Snake venom L-amino acid oxidases: An overview on their antitumor effects

Journal of Venomous Animals and Toxins Including Tropical Diseases

Volumn 20, Issue 1, 2014, Pages

  Costa, Tássia R ^a   Burin, Sandra M ^a   Menaldo, Danilo L ^a   de Castro, Fabíola A ^a   Sampaio, Suely V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antitumor effects; Apoptosis; L amino acid oxidases; Snake venoms

Indexed keywords

AMINO ACID OXIDASE; SNAKE VENOM;

AGKISTRODON CONTORTRIX LATICINCTUS; AGKISTRODON HALYS; AGKISTRODON HALYS PALLAS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BOTHROPS ATROX; BOTHROPS MOOJENI; BOTHROPS PIRAJAI; BUNGARUS FASCIATUS; CALLOSELASMA RHODOSTOMA; CROTALUS ATROX; DEINAGKISTRODON; DNA FRAGMENTATION; DNA REPAIR; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME MECHANISM; ERISTOCOPHIS MACMAHONI; HUMAN; INTRACELLULAR SIGNALING; NONHUMAN; OPHIOPHAGUS HANNAH; POISONOUS SNAKE; PROTEIN PROTEIN INTERACTION; REVIEW; TUMOR CELL; VIPERA BERUS BERUS;

EID: 84921472047     PISSN: 16789180     EISSN: 16789199     Source Type: Journal    
DOI: 10.1186/1678-9199-20-23     Document Type: Review

References (61)

