Die antibakterielle Wirkung der LAAO wurde mit dem “disc diffusion assay”
untersucht. Das Enzym inhibiert das Wachstum von Gram positiven und negativen Bakterien.
LAAO induziert den Zelltod in Leucin-auxothropischen und -prototropischen Hefestämmen. Der Vorgang konnte als Apoptose identifiziert werden. Im Falle der Leucin auxothropischen Stämmen konnte die Zugabe von Katalase die Apoptose nicht verhindern.
Es wird angenommen, dass in Anwesenheit von Katalase der Verbrauch von Leucin und die Erzeugung von lokal hohen Konzentrationen von Wasserstoffperoxyd am Ort der Hefezelle für die Induktion von Apoptose verantwortlich sind
LAAO induziert Nekrose in Jurkatzellen. In Anwesenheit von Katalase, ein Enzym, das Wasserstoffperoxyd effizient entfernt, findet ein Wechsel zu Apoptose statt. Im Gegensatz hierzu mit DAAO, einem sehr ähnlichen Enzym, hebt die Anwesenheit von Katalase den Zelltod auf.
zVAD-fmk, ein Caspaseinhibitor mit einem breiten Spektrum, hebt die Apoptose-induzierenden Effekte der LAAO auf. Dies legt die Vermutung nahe, dass die durch LAAO induzierte Apoptose über den Caspase-abhängigen Weg abläuft. Bcl-2, ein antiapoptotisches Protein, inhibiert die Apoptose. Dies lässt die Vermutung zu, dass die LAAO-abhängige Apoptose den “Mitochondrien-Weg” durchläuft.
Hydrophobe und aromatische Aminosäuren werden durch die LAAO schnell aus dem Medium entfernt (oxidiert). Dies ist wahrscheinlich ein weiterer Effekt, der das Zustandekommen der Apoptose unterstützt. Allerdings hebt die nachträgliche Zufuhr dieser Aminosäuren den Effekt nicht auf. Somit ist davon auszugehen, dass noch weitere Effekte eine Rolle spielen.
Veränderungen des FCS, das dem Medium zugegeben wurde, könnte ein weiterer Faktor bei der Apoptose Induktion sein da nachträgliche/nochmalige Zugabe von FCS den Apoptoseeffekt vermindert.
Glycanreste scheinen bei der Induktion der Toxizität eine wichtige Rolle zu spielen.
Dies folgt aus der Beobachtung, dass Abspaltung der Sialinsäurereste den toxischen Effekt erheblich (>20%) reduziert. Die am Glycan endständig gebundenen Sialinsäuren scheinen beim Binden an die Zelloberfläche und bei der Internalisierung der LAAO wichtig zu sein.
8. Own contributions / Eigenabgrenzung
1. The work presented in this chapter 3 was as a part of collaboration between Prof.
Dr. Sandro Ghisla, Prof. Dr. Peter Macheroux and Prof. Dr. Kai-Uwe Fröhlich (PM and KUF are at the University of Graz). The entire work presented in this chapter was done by myself at the Institute of Microbiology, Biochemistry and Molecular biology University of Graz, Graz, Austria.
2. The work presented in this chapter 4 was done by myself in Graz. Dr. Michael Murkovic carried out the amino acid analysis of yeast media. Heike Fussi and Heide Knauer have taught me the yeast apoptotic techniques.
3. The work presented in chapter 5 was as a part of collaboration between Prof. Dr.
Sandro Ghisla and Dr. Elisa Ferrando May. * PRK and SRA have contributed equally to this work. All the experiments with mammalian cells was done by myself. Sigrid Draxl, Dr. Michael Murkovic and Prof. Peter Macheroux of Technical University Graz, Austria are responsible for the amino acid analysis of LAAO media. PRK has provided the antibodies of LAAO, he has carried out H2O2 measurements with LAAO and DAAO. He has provided the western analysis of cells incubated with LAAO, and has estimated the sialic acid content of native LAAO and of desialylated LAAO. PRK has assessed the activity of pH and of freeze inactivated LAAO.
9. List of publications
Sudharsana Rao Ande*, Phaneeswara Rao Kommoju*, Sigrid Draxl, Michael Murkovic, Peter Macheroux, Sandro Ghisla and Elisa Ferrando-May (2006).
