Fungal ribotoxins: molecular dissection of a family of natural killers

Alegre-Cebollada J Álvarez-García E Monedero V Pérez-Martínez G Martínez del Pozo A Gavilanes JG (2005) Heterologous production of natural and non-cytotoxic variants of fungal ribotoxins in Lactococcus lactis . 8th Symposium on Lactic Acid Bacteria. Genetics, Metabolism, and Applications. Egmond aan Zee (The Netherlands). Abstract number H021.

Alonso MA Carrasco L (1981) Permeabilization of mammalian cells to proteins by the ionophore nigericin. FEBS Lett 127: 112–114.

Alonso MA Carrasco L (1982) Molecular basis of the permeabilization of mammalian cells by ionophores. Eur J Biochem 127: 567–569.

10.1515/BC.2006.069

10.1042/bj1060601

10.1042/bj1060609

10.1084/jem.172.5.1529

Arruda LK Mann BJ Chapman MD (1992) Selective expression of a major allergen and cytotoxin, Aspf1, in Aspergillus fumigatus. Implications for the immunopathogenesis of Aspergillus-related diseases. J Immunol 149: 3354–3359.

10.1126/science.289.5481.905

Banerjee B Kurup VP (2003) Molecular biology of Aspergillus allergens. Front Biosci 8: S128–S139.

Benhar I Pastan I (1995a) Characterization of B1(Fv)PE38 and B1(dsFv)PE38: single-chain and disulfide-stabilized Fv immunotoxins with increased activity that cause complete remissions of established human carcinoma xenografts in nude mice. Clin Cancer Res 1: 1023–1029.

10.1074/jbc.270.40.23373

10.1021/bc980028o

Better M Bernhard SL Lei SP Fishwild DM Carroll SF (1992) Activity of recombinant mitogillin and mitogillin immunoconjugates. J Biol Chem 267: 16712–16718.

10.1007/BF01964057

10.1006/jipa.1998.4762

10.1099/00221287-138-7-1429

Brandhorst T Yang R Kenealy WR (1994) Heterologous expression of the cytotoxin restrictocin in Aspergillus nidulans and Aspergillus niger . Protein Expr Purif 5: 486–497.

Brinkmann U (2000) Recombinant antibody fragments and immunotoxin fusions for cancer therapy. In Vivo 14: 21–27.

Brinkmann U Pastan I (1994) Immunotoxins against cancer. Biochim Biophys Acta 1198: 27–45.

10.1073/pnas.88.19.8616

10.1073/pnas.90.16.7538

10.1016/S0022-2836(02)00235-8

Campos-Olivas R Bruix M Santoro J Martínez del Pozo A Lacadena J Gavilanes JG Rico M (1996a) 1H and 15N nuclear magnetic resonance assignment and secondary structure of the cytotoxic ribonuclease α-sarcin. Protein Sci 5: 969–972.

10.1016/S0014-5793(96)01320-8

10.1016/0042-6822(82)90507-4

Carroll SF Collier RJ (1987) Active site of Pseudomonas aeruginosa exotoxin A. Glutamic acid 553 is photolabeled by NAD and shows functional homology with glutamic acid 148 of diphtheria toxin. J Biol Chem 262: 8707–8711.

10.1046/j.1365-2958.2003.03512.x

10.1016/S0022-2836(03)00922-7

Conde FP Orlandi R Canevari S Mezzanzanica D Ripamonti M Muñoz SM Jorge P Colnaghi MI (1989) The Aspergillus toxin restrictocin is a suitable cytotoxic agent for generation of immunoconjugates with monoclonal antibodies directed against human carcinoma cells. Eur J Biochem 178: 795–802.

10.1111/j.1365-2958.2006.05270.x

10.1073/pnas.86.9.3184

10.1261/rna.2147803

10.1073/pnas.95.23.13436

10.1006/jmbi.1999.3072

10.1093/nar/gkg908

10.1107/S0909049503023896

10.1093/intimm/10.8.1211

Cregg JM Madden KR Barringer KJ Thill GP Stillman C A (1989) Functional characterization of the two alcohol oxidase genes from the yeast Pichia pastoris . Mol Cell Biol 9: 1316–1323.

