J 2008, 95:3366-3380.
50. Petan T, Križaj I, Pungerčar J. Restoration of enzymatic activity in a Ser-49 phospholipase A2 homologue decreases its Ca2+-independant membrane-damaging activity and increases its toxicity. Biochemistry 2007, 46:12795-12809. 10.1021/bi701304e, 17927217.
51. Wüster W, Peppin L, Pook CE, Walker DE. A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Mol Phylogenet Evol 2008, 49(2):445-459. 10.1016/j.ympev.2008.08.019, 18804544.
52. Cidade DAP, Simão TA, Dávila AMR, Wagner G, Junqueira-de-Azevedo ILM, Ho PL, Bon C, Zingali RB, Albano RM. Bothrops jararaca venom gland transcriptome: Analysis of the gene expression pattern. Toxicon 2006, 48:437-461. 10.1016/j.toxicon.2006.07.008, 16905169.
53. Pahari S, Mackessy SP, Kini RM. The venom gland transcriptome of the Desert Massasauga rattlesnake (Sistrurus catenatus edwardsii): towards an understanding of venom composition among advanced snakes (Superfamily Colubroidea). BMC Mol Biol 2007, 8:115. 2242803, 18096037, 10.1186/1471-2199-8-115.
54. Župunski V, Kordiš D, Gubenšek F. Adaptive evolution in the snake venom Kunitz/BPTI protein family. FEBS Letters 2003, 547:131-136. 10.1016/S0014-5793(03)00693-8, 12860400.
55. Du XY, Clemetson KJ. Snake venom L-amino acid oxidases. Toxicon 2002, 40:659-665. 10.1016/S0041-0101(02)00102-2, 12175601.
56. Junqueira-de-Azevedo ILM, Ho PL. A survey of gene expression and diversity in the venom glands of the pit viper snake Bothrops insularis through the generation of expressed sequence tags (ESTs). Gene 2002, 299:279-291. 10.1016/S0378-1119(02)01080-6, 12459276.
57. Kashima S, Roberto PG, Soares AM, Astolfi-Filho S, Pereira JO, Giuliati S, Faria M, Xavier MAS, Fontes MRM, Giglio JR, Franca SC. Analysis of Bothrops jararacussu venomous gland transcriptome focusing on structural and functional aspects: I - gene expression profile of highly expressed phospholipases A2. Biochimie 2004, 86:211-219. 10.1016/j.biochi.2004.02.002, 15134836.
58. Junqueira-de-Azevedo ILM, Ching ATC, Carvalho E, Faria F, Nishiyama ML, Ho PL, Diniz MRV. Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of Cobra (Elapidae) venoms: Implications for snake toxin repertoire evolution. Genetics 2006, 173:877-889. 1526512, 16582429, 10.1534/genetics.106.056515.
59. Zhang B, Liu Q, Yin W, Zhang X, Huang Y, Luo Y, Qiu P, Su X, Yu J, Hu S, Yan G. Transcriptomic analysis of Deinagkistrodon acutus venomous gland focusing on cellular structure and functional aspects using expressed sequence tags. BMC Genomics 2006, 7:152. 1525187, 16776837, 10.1186/1471-2164-7-152.
60. Yamazaki Y, Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon 2004, 44:227-231. 10.1016/j.toxicon.2004.05.023, 15302528.
61. Gorbacheva EV, Starkov VG, Tsetlin VI, Utkin YN, Vulfius CA. Viperidae snake venoms block nicotinic acetylcholine receptors and voltage-gated Ca2+ channels in identified neurons of fresh-water snail Lymnaea stagnalis. Biochem (Moscow) A Membrane Cell Biol 2008, 2:14-18.
62. Kemparaju K, Girish KS. Snake venom hyaluronidase: a therapeutic target. Cell Biochem Funct 2006, 24:7-12. 10.1002/cbf.1261, 16245359.
63. Doley R, Tram NNB, Reza MA, Kini RM. Unusual accelerated rate of deletions and insertions in toxin genes in the venom glands of the pygmy copperhead (Austrelaps labialis) from Kangaroo Island. BMC Evol Biol 2008, 8:70. 2287176, 18307759, 10.1186/1471-2148-8-70.
64. Li Y, Qin Y, Li H, Wu R, Yan C, Du H. Lysosomal acid lipase over-expression disrupts lamellar body genesis and alveolar structure in the lung. Int J Exp Path 2007, 88:427-436.
65. Qu P, Du H, Wilkes DS, Yan C. Critical roles of lysosomal acid lipase in T cell development and function. Am J Pathol 2009, 174:944-956. 2665754, 19179613, 10.2353/ajpath.2009.080562.
66. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
67. Baral PK, Jajčanin-Jozić N, Deller S, Macheroux P, Abramić M, Gruber K. The first structure of dipeptidyl-peptidase III provides insight into the catalytic mechanism and mode of substrate binding. J Biol Chem 2008, 283(32):22316-22324. 10.1074/jbc.M803522200, 18550518.
68. Lee CM, Snyder SH. Dipeptidyl-aminopeptidase III of rat brain: selective affinity for enkephalin and angiotensin. J Biol Chem 1982, 257(20):12043-12050.