Mechanisms of cell death induction by L-amino acid oxidase, a major component of ophidian venom. (Manuscript accepted for publication in Apoptosis)
Sudharsana Rao Ande, Heike Fussi, Heide Knauer, Michael Murkovic, Sandro GhislaKai-Uwe Fröhlich and Peter Macheroux (2006). Induction of apoptosis in yeast by ophidian L-amino acid oxidase (Manuscript to be submitted)
Phaneeswara Rao Kommoju, Sudharsana Rao Ande, Peter Macheroux, Elisa Ferrando-May and Sandro Ghisla, (2005): Mechanisms of cell death induction by L-amino acid oxidase a flavoenzyme from snake venom, in Flavins and Flavoproteins 2005, Proceedings of the Fifteenth International Symposium, Shonan Village Center, Japan. pp. 761-766.
Sudharsana Rao Ande, Sandro Ghisla, Kai-Uwe Fröhlich and Peter Macheroux (2006). Antibacterial activity of L-amino acid oxidase (Manuscript in preparation)
10. References
Ali, S.A., S. Stoeva, A. Abbasi, J.M. Alam, R. Kayed, M. Faigle, B. Neumeister, and W. Voelter. 2000. Isolation, structural, and functional characterization of an apoptosis-inducing L-amino acid oxidase from leaf-nosed viper (Eristocophis macmahoni) snake venom. Arch Biochem Biophys. 384:216-26.
Aminoff, D. 1961. Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids. Biochem J. 81:384-92.
Amstad, P.A., H. Liu, M. Ichimiya, I.K. Berezesky, B.F. Trump, I.A. Buhimschi, and P.L. Gutierrez. 2001. BCL-2 is involved in preventing oxidant-induced cell death and in decreasing oxygen radical production. Redox Rep. 6:351-62.
Ande, S., P. Kommoju, S. Draxl, M. Murkovic, P. Macheroux, S. Ghisla , and E.
Ferrando-May. 2006. Mechanisms of cell death induction by L-amino acid oxidase, a major component of ophidian venom.
Ankarcrona, M., J.M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S.A.
Lipton, and P. Nicotera. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:961-73.
Annis, M.G., J.A. Yethon, B. Leber, and D.W. Andrews. 2004. There is more to life and death than mitochondria: Bcl-2 proteins at the endoplasmic reticulum. Biochim Biophys Acta. 1644:115-23.
Araki, S., T. Ishida, T. Yamamoto, K. Kaji, and H. Hayashi. 1993. Induction of apoptosis by hemorrhagic snake venom in vascular endothelial cells. Biochem Biophys Res Commun. 190:148-53.
Blixt, O., B.E. Collins, I.M. van den Nieuwenhof, P.R. Crocker, and J.C. Paulson.
2003. Sialoside specificity of the siglec family assessed using novel multivalent probes: identification of potent inhibitors of myelin-associated glycoprotein. J Biol Chem. 278:31007-19.
Bonfoco, E., D. Krainc, M. Ankarcrona, P. Nicotera, and S.A. Lipton. 1995.
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. 92:7162-6.
Borner, C. 2003. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol. 39:615-47.
Bross, P., S. Engst, A.W. Strauss, D.P. Kelly, I. Rasched, and S. Ghisla. 1990.
Characterization of wild-type and an active site mutant of human medium chain acyl-CoA dehydrogenase after expression in Escherichia coli. J Biol Chem. 265:7116-9.
Butzke, D., N. Machuy, B. Thiede, R. Hurwitz, S. Goedert, and T. Rudel. 2004.
Hydrogen peroxide produced by Aplysia ink toxin kills tumor cells independent of apoptosis via peroxiredoxin I sensitive pathways. Cell Death Differ. 11:608-17.
Chavan, S.S., W. Tian, K. Hsueh, D. Jawaheer, P.K. Gregersen, and C.C. Chu. 2002.
Characterization of the human homolog of the IL-4 induced gene-1 (Fig1). Biochim Biophys Acta. 1576:70-80.
Choi, W.S., E.H. Lee, C.W. Chung, Y.K. Jung, B.K. Jin, S.U. Kim, T.H. Oh, T.C.