10.1038/nbt0893-905

10.1002/1097-0134(20001115)41:3<350::AID-PROT70>3.0.CO;2-V

10.1183/09031936.06.00074705

Doumen J Gonciarz M Zegers I Loris R Wyns L Steyaert J (1996) A catalytic function for the structurally conserved residue Phe 100 of ribonuclease T1. Protein Sci 5: 1523–1530.

Ehrlich P (1956) The relationship between chemical constitution, distribution, and pharmacological action. The Collected Papers of Paul Ehrlich, Vol. 1 ( Himmelweit F Marquardt M & Dale H , eds), pp. 596. Pergamon Press, New York.

Endo Y Tsurugi K (1987) RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 262: 8128–8130.

Endo Y Wool IG (1982) The site of action of α-sarcin on eukaryotic ribosomes. The sequence at the α-sarcin cleavage site in 28 S ribosomal ribonucleic acid. J Biol Chem 257: 9054–9060.

Endo Y Huber PW Wool IG (1983) The ribonuclease activity of the cytotoxin α-sarcin. The characteristics of the enzymatic activity of α-sarcin with ribosomes and ribonucleic acids as substrates. J Biol Chem 258: 2662–2667.

Endo Y Mitsui K Motizuki M Tsurugi K (1987) The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28 S ribosomal RNA caused by the toxins. J Biol Chem 262: 5908–5912.

Endo Y Chan YL Lin A Tsurugi K Wool IG (1988) The cytotoxins α-sarcin and ricin retain their specificity when tested on a synthetic oligoribonucleotide (35-mer) that mimics a region of 28 S ribosomal ribonucleic acid. J Biol Chem 263: 7917–7920.

Endo Y Oka T Tsurugi K Natori Y (1993a) The biosynthesis of a cytotoxic protein, α-sarcin, in a mold of Aspergillus giganteus. I. Synthesis of prepro- and pro-α-sarcin in vitro . Tokushima J Exp Med 40: 1–6.

Endo Y Oka T Yokota S Tsurugi K Natori Y (1993b) The biosynthesis of a cytotoxic protein, α-sarcin, in a mold of Aspergillus giganteus. II. Maturation of precursor form of α-sarcin in vivo . Tokushima J Exp Med 40: 7–12.

Engert A Diehl V Schnell R et al. (1997) A phase-I study of an anti-CD25 ricin A-chain immunotoxin (RFT5-SMPT-dgA) in patients with refractory Hodgkin's lymphoma. Blood 89: 403–410.

10.1016/0092-8674(80)90323-2

10.1021/bi00325a008

Foss FM Saleh MN Krueger JG Nichols JC Murphy JR (1998) Diphtheria toxin fusion proteins. Curr Top Microbiol Immunol 234: 63–81.

10.1016/S0092-8674(00)80690-X

10.1038/nature04341

García-Mayoral MF Pérez-Cañadillas JM Santoro J Ibarra-Molero B Sánchez-Ruiz JM Lacadena J Martínez del Pozo A Gavilanes JG Rico M Bruix M (2003) Dissecting structural and electrostatic interactions of charged groups in α-sarcin. An NMR study of some mutants involving the catalytic residues. Biochemistry 42: 13122–13133.

10.1110/ps.03532204

10.1007/s00249-005-0473-0

10.1016/j.febslet.2005.11.027

García-Mayoral MF Martínez del Pozo A Campos-Olivas R Gavilanes JG Santoro J Rico M Laurents DV Bruix M (2006) pH-dependent conformational stability of the ribotoxin α-sarcin and four active site charge substitution variants. Biochemistry 45: 13705–13718.

10.1110/ps.9601

10.1074/jbc.M200922200

10.1111/j.1742-4658.2005.04674.x

10.1042/bj2580569

10.1042/bj2650815

Gasset M Oñaderra M Martínez del Pozo A Schiavo GP Laynez J Usobiaga P Gavilanes JG (1991a) Effect of the antitumour protein α-sarcin on the thermotropic behaviour of acid phospholipid vesicles. Biochim Biophys Acta 1068: 9–16.

