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

Vallon O, Bulté L, Kuras R, Olive J, Wollman FA: Extensive accumulation of an extracellular L-amino acid oxidase during gametogenesis of Chlamydomonas reinhardtii . Eur J Biochem 1993, 215(2):351–360. 10.1111/j.1432-1033.1993.tb18041.x Du XY, Clemetson KJ: Snake venom L-amino acid oxidases. Toxicon 2002, 40(6):659–665. 10.1016/S0041-0101(02)00102-2 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 snail Aplysia californica . Chemistry 2009, 15(7):1597–1603. 10.1002/chem.200801696 Chen WM, Sheu FS, Sheu SY: Novel L-amino acid oxidase with algicidal activity against toxic cyanobacterium Microcystis aeruginosa synthesized by a bacterium Aquimarina sp . Enzyme Microb Technol 2011, 49(4):372–379. 10.1016/j.enzmictec.2011.06.016 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. Nuutinen JT, Marttinen E, Soliymani R, Hildén K, Timonen S: L-amino acid oxidase of the fungus Hebeloma cylindrosporum displays substrate preference towards glutamate. Microbiology 2012, 158(Pt 1):272–283. 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 Curti B, Ronchi S, Pilone Simonetta M: D- and L-amino acid oxidases. In Chemistry and biochemistry of flavoenzymes, Volume 3. Edited by: Müller F. Boca Raton: CRC Press; 1992:69–94. Kommoju PR, Macheroux P, Ghisla S: Molecular cloning, expression and purification of L-amino acid oxidase from the Malayan pit viper Calloselasma rhodostoma . Protein Expr Purif 2007, 52(1):89–95. 10.1016/j.pep.2006.09.016 Li R, Zhu S, Wu J, Wang W, Lu Q, Clemetson KJ: L-amino acid oxidase from Naja atra venom activates and binds to human platelets. Acta Biochim Biophys Sin (Shangai) 2008, 40(1):19–26. 10.1111/j.1745-7270.2008.00372.x 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 from Bothrops pauloensis snake venom. Biochimie 2009, 91(4):490–501. 10.1016/j.biochi.2008.12.004 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 from Agkistrodon blomhoffii ussurensis . Biochimie 2010, 92(4):343–349. 10.1016/j.biochi.2010.01.013 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 from Bothrops atrox snake venom. Biochimie 2011, 93(5):941–947. 10.1016/j.biochi.2011.01.009 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 from Agkistrodon contortrix laticinctus snake venom: preliminary crystallographic data. Arch Biochem Biophys 1999, 368(2):285–290. 10.1006/abbi.1999.1287 Stiles BG, Sexton FW, Weinstein SA: Antibacterial effects of different snake venoms: purification and characterization of antibacterial proteins from Pseudechis australis (Australian king brown or mulga snake) venom. Toxicon 1991, 29(9):1129–1141. 10.1016/0041-0101(91)90210-I Samel M, Tõnismägi K, Rönnholm G, Vija H, Siigur J, Kalkkinen N, Siigur E: L-amino acid oxidase from Naja naja oxinana venom. Comp Biochem Physiol B Biochem Mol Biol 2008, 149(4):572–580. 10.1016/j.cbpb.2007.11.008 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 from Daboia russellii siamensis venom. Toxicon 2009, 54(6):763–771. 10.1016/j.toxicon.2009.06.004 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 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 from Bothrops leucurus venom. Biochim Biophys Acta 2011, 1810(7):683–694. 10.1016/j.bbagen.2011.04.003 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 from Bothrops pirajai induces apoptosis in BCR-ABL-positive cells and potentiates imatinib mesylate effect. Basic Clin Pharmacol Toxicol 2013, 113(2):103–112. 10.1111/bcpt.12073 Vargas LJ, Quintana JC, Pereañez JA, Núñez V, Sanz L, Calvete J: Cloning and characterization of an antibacterial L-amino acid oxidase from Crotalus durissus cumanensis venom. Toxicon 2013, 64: 1–11. doi:10.1016/j.toxicon.2012.11.027 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 from Dorstenia 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 Zhang L, Wu WT: Isolation and characterization of ACTX-6: a cytotoxic L-amino acid oxidase from Agkistrodon acutus snake venom. Nat Prod Res 2008, 22(6):554–563. 10.1080/14786410701592679 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 of Bothrops snake venoms and isolated toxins on human lymphocyte DNA. Toxicon 2013, 65: 9–14. doi: 10.1016/j.toxicon.2012.12.020 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 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 from Bothrops pirajai snake venom. Bioorg Med Chem 2006, 14(20):7034–7043. 10.1016/j.bmc.2006.06.025 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 from Bothrops atrox snake venom. Comp Biochem Physiol A Mol Integr Physiol 2008, 151(4):542–550. 10.1016/j.cbpa.2008.07.007 Imlay JA: Pathways of oxidative damage. Annu Rev Microbiol 2003, 57: 395–418. 10.1146/annurev.micro.57.030502.090938 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 from Bothropoides mattogrosensis pitviper venom. PLoS ONE 2012, 7(3):e33639. 10.1371/journal.pone.0033639 Yang CA, Cheng CH, Liu SY, Lo CT, Lee JW, Peng KC: Identification of antibacterial mechanism of L-amino acid oxidase derived from Trichoderma harzianum ETS 323. FEBS J 2011, 278(18):3381–3394. 10.1111/j.1742-4658.2011.08262.x 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 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 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 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 Schafer KA: The cell cycle: a review. Vet Pathol 1998, 35(6):461–478. 10.1177/030098589803500601 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. 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 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 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. 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 Amarante-Mendes GP, Green DR: The regulation of apoptotic cell death. Braz J Med Biol Res 1999, 32(9):1053–1061. 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 Zivny J, Klener P Jr, 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 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 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 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 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 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 from Agkistrodon halys pallas venom. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 5):974–977. Wei JF, Yang HW, Wei XL, Qiao LY, Wang WY, He SH: Purification, characterization and biological activities of the L-amino acid oxidase from Bungarus fasciatus snake venom. Toxicon 2009, 54(3):262–271. 10.1016/j.toxicon.2009.04.017 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 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. 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 from Lachesis muta snake venom. Toxicon 2012, 60(7):1263–1276. 10.1016/j.toxicon.2012.08.008 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 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 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 from Vipera berus berus (common viper) venom. Biochim Biophys Acta 2006, 1764(4):707–714. 10.1016/j.bbapap.2006.01.021 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 Zhang L, Wei LJ: ACTX-8, a cytotoxic L-amino acid oxidase isolated from Agkistrodon acutus snake venom, induces apoptosis in Hela cervical cancer cells. Life Sci 2007, 80(13):1189–1197. 10.1016/j.lfs.2006.12.024 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 Liu JW, Chai MQ, Du XY, Song JG, Zhou YC: Purification and characterization of L-amino acid oxidase from Agkistrodon halys pallas venom. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2002, 34(3):305–310. Article in Chinese 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 from Bothrops moojeni : biochemical and functional characterization. Int J Biol Macromol 2007, 41(2):132–140. 10.1016/j.ijbiomac.2007.01.006 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