Saido, and Y.J. Oh. 2001. Cleavage of Bax is mediated by caspasedependent or -independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2. J Neurochem. 77:1531-41.
Cikala, M., B. Wilm, E. Hobmayer, A. Bottger, and C.N. David. 1999. Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol. 9:959-62.
Coles, C.J., D.E. Edmondson, and T.P. Singer. 1977. Reversible inactivation of L-amino acid oxidase. Properties of the three conformational forms. J Biol Chem.
252:8035-9.
Crocker, P.R., and A. Varki. 2001. Siglecs, sialic acids and innate immunity. Trends Immunol. 22:337-42.
Crocker, P.R., and J. Zhang. 2002. New I-type lectins of the CD 33-related siglec subgroup identified through genomics. Biochem Soc Symp:83-94.
Curti, B., V. Massey, and M. Zmudka. 1968. Inactivation of snake venom L-amino acid oxidase by freezing. J Biol Chem. 243:2306-14.
Curti, B., S. Ronchi, U. Branzoli, G. Ferri, and C.H. Williams, Jr. 1973. Improved purification, amino acid analysis and molecular weight of homogenous D-amino acid oxidase from pig kidney. Biochim Biophys Acta. 327:266-73.
Davies, K.J. 1999. The broad spectrum of responses to oxidants in proliferating cells:
a new paradigm for oxidative stress. IUBMB Life. 48:41-7.
Dorland, R.B., J.L. Middlebrook, and S.H. Leppla. 1979. Receptor-mediated internalization and degradation of diphtheria toxin by monkey kidney cells. J Biol Chem. 254:11337-42.
Du, X.Y., and K.J. Clemetson. 2002. Snake venom L-amino acid oxidases. Toxicon.
40:659-65.
Dypbukt, J.M., M. Ankarcrona, M. Burkitt, A. Sjoholm, K. Strom, S. Orrenius, and P.
Nicotera. 1994. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J Biol Chem. 269:30553-60.
Earnshaw, W.C., L.M. Martins, and S.H. Kaufmann. 1999. Mammalian caspases:
structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem.
68:383-424.
Eguchi, Y., S. Shimizu, and Y. Tsujimoto. 1997. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57:1835-40.
Ehara, T., S. Kitajima, N. Kanzawa, T. Tamiya, and T. Tsuchiya. 2002. Antimicrobial action of achacin is mediated by L-amino acid oxidase activity. FEBS Lett. 531:509-12.
Eisler, H., K.U. Frohlich, and E. Heidenreich. 2004. Starvation for an essential amino acid induces apoptosis and oxidative stress in yeast. Exp Cell Res. 300:345-53.
Ellerby, L.M., H.M. Ellerby, S.M. Park, A.L. Holleran, A.N. Murphy, G. Fiskum, D.J.
Kane, M.P. Testa, C. Kayalar, and D.E. Bredesen. 1996. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J Neurochem. 67:1259-67.
Fadeel, B., B. Gleiss, K. Hogstrand, J. Chandra, T. Wiedmer, P.J. Sims, J.I. Henter, S.
Orrenius, and A. Samali. 1999. Phosphatidylserine exposure during apoptosis is a cell-type-specific event and does not correlate with plasma membrane phospholipid scramblase expression. Biochem Biophys Res Commun. 266:504-11.
Ferrer, E. 2001. Snake venom: The pain and potential of the poison. The cold blooded news. 28.
Ge, X., Y.M. Fu, Y.Q. Li, and G.G. Meadows. 2002. Activation of caspases and cleavage of Bid are required for tyrosine and phenylalanine deficiency-induced apoptosis of human A375 melanoma cells. Arch Biochem Biophys. 403:50-8.
Geueke, B., and W. Hummel. 2003. Heterologous expression of Rhodococcus opacus L-amino acid oxidase in Streptomyces lividans. Protein Expr Purif. 28:303-9.
Geyer, A., T.B. Fitzpatrick, P.D. Pawelek, K. Kitzing, A. Vrielink, S. Ghisla, and P.
Macheroux. 2001. Structure and characterization of the glycan moiety of L-amino-acid oxidase from the Malayan pit viper Calloselasma rhodostoma. Eur J Biochem.