10.1016/0167-4838(91)90111-C

Gasset M Mancheño JM Lacadena J Turnay J Olmo N Lizarbe MA Martínez del Pozo A Oñaderra M Gavilanes JG (1994) α-Sarcin, a ribosome-inactivating protein that translocates across the membrane of phospholipid vesicles. Curr Topics Pept Protein Res 1: 99–104.

Gasset M Mancheño JM Lacadena J Martínez del Pozo A Oñaderra M Gavilanes JG (1995) Spectroscopic characterization of the alkylated α-sarcin cytotoxin: analysis of the structural requirements for the protein–lipid bilayer hydrophobic interaction. Biochim Biophys Acta 1252: 43–52.

10.1016/0022-1759(93)90335-5

10.1006/jmbi.1996.0130

Gohda K Oka K Tomita K Hakoshima T (1994) Crystal structure of RNase T1 complexed with the product nucleotide 3′-GMP. Structural evidence for direct interaction of histidine 40 and glutamic acid 58 with the 2′-hydroxyl group of the ribose. J Biol Chem 269: 17531–17536.

10.1042/bj3450247

10.1067/mai.2002.130179

10.1016/S1046-5928(03)00012-3

10.1186/1475-2859-4-33

10.1021/bi9815243

10.1016/S0091-6749(99)70330-1

Herrero-Galán E Lacadena J Martínez del Pozo A Olmo N Boucias DG Oñaderra M Gavilanes JG (2007) Hirsutellin A: an advanced ribonuclease. Structural and functional studies. Unpublished results.

Hertler AA Frankel AE (1989) Immunotoxins: a clinical review of their use in the treatment of malignancies. J Clin Oncol 7: 1932–1942.

10.1016/S0041-0101(96)00170-5

10.1016/0263-7855(96)00018-5

10.1016/j.jmb.2005.12.033

10.1139/o95-124

10.1074/jbc.274.18.12576

10.1016/S0014-5793(99)01753-6

10.1046/j.1365-2958.1998.00987.x

10.1016/S0076-6879(01)41161-X

Kondo T FitzGerald D Chaudhary VK Adhya S Pastan I (1988) Activity of immunotoxins constructed with modified Pseudomonas exotoxin. A lacking the cell recognition domain. J Biol Chem 263: 9470–9475.

10.1016/0263-7855(96)00009-4

Korennykh AV Piccirilli JA Correll CC (2006) The electrostatic character of the ribosomal surface enables extraordinarily rapid target location by ribotoxins. Nature Str Mol Biol 13: 436–443.

10.1517/14656566.1.6.1117

10.2174/1389201013378635

Kreitman RJ (2003) Recombinant toxins for the treatment of cancer. Curr Opin Mol Ther 5: 44–51.

10.1073/pnas.87.21.8291

10.1021/bc00020a002

Kreitman RJ Wilson WH Robbins D Margulies I Stetler-Stevenson M Waldmann TA Pastan I (1999) Responses in refractory hairy cell leukemia to a recombinant immunotoxin. Blood 94: 3340–3348.

10.1073/pnas.93.3.974

10.1016/j.copbio.2005.08.006

Kurup VP Kumar A Kenealy WR Greenberger PA (1994) Aspergillus ribotoxins react with IgE and IgG antibodies of patients with allergic bronchopulmonary aspergillosis. J Lab Clin Med 123: 749–756.

10.1016/S0196-9781(98)00113-2

10.1186/1476-7961-4-11

10.1016/0378-1119(94)90370-0

10.1042/bj3090581

10.1016/S0014-5793(98)00137-9

10.1002/(SICI)1097-0134(19991115)37:3<474::AID-PROT14>3.0.CO;2-N

Lacadena J Carreras-Sangrá N Oñaderra M Martínez del Pozo A Gavilanes JG (2005) Production and purification of an immunotoxin based on the ribotoxin α-sarcin. In: 7th International Meeting on Ribonucleases. (Urbániková, ed), pp. 65, Abstract number P10. ASCO Art & Science, Bratislava, Stará Lesná (Slovak Republic).

10.1111/j.1365-2958.1991.tb01930.x

Lamy B Davies J Schindler D (1992) The Aspergillus ribonucleolytic toxins (ribotoxins). Genetically Engineered Toxins ( Frankel AE , ed), pp. 237–258. Marcel Dekker Inc., New York, NY.