1. Vallon O, Bulté L, Kuras R, Olive J, Wollman FA. Extensive accumulation of an extracellular L-amino acid oxidase during gametogenesis ofChlamydomonas reinhardtii. Eur J Biochem 1993, 215(2):351-360. 10.1111/j.1432-1033.1993.tb18041.x, 8344302.
2. Du XY, Clemetson KJ. Snake venom L-amino acid oxidases. Toxicon 2002, 40(6):659-665. 10.1016/S0041-0101(02)00102-2, 12175601.
3. Kamio M, Ko KC, Zheng S, Wang B, Collins SL, Gadda G, Tai PC, Derby CD. The chemistry of escapin: identification and quantification of the components in the complex mixture generated by an L-amino acid oxidase in the defensive secretion of the sea snailAplysia californica. Chemistry 2009, 15(7):1597-1603. 10.1002/chem.200801696, 19130530.
4. Chen WM, Sheu FS, Sheu SY. Novel L-amino acid oxidase with algicidal activity against toxic cyanobacteriumMicrocystis aeruginosasynthesized by a bacteriumAquimarina sp. Enzyme Microb Technol 2011, 49(4):372-379. 10.1016/j.enzmictec.2011.06.016, 22112563.
5. Wang F, Li R, Xie M, Li A. The serum of rabbitfish (Siganus oramin) has antimicrobial activity to some pathogenic organisms and a novel serum L-amino acid oxidase is isolated. Fish Shellfish Immunol 2011, 30(4-5):1095-1108.
6. Nuutinen JT, Marttinen E, Soliymani R, Hildén K, Timonen S. L-amino acid oxidase of the fungusHebeloma cylindrosporumdisplays substrate preference towards glutamate. Microbiology 2012, 158(Pt 1):272-283.
7. Guo C, Liu S, Yao Y, Zhang Q, Sun MZ. Past decade study of snake venom L-amino acid oxidase. Toxicon 2012, 60(3):302-311. 10.1016/j.toxicon.2012.05.001, 22579637.
8. Curti B, Ronchi S, Pilone Simonetta M. D- and L-amino acid oxidases. Chemistry and biochemistry of flavoenzymes, Volume 3 1992, 69-94. Boca Raton: CRC Press, Müller F.
9. Kommoju PR, Macheroux P, Ghisla S. Molecular cloning, expression and purification of L-amino acid oxidase from the Malayan pit viperCalloselasma rhodostoma. Protein Expr Purif 2007, 52(1):89-95. 10.1016/j.pep.2006.09.016, 17127077.
10. Li R, Zhu S, Wu J, Wang W, Lu Q, Clemetson KJ. L-amino acid oxidase fromNaja atravenom activates and binds to human platelets. Acta Biochim Biophys Sin (Shangai) 2008, 40(1):19-26.
11. Rodrigues RS, da Silva JF, Boldrini França J, Fonseca FP, Otaviano AR, Henrique Silva F, Hamaguchi A, Magro AJ, Braz AS, dos Santos JI, Homsi-Brandeburgo MI, Fontes MR, Fuly AL, Soares AM, Rodrigues VM. Structural and functional properties of Bp-LAAO, a new L-amino acid oxidase isolated fromBothrops pauloensissnake venom. Biochimie 2009, 91(4):490-501. 10.1016/j.biochi.2008.12.004, 19135502.
12. Sun MZ, Guo C, Tian Y, Chen D, Greenaway FT, Liu S. Biochemical, functional and structural characterization of Akbu-LAAO: a novel snake venom L-amino acid oxidase fromAgkistrodon blomhoffii ussurensis. Biochimie 2010, 92(4):343-349. 10.1016/j.biochi.2010.01.013, 20100538.
13. de Melo Alves-Paiva R, de Freitas Figueiredo R, Antonucci GA, Paiva HH, de Lourdes Pires Bianchi M, Rodrigues KC, Lucarini R, Caetano RC, Linhari Rodrigues Pietro RC, Gomes Martins CH, de Albuquerque S, Sampaio SV. Cell cycle arrest evidence, parasiticidal and bactericidal properties induced by L-amino acid oxidase fromBothrops atroxsnake venom. Biochimie 2011, 93(5):941-947. 10.1016/j.biochi.2011.01.009, 21300133.
14. Souza DH, Eugenio LM, Fletcher JE, Jiang MS, Garratt RC, Oliva G, Selistre-de-Araújo HS. Isolation and structural characterization of a cytotoxic L-amino acid oxidase fromAgkistrodon contortrix laticinctussnake venom: preliminary crystallographic data. Arch Biochem Biophys 1999, 368(2):285-290. 10.1006/abbi.1999.1287, 10441379.