268:4044-53.
Hockenbery, D.M., Z.N. Oltvai, X.M. Yin, C.L. Milliman, and S.J. Korsmeyer. 1993.
Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:241-51.
Iijima, R., J. Kisugi, and M. Yamazaki. 2003. L-amino acid oxidase activity of an antineoplastic factor of a marine mollusk and its relationship to cytotoxicity. Dev Comp Immunol. 27:505-12.
Jurgensmeier, J.M., Z. Xie, Q. Deveraux, L. Ellerby, D. Bredesen, and J.C. Reed.
1998. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci U S A. 95:4997-5002.
Kane, D.J., T. Ord, R. Anton, and D.E. Bredesen. 1995. Expression of bcl-2 inhibits necrotic neural cell death. J Neurosci Res. 40:269-75.
Kanzawa, N., S. Shintani, K. Ohta, S. Kitajima, T. Ehara, H. Kobayashi, H. Kizaki, and T. Tsuchiya. 2004. Achacin induces cell death in HeLa cells through two different mechanisms. Arch Biochem Biophys. 422:103-9.
Keen, J.H., F.R. Maxfield, M.C. Hardegree, and W.H. Habig. 1982. Receptor-mediated endocytosis of diphtheria toxin by cells in culture. Proc Natl Acad Sci U S A. 79:2912-6.
Kelm, S., and R. Schauer. 1997. Sialic acids in molecular and cellular interactions. Int Rev Cytol. 175:137-240.
Kerr, J.F., A.H. Wyllie, and A.R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 26:239-57.
Klassen, R., and F. Meinhardt. 2005. Induction of DNA damage and apoptosis in Saccharomyces cerevisiae by a yeast killer toxin. Cell Microbiol. 7:393-401.
Kommoju, P. 2005. Mechanisms of cell death induction by L-amino acid oxidase, a main component of ophidian venom. In 15th International Symposium on Flavins and Flavoproteins.
Laun, P., A. Pichova, F. Madeo, J. Fuchs, A. Ellinger, S. Kohlwein, I. Dawes, K.U.
Frohlich, and M. Breitenbach. 2001. Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol. 39:1166-73.
Leicht, M., G. Marx, D. Karbach, M. Gekle, T. Kohler, and H.G. Zimmer. 2003.
Mechanism of cell death of rat cardiac fibroblasts induced by serum depletion. Mol Cell Biochem. 251:119-26.
Leist, M., B. Single, A.F. Castoldi, S. Kuhnle, and P. Nicotera. 1997. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 185:1481-6.
Li, Z.Y., T.F. Yu, and E.C. Lian. 1994. Purification and characterization of L-amino acid oxidase from king cobra (Ophiophagus hannah) venom and its effects on human platelet aggregation. Toxicon. 32:1349-58.
Liu, Q.A., and M.O. Hengartner. 1999. The molecular mechanism of programmed cell death in C. elegans. Ann N Y Acad Sci. 887:92-104.
Lu, Q.M., Q. Wei, Y. Jin, J.F. Wei, W.Y. Wang, and Y.L. Xiong. 2002. L-amino acid oxidase from Trimeresurus jerdonii snake venom: purification, characterization, platelet aggregation-inducing and antibacterial effects. J Nat Toxins. 11:345-52.
Ludovico, P., M.J. Sousa, M.T. Silva, C. Leao, and M. Corte-Real. 2001.
Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology. 147:2409-15.
Macheroux, P., O. Seth, C. Bollschweiler, M. Schwarz, M. Kurfurst, L.C. Au, and S.
Ghisla. 2001. L-amino-acid oxidase from the Malayan pit viper Calloselasma rhodostoma. Comparative sequence analysis and characterization of active and inactive forms of the enzyme. Eur J Biochem. 268:1679-86.
Madeo, F., E. Frohlich, and K.U. Frohlich. 1997. A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol. 139:729-34.
Madeo, F., E. Frohlich, M. Ligr, M. Grey, S.J. Sigrist, D.H. Wolf, and K.U. Frohlich.
1999. Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol. 145:757-67.