LeMaistre CF Saleh MN Kuzel TM et al. (1998) Phase I trial of a ligand fusion-protein (DAB389IL-2) in lymphomas expressing the receptor for interleukin-2. Blood 91: 399–405.

10.1074/jbc.M302873200

Li Q Verschraegen CF Mendoza J Hassan R (2004) Cytotoxic activity of the recombinant anti-mesothelin immunotoxin, SS1(dsFv)PE38, towards tumor cell lines established from ascites of patients with peritoneal mesotheliomas. Anticancer Res 24: 1327–1335.

10.1016/0041-0101(94)00140-4

Liu R Liebman SW (1996) A translational fidelity mutation in the universally conserved sarcin/ricin domain of 25S yeast ribosomal RNA. RNA 2: 254–263.

10.1128/AEM.71.9.5332-5340.2005

López-Otín C Barber D Fernández-Luna JL Soriano F Méndez E (1984) The primary structure of the cytotoxin restrictocin. Eur J Biochem 143: 621–634.

10.1016/S0076-6879(01)41160-8

10.1016/j.jmb.2006.02.014

10.1038/nature04300

10.1128/CDLI.11.3.552-558.2004

10.1016/0167-4838(88)90036-2

Martínez del Pozo A Gasset M Oñaderra M Gavilanes JG (1989) Effect of divalent cations on structure – function relationships of the antitumour protein α-sarcin. Int J Pept Protein Res 34: 416–422.

Mancheño JM Gasset M Lacadena J Ramón F Martínez del Pozo A Oñaderra M Gavilanes JG (1994) Kinetic study of the aggregation and lipid mixing produced by α-sarcin on phosphatidylglycerol and phosphatidylserine vesicles: stopped-flow light scattering and fluorescence energy transfer measurements. Biophys J 67: 1117–1125.

10.1006/jtbi.1995.0022

10.1016/S0006-3495(95)80421-2

Mancheño JM Martínez del Pozo A Albar JP Oñaderra M Gavilanes JG (1998) A peptide of nine amino acid residues from α-sarcin cytotoxin is a membrane-perturbing structure. J Pept Res 51: 142–148.

10.1006/prep.1997.0846

10.1006/jipa.1999.4859

10.1016/S0041-0101(99)00103-8

10.1006/meth.2000.1145

Masip M Lacadena J Mancheño JM Oñaderra M Martínez-Ruiz A Martínez del Pozo A Gavilanes JG (2001) Arginine 121 is a crucial residue for the specific cytotoxic activity of the ribotoxin α-sarcin. Eur J Biochem 268: 6190–6196.

10.1110/ps.0225903

10.1016/S0022-2836(02)00568-5

Meyer V Stahl U (2002) New insights in the regulation of the afp gene encoding the antifungal protein of Aspergillus giganteus . Curr Genet 42: 36–42.

10.1007/s00438-001-0609-6

Meyer V Stahl U (2003) The influence of co-cultivation on expression of the antifungal protein in Aspergillus giganteus . J Basic Microbiol 43: 68–74.

10.1016/0014-5793(88)81162-1

10.1038/334362a0

Moser M Crameri R Menz G Schneider T Dudler T Virchow C Gmachl M Blaser K Suter M (1992) Cloning and expression of recombinant Aspergillus fumigatus allergen I/a (rAsp f I/a) with IgE binding and type I skin test activity. J Immunol 149: 454–460.

10.1073/pnas.94.23.12280

10.1128/JB.187.9.3151-3157.2005

Nayak SK Batra JK (1997) A single amino acid substitution in ribonucleolytic toxin restrictocin abolishes its specific substrate recognition activity. Biochemistry 36: 13693–13699.

Nayak SK Bagga S Gaur D Nair DT Salunke DM Batra JK (2001) Mechanism of specific target recognition and RNA hydrolysis by ribonucleolytic toxin restrictocin. Biochemistry 40: 9115–9124.

10.1146/annurev.arplant.52.1.785

10.1038/nature04332

10.1016/j.sbi.2005.05.004

10.1021/bi00047a025

Olmo N Turnay J Lizarbe MA Gavilanes JG (1993) Cytotoxic effect of α-sarcin, a ribosome inactivating protein, in cultured Rugli cells. STP Pharma Sciences 3: 93–96.