69. Abramić M, Zubanović M, Vitale L. Dipeptidyl peptidase III from human erythrocytes. Biol Chem Hoppe Seyler 1988, 369:29-38.
70. Skurk T, Lee YM, Hauner H. Angiotensin II and its metabolites stimulate PAI-1 protein release from human adipocytes in primary culture. Hypertension 2001, 37:1336-1340.
71. Turner AJ, Isaac RE, Coates D. The neprilysin (NEP) family of zinc metalloendopeptidases: Genomics and function. Bioessays 2001, 23(3):261-269. 10.1002/1521-1878(200103)23:3<261::AID-BIES1036>3.0.CO;2-K, 11223883.
72. Matsas R, Fulcher IS, Kenny AJ, Turner AJ. Substance P and (Leu)enkephalin are hydrolysed by an enzyme in pig caudate synaptic membranes that is identical with the endopeptidase of kidney microvilli. Proc Natl Acad Sci USA 1983, 80:3111-3115. 393984, 6190172, 10.1073/pnas.80.10.3111.
73. Isaac RE. Neuropeptide-degrading endopeptidase activity of locust (Schistocerca gregaria) synaptic membranes. Biochem J 1988, 255:843-847. 1135318, 3063256.
74. Fry BG, Scheib H, Weerd L, Young B, McNaughtan J, Ramjan SFR, Vidal N, Poelmann RE, Norman JA. Evolution of an arsenal. Mol Cell Prot 2008, 7:215-246.
75. Deshimaru M, Ogawa T, Nakashima KI, Nobuhisa I, Chijiwa T, Shimohigashi Y, Fukumaki Y, Niwa M, Yamashina I, Hattori S, Ohno M. Accelerated evolution of crotalinae snake venom gland serine proteases. FEBS Letters 1996, 397:83-88. 10.1016/S0014-5793(96)01144-1, 8941719.
76. Ogawa T, Chijiwa T, Oda-Ueda N, Ohno M. Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon 2005, 45:1-14. 10.1016/j.toxicon.2004.07.028, 15581677.
77. Nakashima K, Ogawa T, Oda N, Hattori M, Sakaki Y, Kihara H, Ohno M. Accelerated evolution of Trimeresurus flavovirids venom gland phosphlipase A2 isoenzymes. Proc Natl Acad Sci USA 1993, 90:5964-5968. 46847, 8327468, 10.1073/pnas.90.13.5964.
78. Brecher P, Kuan HT. Lipoprotein lipase and acid lipase activity in rabbit brain microvessels. J Lipid Res 1979, 20:464-471.
79. Sandbank U, Djaldetti M. Effect of Echis colorata venom inoculation on the nervous system of the dog and guinea pig. Acta Neuropath 1966, 6:61-69. 10.1007/BF00691082, 4165220.
80. The PartiGene EST-software pipeline at the nematode and neglected genomics database. , http://www.nematodes.org/bioinformatics/PartiGene/index.shtml
81. Parkinson J, Anthony A, Wasmuth J, Schmid R, Hedley A, Blaxter M. PartiGene - constructing partial genomes. Bioinformatics 2004, 20:1398-1404. 10.1093/bioinformatics/bth101, 14988115.
82. Glenner GG, Folk JE. Glutamyl peptidases in rat and guinea pig kidney slices. Nature 1961, 192:338-340. 10.1038/192338a0, 13899212.
83. Marchio S, Lahdenranta J, Schlingemann RO, Valdembri D, Wesseling P, Arap MA, Hajitou A, Ozawa MG, Trepel M, Giordano RJ, Nanus DM, Dijkman HB, Ooserwijk E, Sidman RL, Cooper MD, Bussolino F, Pasqualini R, Arap W. Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 2004, 5:151-162. 10.1016/S1535-6108(04)00025-X, 14998491.
84. Fournie-Zaluski MC, Fassot C, Valentin B, Djordjijevic D, Reaux-Le Goazigo A, Corvol P, Roques BP, Llorens-Cortes C. Brain renin-angiotensin system blockade by systemically active aminopeptidase A inhibitors: a potential treatment of salt-dependent hypertension. Proc Natl Acad Sci USA 2004, 101:7775-7780. 419682, 15136730, 10.1073/pnas.0402312101.
85. Fürstenau CR, Trentin DDS, Barreto-Chaves MLM, Sarkis JJF. Ecto-nucleotide pyrophosphate/phosphodiesterase as part of a multiple system for nucleotide hydrolysis by platelets from rats: Kinetic characterization and biochemical properties. Platelets 2006, 17(2):84-91. 10.1080/09537100500246641, 16421009.
86. Taborska E. Intraspecies variability of the venom of Echis carinatus. Physiol Bohemoslov 1971, 20:307-318.
87. Sales PBV, Santoro ML. Nucleotide and DNase activities in Brazilian snake venoms. Comp Biochem Physiol C Toxicol Pharmacol 2008, 147(1):85-95. 10.1016/j.cbpc.2007.08.003, 17904425.
88. Champagne DE. Antihemostatic molecules from saliva of blood-feeding arthropods. Pathophysiol Haemos Thromb 2005, 34:221-227.