Mason, J.M., M.D. Naidu, M. Barcia, D. Porti, S.S. Chavan, and C.C. Chu. 2004. IL-4-induced gene-1 is a leukocyte L-amino acid oxidase with an unusual acidic pH preference and lysosomal localization. J Immunol. 173:4561-7.
Meier, P., A. Finch, and G. Evan. 2000. Apoptosis in development. Nature. 407:796-801.
Middlebrook, J.L., R.B. Dorland, and S.H. Leppla. 1979. Effects of lectins on the interaction of diphtheria toxin with mammalian cells. Exp Cell Res. 121:95-101.
Mirkovic, N., D.W. Voehringer, M.D. Story, D.J. McConkey, T.J. McDonnell, and R.E. Meyn. 1997. Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene. 15:1461-70.
Mitsuru, J., N. Fumie, S. Ryuichi, M. Koji, and K. Hisao. 2003. Characterization of L-amino acid oxidase and antimicrobial activity of aplysianin A, a sea hare-derived protein, AIP, from parasite-infected fish induces apoptosis in mammalian cells by two different molecular mechanisms. Cell Death Differ. 8:298-307.
Naclerio, G., L. Baccigalupi, C. Caruso, M. De Felice, and E. Ricca. 1995. Bacillus subtilis Vegetative Catalase Is an Extracellular Enzyme. Appl Environ Microbiol.
61:4471-4473.
Nathan, I., A. Dvilansky, T. Yirmiyahu, M. Aharon, and A. Livne. 1982. Impairment of platelet aggregation by Echis colorata venom mediated by L-amino acid oxidase or H2O2. Thromb Haemost. 48:277-82.
Nicotera, P., M. Leist, and E. Ferrando-May. 1998. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett. 102-103:139-42.
Niedermann, D.M., and K. Lerch. 1991. Regulation of biosynthesis of L-amino acid oxidase by Neurospora crassa. FEMS Microbiol Lett. 63:309-13.
Nishizawa, T., C.C. Aldrich, and D.H. Sherman. 2005. Molecular analysis of the rebeccamycin L-amino acid oxidase from Lechevalieria aerocolonigenes ATCC 39243. J Bacteriol. 187:2084-92.
Nisizawa, K., and W. Pigman. 1959. The composition and properties of the mucin clot from cattle submaxillary glands. Arch Oral Biol. 1:161-70.
Ogawa, M., S. Nakamura, T. Atsuchi, T. Tamiya, T. Tsuchiya, and S. Nakai. 1999.
Macromolecular antimicrobial glycoprotein, achacin, expressed in a methylotrophic yeast Pichia pastoris. FEBS Lett. 448:41-4.
Orlov, S.N., D. Pchejetski, S. Taurin, N. Thorin-Trescases, G.V. Maximov, A.V.
Pshezhetsky, A.B. Rubin, and P. Hamet. 2004. Apoptosis in serum-deprived vascular smooth muscle cells: evidence for cell volume-independent mechanism. Apoptosis.
9:55-66.
Otsuka-Fuchino, H., Y. Watanabe, C. Hirakawa, J. Takeda, T. Tamiya, J.J.
Matsumoto, and T. Tsuchiya. 1993. Morphological aspects of Achacin-treated bacteria. Comp Biochem Physiol C. 104:37-42.
Pawelek, P.D., J. Cheah, R. Coulombe, P. Macheroux, S. Ghisla, and A. Vrielink.
2000. The structure of L-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. Embo J. 19:4204-15.
Pollegioni, L., G. Molla, S. Campaner, E. Martegani, and M.S. Pilone. 1997. Cloning, sequencing and expression in E. coli of a D-amino acid oxidase cDNA from Rhodotorula gracilis active on cephalosporin C. J Biotechnol. 58:115-23.
Ponnudurai, G., M.C. Chung, and N.H. Tan. 1994. Purification and properties of the L-amino acid oxidase from Malayan pit viper (Calloselasma rhodostoma) venom.
Arch Biochem Biophys. 313:373-8.
Reed, J.C. 1997. Cytochrome c: can't live with it--can't live without it. Cell. 91:559-62.
Reed, J.C. 2000. Mechanisms of apoptosis. Am J Pathol. 157:1415-30.
Richardson, H., and S. Kumar. 2002. Death to flies: Drosophila as a model system to study programmed cell death. J Immunol Methods. 265:21-38.