15. Stiles BG, Sexton FW, Weinstein SA. Antibacterial effects of different snake venoms: purification and characterization of antibacterial proteins fromPseudechis australis(Australian king brown or mulga snake) venom. Toxicon 1991, 29(9):1129-1141. 10.1016/0041-0101(91)90210-I, 1796476.
16. Samel M, Tõnismägi K, Rönnholm G, Vija H, Siigur J, Kalkkinen N, Siigur E. L-amino acid oxidase fromNaja naja oxinanavenom. Comp Biochem Physiol B Biochem Mol Biol 2008, 149(4):572-580. 10.1016/j.cbpb.2007.11.008, 18294891.
17. Zhong SR, Jin Y, Wu JB, Jia YH, Xu GL, Wang GC, Xiong YL, Lu QM. Purification and characterization of a new L-amino acid oxidase fromDaboia russellii siamensisvenom. Toxicon 2009, 54(6):763-771. 10.1016/j.toxicon.2009.06.004, 19523971.
18. Lee ML, Tan NH, Fung SY, Sekaran SD. Antibacterial action of a heat-stable form of L-amino acid oxidase isolated from king cobra (Ophiophagus hannah) venom. Comp Biochem Physiol C Toxicol Pharmacol 2011, 153(2):237-242. 10.1016/j.cbpc.2010.11.001, 21059402.
19. Naumann GB, Silva LF, Silva L, Faria G, Richardson M, Evangelista K, Kohlhoff M, Gontijo CM, Navdaev A, de Rezende FF, Eble JA, Sanchez EF. Cytotoxicity and inhibition of platelet aggregation caused by an L-amino acid oxidase fromBothrops leucurusvenom. Biochim Biophys Acta 2011, 1810(7):683-694. 10.1016/j.bbagen.2011.04.003, 21539897.
20. Burin SM, Ayres LR, Neves RP, Ambrósio L, de Morais FR, Dias-Baruffi M, Sampaio SV, Pereira-Crott LS, de Castro FA. L-amino acid oxidase isolated fromBothrops pirajaiinduces apoptosis in BCR-ABL-positive cells and potentiates imatinib mesylate effect. Basic Clin Pharmacol Toxicol 2013, 113(2):103-112. 10.1111/bcpt.12073, 23551499.
21. Vargas LJ, Quintana JC, Pereañez JA, Núñez V, Sanz L, Calvete J. Cloning and characterization of an antibacterial L-amino acid oxidase fromCrotalus durissus cumanensisvenom. Toxicon 2013, 64:1-11. doi:10.1016/j.toxicon.2012.11.027.
22. Pieme CA, Guru SK, Ambassa P, Kumar S, Ngameni B, Ngogang JY, Bhushan S, Saxena AK. Induction of mitochondrial dependent apoptosis and cell cycle arrest in human promyelocytic leukemia HL-60 cells by an extract fromDorstenia psilurus: a spice from Cameroon. BMC Complement Altern Med 2013, 13:223-231. doi:10.1186/1472-6882-13-223, 10.1186/1472-6882-13-223, 3847675, 24016040.
23. Zhang L, Wu WT. Isolation and characterization of ACTX-6: a cytotoxic L-amino acid oxidase fromAgkistrodon acutussnake venom. Nat Prod Res 2008, 22(6):554-563. 10.1080/14786410701592679, 18415865.
24. Marcussi S, Stábeli RG, Santos-Filho NA, Menaldo DL, Silva Pereira LL, Zuliani JP, Calderon LA, da Silva SL, Antunes LM, Soares AM. Genotoxic effect ofBothropssnake venoms and isolated toxins on human lymphocyte DNA. Toxicon 2013, 65:9-14. doi: 10.1016/j.toxicon.2012.12.020.
25. Ahn MY, Lee BM, Kim YS. Characterization and cytotoxicity of L-amino acid oxidase from the venom of King Cobra (Ophiophagus hannah). Int J Biochem Cell Biol 1997, 29(6):911-919. 10.1016/S1357-2725(97)00024-1, 9304806.
26. Izidoro LFM, Ribeiro MC, Souza GR, Sant'Ana CD, Hamaguchi A, Homsi-Brandeburgo MI, Goulart LR, Beleboni RO, Nomizo A, Sampaio SV, Soares AM, Rodrigues VM. Biochemical and functional characterization of an L-amino acid oxidase isolated fromBothrops pirajaisnake venom. Bioorg Med Chem 2006, 14(20):7034-7043. 10.1016/j.bmc.2006.06.025, 16809041.
27. Alves RM, Antonucci GA, Paiva HH, Cintra ACO, Franco JJ, Mendonça-Franqueiro EP, Dorta DJ, Giglio JR, Rosa JC, Fuly AL, Dias-Baruffi M, Soares AM, Sampaio SV. Evidence of caspase-mediated apoptosis induced by L-amino acid oxidase isolated fromBothrops atroxsnake venom. Comp Biochem Physiol A Mol Integr Physiol 2008, 151(4):542-550. 10.1016/j.cbpa.2008.07.007, 18804547.
28. Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol 2003, 57:395-418. 10.1146/annurev.micro.57.030502.090938, 14527285.
29. Okubo BM, Silva ON, Migliolo L, Gomes DG, Porto WF, Batista CL, Ramos CS, Holanda HHS, Dias SC, Franco OL, Moreno SE. Evaluation of an antimicrobial L-amino acid oxidase and peptide derivatives fromBothropoides mattogrosensispitviper venom. PLoS ONE 2012, 7(3):e33639. 10.1371/journal.pone.0033639, 3306279, 22438972.
30. Yang CA, Cheng CH, Liu SY, Lo CT, Lee JW, Peng KC. Identification of antibacterial mechanism of L-amino acid oxidase derived fromTrichoderma harzianumETS 323. FEBS J 2011, 278(18):3381-3394. 10.1111/j.1742-4658.2011.08262.x, 21781279.
31. Araki S, Ishida T, Yamamoto T, Kaji K, Hayashi H. Induction of apoptosis by hemorrhagic snake venom in vascular endothelial cells. Biochem Biophys Res Commun 1993, 190(1):148-153. 10.1006/bbrc.1993.1023, 8422240.
32. Suhr SM, Kim DS. Identification of the snake venom substance that induces apoptosis. Biochem Biophys Res Commun 1996, 224(1):134-139. 10.1006/bbrc.1996.0996, 8694800.
33. Torii S, Naito M, Tsuruo T. Apoxin I, a novel apoptosis-inducing factor with L-amino acid oxidase activity purified from Western diamondback rattlesnake venom. J Biol Chem 1997, 272(14):9539-9542. 10.1074/jbc.272.14.9539, 9083096.
34. Ande SR, Kommoju PR, Draxl S, Murkovic M, Macheroux P, Ghisla S, Ferrando-May E. Mechanisms of cell death induction by L-amino acid oxidase, a major component of ophidian venom. Apoptosis 2006, 11(8):1439-1451. 10.1007/s10495-006-7959-9, 16770529.
35. Schafer KA. The cell cycle: a review. Vet Pathol 1998, 35(6):461-478. 10.1177/030098589803500601, 9823588.
36. Douglas RM, Haddad GG. Invited review: effect of oxygen deprivation on cell cycle activity: a profile of delay and arrest. J Appl Physiol 2003, 94(5):2068-2083.
37. Vermeulen K, Van Bockstaele DR, Berneman ZN. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 2003, 36(3):131-149. 10.1046/j.1365-2184.2003.00266.x, 12814430.
38. Kerr JF, Winterford CM, Harmon BV. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994, 73(8):2013-2026. 10.1002/1097-0142(19940415)73:8<2013::AID-CNCR2820730802>3.0.CO;2-J, 8156506.
39. Dypbukt JM, Ankarcrona M, Burkitt M, Sjoholm A, Strom K, Orrenius S, Nicotera P. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J Biol Chem 1994, 269(48):30553-30560.
40. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 1995, 92(16):7162-7166. 10.1073/pnas.92.16.7162, 41299, 7638161.
41. Amarante-Mendes GP, Green DR. The regulation of apoptotic cell death. Braz J Med Biol Res 1999, 32(9):1053-1061.
42. Pereira WO, Amarante-Mendes GP. Apoptosis: a programme of cell death or cell disposal?. Scand J Immunol 2011, 73(5):401-407. 10.1111/j.1365-3083.2011.02513.x, 21223349.
43. Zivny J, Klener P, Pytlik R, Andera L. The role of apoptosis in cancer development and treatment: focusing on the development and treatment of hematologic malignancies. Curr Pharm Des 2010, 16(1):11-33. 10.2174/138161210789941883, 20214615.
44. Borner C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003, 39(11):615-647. 10.1016/S0161-5890(02)00252-3, 12493639.
45. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102(1):33-42. 10.1016/S0092-8674(00)00008-8, 10929711.
46. Sharma K, Wang RX, Zhang LY, Yin DL, Luo XY, Solomon JC, Jiang RF, Markos K, Davidson W, Scott DW, Shi YF. Death the Fas way: regulation and pathophysiology of CD95 and its ligand. Pharmacol Ther 2000, 88(3):333-347. 10.1016/S0163-7258(00)00096-6, 11337030.
47. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397(6718):441-446. 10.1038/17135, 9989411.
48. Zhang H, Teng M, Niu L, Wang Y, Wang Y, Liu Q, Huang Q, Hao Q, Dong Y, Liu P. Purification, partial characterization, crystallization and structural determination of AHP-LAAO, a novel L-amino acid oxidase with cell apoptosis-inducing activity fromAgkistrodon halys pallasvenom. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 5):974-977.
49. Wei JF, Yang HW, Wei XL, Qiao LY, Wang WY, He SH. Purification, characterization and biological activities of the L-amino acid oxidase fromBungarus fasciatussnake venom. Toxicon 2009, 54(3):262-271. 10.1016/j.toxicon.2009.04.017, 19393676.
50. Rojkind M, Domínguez-Rosales JA, Nieto N, Greenwel P. Role of hydrogen peroxide and oxidative stress in healing responses. Cell Mol Life Sci 2002, 59(11):1872-1891. 10.1007/PL00012511, 12530519.
51. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65(1-2):55-63.
52. Bregge-Silva C, Nonato MC, de Albuquerque S, Ho PL, de Azevedo IL J, Vasconcelos Diniz MR, Lomonte B, Rucavado A, Díaz C, Gutiérrez JM, Arantes EC. Isolation and biochemical, functional and structural characterization of a novel L-amino acid oxidase fromLachesis mutasnake venom. Toxicon 2012, 60(7):1263-1276. 10.1016/j.toxicon.2012.08.008, 22963728.
53. Ali SA, Stoeva S, Abbasi A, Alam JM, Kayed R, Faigle M, Neumeister B, Voelter W. Isolation, structural, and functional characterization of an apoptosis-inducing L-amino acid oxidase from leaf-nosed viper (Eristocophis macmahoni) snake venom. Arch Biochem Biophys 2000, 384(2):216-226. 10.1006/abbi.2000.2130, 11368308.
54. Torii S, Yamane K, Mashima T, Haga N, Yamamoto K, Fox JW, Naito M, Tsuruo T. Molecular cloning and functional analysis of apoxin I, a snake venom-derived apoptosis-inducing factor with L-amino acid oxidase activity. Biochemistry 2000, 39(12):3197-3205. 10.1021/bi992416z, 10727211.
55. Samel M, Vija H, Ronnholm G, Siigur J, Kalkkinen N, Siigur E. Isolation and characterization of an apoptotic and platelet aggregation inhibiting L-amino acid oxidase fromVipera berus berus(common viper) venom. Biochim Biophys Acta 2006, 1764(4):707-714. 10.1016/j.bbapap.2006.01.021, 16574513.
56. Nicoletti L, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991, 139(2):271-279. 10.1016/0022-1759(91)90198-O, 1710634.
57. Zhang L, Wei LJ. ACTX-8, a cytotoxic L-amino acid oxidase isolated fromAgkistrodon acutussnake venom, induces apoptosis in Hela cervical cancer cells. Life Sci 2007, 80(13):1189-1197. 10.1016/j.lfs.2006.12.024, 17275856.
58. Gomes A, Choudhury SR, Saha A, Mishra R, Giri B, Biswas AK, Debnath A, Gomes A. A heat stable protein toxin (drCT-I) from the Indian Viper (Daboia russelli russelli) venom having antiproliferative, cytotoxic and apoptotic activities. Toxicon 2007, 49(1):46-56. 10.1016/j.toxicon.2006.09.009, 17055549.
59. Liu JW, Chai MQ, Du XY, Song JG, Zhou YC. Purification and characterization of L-amino acid oxidase fromAgkistrodon halys pallasvenom. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2002, 34(3):305-310. Article in Chinese.
60. Stábeli RG, Sant'Ana CD, Ribeiro PH, Costa TR, Ticli FK, Pires MG, Nomizo A, Albuquerque S, Malta-Neto NR, Marins M, Sampaio SV, Soares AM. Cytotoxic L-amino acid oxidase fromBothrops moojeni: biochemical and functional characterization. Int J Biol Macromol 2007, 41(2):132-140. 10.1016/j.ijbiomac.2007.01.006, 17320169.
61. Lee ML, Chung I, Fung SY, Kanthimathi MS, Tan NH. Anti-proliferative activity of king cobra (Ophiophagus hannah) venom L-amino acid oxidase. Basic Clin Pharmacol Toxicol 2013, doi:10.1111/bcpt.12155.