Olmo N Turnay J González de Buitrago G LópezdeSilanes I Gavilanes JG Lizarbe MA (2001) Cytotoxic mechanism of the ribotoxin α-sarcin. Induction of cell death via apoptosis. Eur J Biochem 268: 2113–2123.

Olsnes S Pihl A (1973a) Isolation and properties of abrin: a toxic protein inhibiting protein synthesis. Evidence for different biological functions of its two constituent-peptide chains. Eur J Biochem 35: 179–185.

10.1021/bi00740a028

Olson BH Goerner GL (1965) α-Sarcin, a new antitumour agent. I. Isolation, purification, chemical composition, and the identity of a new amino acid. Appl Microbiol 13: 314–321.

Olson BH Jennings JC Roga V Junek AJ Schuurmans DM (1965) α-Sarcin, a new antitumour agent. II. Fermentation and antitumour spectrum. Appl Microbiol 13: 322–326.

Oñaderra M Gasset M Martínez del Pozo A Gavilanes JG (1989) Molecular aspects of α-sarcin penetration in phospholipid bilayers. Biochem Soc Trans 17: 999–1000.

10.1042/bj2950221

Orlandi R Canevari S Conde FP Leoni F Mezzanzanica D Ripamonti M Colnaghi MI (1988) Immunoconjugate generation between the ribosome inactivating protein restrictocin and an anti-human breast carcinoma MAB. Cancer Immunol Immunother 26: 114–120.

Otero MJ Carrasco L (1986) External ATP permeabilizes transformed cells to macromolecules. Biochem Biophys Res Commun 134: 453–460.

10.1016/0014-4827(88)90033-X

O'Toole JE Esseltine D Lynch TJ Lambert JM Grossbard ML (1998) Clinical trials with blocked ricin immunotoxins. Curr Top Microbiol Immunol 234: 35–56.

10.1002/anie.199103433

10.1073/pnas.88.8.3358

10.1038/nm0396-350

Parente D Raucci G Celano B et al. (1996) Clavin, a type-1 ribosome-inactivating protein from Aspergillus clavatus IFO 8605. cDNA isolation, heterologous expression, biochemical and biological characterization of the recombinant protein. Eur J Biochem 239: 272–280.

10.1111/j.1574-6968.1993.tb06357.x

Pasqualotto A (2006) Post-operative aspergillosis. Clin Microbiol Infect 12: S25.

Pastan I (2003) Immunotoxins containing Pseudomonas exotoxin A: a short history. Cancer Immunol Immunother 52: 338–341.

10.1126/science.1683495

10.1146/annurev.bi.61.070192.001555

10.1021/bi981672t

10.1006/jmbi.2000.3813

10.1023/A:1021698308683

Pérez-Cañadillas JM García-Mayoral MF Laurents DV Martínez del Pozo A Gavilanes JG Rico M Bruix M (2003) Tautomeric state of α-sarcin histidines. Nδ tautomers are a common feature in the active site of extracellular microbial ribonucleases. FEBS Lett 534: 197–201.

10.1096/fj.00-0751rev

10.1006/jmbi.1996.0784

Piechura JE Huang CJ Cohen SH Kidd JM Kurup VP Calvanico NJ (1983) Antigens of Aspergillus fumigatus. II. Electrophoretic and clinical studies. Immunology 49: 657–665.

10.1016/S0959-440X(00)00184-6

10.1006/bbrc.1996.0697

10.1042/bj3240815

10.1016/S0014-5793(97)00333-5

Rathore D Nayak SK Batra JK (1997) Overproduction of fungal ribotoxin α-sarcin in Escherichia coli: generation of an active immunotoxin. Gene 190: 31–35.

10.1016/S0167-7799(98)01226-8

10.1016/0006-291X(82)91868-X

Roga V Hedeman LP Olson BH (1971) Evaluation of mitogillin (NSC-69529) in the treatment of naturally occurring canine neoplasms. Cancer Chemother Rep 55: 101–113.