Sakurai, Y., H. Takatsuka, A. Yoshioka, T. Matsui, M. Suzuki, K. Titani, and Y.
Fujimura. 2001. Inhibition of human platelet aggregation by L-amino acid oxidase purified from Naja naja kaouthia venom. Toxicon. 39:1827-33.
Schendel, S.L., Z. Xie, M.O. Montal, S. Matsuyama, M. Montal, and J.C. Reed. 1997.
Channel formation by antiapoptotic protein Bcl-2. Proc Natl Acad Sci U S A.
94:5113-8.
Schinzel, A., T. Kaufmann, and C. Borner. 2004. Bcl-2 family members: integrators of survival and death signals in physiology and pathology [corrected]. Biochim Biophys Acta. 1644:95-105.
Single, B., M. Leist, and P. Nicotera. 2001. Differential effects of bcl-2 on cell death triggered under ATP-depleting conditions. Exp Cell Res. 262:8-16.
Skarnes, R.C. 1970. L-amino-acid oxidase, a bactericidal system. Nature. 225:1072-3.
Solomon, M., B. Belenghi, M. Delledonne, E. Menachem, and A. Levine. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell. 11:431-44.
Souza, D.H., L.M. Eugenio, J.E. Fletcher, M.S. Jiang, R.C. Garratt, G. Oliva, and H.S. Selistre-de-Araujo. 1999. Isolation and structural characterization of a cytotoxic L-amino acid oxidase from Agkistrodon contortrix laticinctus snake venom:
preliminary crystallographic data. Arch Biochem Biophys. 368:285-90.
Stabeli, R.G., S. Marcussi, G.B. Carlos, R.C. Pietro, H.S. Selistre-de-Araujo, J.R.
Giglio, E.B. Oliveira, and A.M. Soares. 2004. Platelet aggregation and antibacterial effects of an l-amino acid oxidase purified from Bothrops alternatus snake venom.
Bioorg Med Chem. 12:2881-6.
Stiles, B.G., F.W. Sexton, and S.A. Weinstein. 1991. Antibacterial effects of different snake venoms: purification and characterization of antibacterial proteins from Pseudechis australis (Australian king brown or mulga snake) venom. Toxicon.
29:1129-41.
Suhr, S.M., and D.S. Kim. 1996. Identification of the snake venom substance that induces apoptosis. Biochem Biophys Res Commun. 224:134-9.
Suhr, S.M., and D.S. Kim. 1999. Comparison of the apoptotic pathways induced by L-amino acid oxidase and hydrogen peroxide. J Biochem (Tokyo). 125:305-9.
Sun, L.K., Y. Yoshii, A. Hyodo, H. Tsurushima, A. Saito, T. Harakuni, Y.P. Li, K.
Kariya, M. Nozaki, and N. Morine. 2003. Apoptotic effect in the glioma cells induced by specific protein extracted from Okinawa Habu (Trimeresurus flavoviridis) venom in relation to oxidative stress. Toxicol In Vitro. 17:169-77.
Susin, S.A., N. Zamzami, M. Castedo, T. Hirsch, P. Marchetti, A. Macho, E. Daugas, M. Geuskens, and G. Kroemer. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med. 184:1331-41.
Takatsuka, H., Y. Sakurai, A. Yoshioka, T. Kokubo, Y. Usami, M. Suzuki, T. Matsui, K. Titani, H. Yagi, M. Matsumoto, and Y. Fujimura. 2001. Molecular characterization of L-amino acid oxidase from Agkistrodon halys blomhoffii with special reference to platelet aggregation. Biochim Biophys Acta. 1544:267-77.
Tempone, A.G., H.F. Andrade, Jr., P.J. Spencer, C.O. Lourenco, J.R. Rogero, and N.
Nascimento. 2001. Bothrops moojeni venom kills Leishmania spp. with hydrogen peroxide generated by its L-amino acid oxidase. Biochem Biophys Res Commun.
280:620-4.
Thornberry, N.A., and Y. Lazebnik. 1998. Caspases: enemies within. Science.
281:1312-6.