10.1016/S1130-1406(05)70047-4

Rosok MJ Eghtedarzadeh-Kondri M Young K Bajorath J Glaser S Yelton D (1998) Analysis of BR96 binding sites for antigen and anti-idiotype by codon-based scanning mutagenesis. J Immunol 160: 2353–2359.

10.1021/bi00827a021

Sacco G Drickamer K Wool IG (1983) The primary structure of the cytotoxin α-sarcin. J Biol Chem 258: 5811–5818.

Sato K Egami F (1957) Studies on ribonucleases in takadiastase. J Biochem 44: 753–767.

10.1042/bj1450353

10.1093/nar/4.4.1097

Schnell R Vitetta E Schindler J Barth S Winkler U Borchmann P Hansmann ML Diehl V Ghetie V Engert A (1998) Clinical trials with an anti-CD25 ricin A-chain experimental and immunotoxin (RFT5-SMPT-dgA) in Hodgkin's lymphoma. Leuk Lymphoma 30: 525–537.

Scott AM Geleick D Rubira M et al. (2000) Construction, production, and characterization of humanized anti-Lewis Y monoclonal antibody 3S193 for targeted immunotherapy of solid tumors. Cancer Res 60: 3254–3261.

10.1107/S0108768190009569

10.1515/BC.2004.150

10.1111/j.1365-2958.1993.tb01236.x

Smith JM Tang CM Van Noorden S Holden DW (1994) Virulence of Aspergillus fumigatus double mutants lacking restrictocin and an alkaline protease in a low-dose model of invasive pulmonary aspergillosis. Infect Immun 62: 5247–5254.

10.1093/nar/gkj470

10.1126/science.289.5483.1352

Steyaert J (1997) A decade of protein engineering on ribonuclease T1. Atomic dissection of the enzyme–substrate interactions. Eur J Biochem 247: 1–11.

10.1021/bi00490a025

10.1093/nar/16.4.1349

10.1038/nbt0492-405

10.1128/JVI.02452-05

Sylvester ID Roberts LM Lord JM (1997) Characterization of prokaryotic recombinant Aspergillus ribotoxin α-sarcin. Biochim Biophys Acta 1358: 53–60.

10.1006/jmbi.1994.0124

10.1126/science.8327892

10.1007/BF00925735

Uchida T Arima T Egami F (1970) Specificity of RNase U2. J Biochem (Tokyo) 67: 91–102.

10.1074/jbc.M207424200

10.1016/S0022-2836(02)00304-2

10.1007/BF01962595

10.1038/341544a0

Wawrzynczak EJ Henry RV Cumber AJ Parnell GD Derbyshire EJ Ulbrich N (1991) Biochemical, cytotoxic and pharmacokinetic properties of an immunotoxin composed of a mouse monoclonal antibody Fib75 and the ribosome-inactivating protein α-sarcin from Aspergillus giganteus . Eur J Biochem 196: 203–209.

10.1006/abbi.1997.0175

10.1016/S1046-5928(02)00009-8

10.1128/AEM.70.6.3370-3376.2004

Woo JH Liu YY Neville DM Jr (2006) Minimization of aggregation of secreted bivalent anti-human T cell immunotoxin in Pichia pastoris bioreactor culture by optimizing culture conditions for protein secretion. J Biotechnol 121: 75–85.

Wool IG (1984) The mechanism of action of the cytotoxic nuclease α-sarcin and its use to analyse ribosome structure. Trends Biochem Sci 9: 14–17.

10.1016/0968-0004(96)20011-8

Wool IG (1997) Structure and mechanism of action of cytotoxic ribonuclease α-sarcin. Ribonucleases. Structures and Functions ( D'Alessio G & Riordan JF , eds), pp. 131–162. Academic Press, New York.

10.1016/0968-0004(92)90407-Z

10.1006/jmbi.2000.4265

10.1016/j.abb.2004.04.018

Yang R Kenealy WR (1992a) Effects of amino-terminal extensions and specific mutations on the activity of restrictocin. J Biol Chem 267: 16801–16805.

10.1099/00221287-138-7-1421

10.1016/S0969-2126(96)00090-1

10.1038/nsb1101-968

10.1021/bi00531a025

Yoshida H (2001) The ribonuclease T1 family. Methods Enzymol 341: 28–41.

10.1042/bj2940001