Torii, S., M. Naito, and T. Tsuruo. 1997. Apoxin I, a novel apoptosis-inducing factor with L-amino acid oxidase activity purified from Western diamondback rattlesnake venom. J Biol Chem. 272:9539-42.
Torii, S., K. Yamane, T. Mashima, N. Haga, K. Yamamoto, J.W. Fox, M. Naito, and T. Tsuruo. 2000. Molecular cloning and functional analysis of apoxin I, a snake venom-derived apoptosis-inducing factor with L-amino acid oxidase activity.
Biochemistry. 39:3197-205.
Toyama, M.H., O. Toyama Dde, L.F. Passero, M.D. Laurenti, C.E. Corbett, T.Y.
Tomokane, F.V. Fonseca, E. Antunes, P.P. Joazeiro, L.O. Beriam, M.A. Martins, H.S.
Monteiro, and M.C. Fonteles. 2006. Isolation of a new L-amino acid oxidase from Crotalus durissus cascavella venom. Toxicon. 47:47-57.
Tsujimoto, Y., S. Shimizu, Y. Eguchi, W. Kamiike, and H. Matsuda. 1997. Bcl-2 and Bcl-xL block apoptosis as well as necrosis: possible involvement of common mediators in apoptotic and necrotic signal transduction pathways. Leukemia. 11 Suppl 3:380-2.
Vallon, O., L. Bulte, R. Kuras, J. Olive, and F.A. Wollman. 1993. Extensive accumulation of an extracellular L-amino-acid oxidase during gametogenesis of Chlamydomonas reinhardtii. Eur J Biochem. 215:351-60.
Varki, A. 1992. Selectins and other mammalian sialic acid-binding lectins. Curr Opin Cell Biol. 4:257-66.
Varki, A. 1997. Sialic acids as ligands in recognition phenomena. Faseb J. 11:248-55.
Vaux, D.L. 1993. Toward an understanding of the molecular mechanisms of physiological cell death. Proc Natl Acad Sci U S A. 90:786-9.
Vaux, D.L., S. Cory, and J.M. Adams. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature. 335:440-2.
Voehringer, D.W., and R.E. Meyn. 2000. Redox aspects of Bcl-2 function. Antioxid Redox Signal. 2:537-50.
von Gunten, S., S. Yousefi, M. Seitz, S.M. Jakob, T. Schaffner, R. Seger, J. Takala, P.M. Villiger, and H.U. Simon. 2005. Siglec-9 transduces apoptotic and nonapoptotic death signals into neutrophils depending on the proinflammatory cytokine environment. Blood. 106:1423-31.
Wei, J.F., Q. Wei, Q.M. Lu, H. Tai, Y. Jin, W.Y. Wang, and Y.L. Xiong. 2003.
Purification, characterization and biological activity of an L-amino acid oxidase from Trimeresurus mucrosquamatus venom. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai). 35:219-24.
Yang, H., P.M. Johnson, K.C. Ko, M. Kamio, M.W. Germann, C.D. Derby, and P.C.
Tai. 2005. Cloning, characterization and expression of escapin, a broadly antimicrobial FAD-containing L-amino acid oxidase from ink of the sea hare Aplysia californica. J Exp Biol. 208:3609-22.
Zamaraeva, M.V., R.Z. Sabirov, E. Maeno, Y. Ando-Akatsuka, S.V. Bessonova, and Y. Okada. 2005. Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ. 12:1390-7.
Zeller, A.E. 1977. Snake venom action: are enzymes involved in it? Experientia.
33:143-50.
Zhang, H., M. Teng, L. Niu, Y. Wang, Y. Wang, Q. Liu, Q. Huang, Q. Hao, Y. Dong, and P. Liu. 2004a. 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. 60:974-7.
Zhang, H., Q. Yang, M. Sun, M. Teng, and L. Niu. 2004b. Hydrogen peroxide produced by two amino acid oxidases mediates antibacterial actions. J Microbiol.
42:336-9.
Zhang, Y.J., J.H. Wang, W.H. Lee, Q. Wang, H. Liu, Y.T. Zheng, and Y. Zhang.
2003. Molecular characterization of Trimeresurus stejnegeri venom L-amino acid oxidase with potential anti-HIV activity. Biochem Biophys Res Commun. 309:598-604.