Alcohol oxidase: A complex peroxisomal, oligomeric flavoprotein

FEMS Yeast Research

Volumn 5, Issue 11, 2005, Pages 975-983

  Ozimek, Paulina ^a   Veenhuis, Marten ^a   Van Der Klei, Ida J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Alcohol oxidase; Dofactor binding; Peroxisome; Protein sorting

Indexed keywords

ALCOHOL OXIDASE; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; FORMALDEHYDE; HYDROGEN PEROXIDE; METHANOL;

ALCOHOL METABOLISM; ALCOHOL OXIDATION; CATALYSIS; CATALYST; CELL ORGANELLE; CELL SELECTION; COMPLEX FORMATION; COVALENT BOND; ENZYME ACTIVATION; ENZYME REPRESSION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PEROXISOME; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; SHORT SURVEY; TRANSCRIPTION INITIATION; YEAST;

ALCOHOL OXIDOREDUCTASES; FLAVIN-ADENINE DINUCLEOTIDE; FLAVOPROTEINS; PEROXISOMES; YEASTS;

EID: 27644453559     PISSN: 15671356     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.femsyr.2005.06.005     Document Type: Short Survey

References (90)

1. M. Kiess, H.J. Hecht, and H.M. Kalisz Glucose oxidase from Penicillium amagasakiense. Primary structure and comparison with other glucose-methanol- choline (GMC) oxidoreductases Eur. J. Biochem. 252 1998 90 99
2. N. Kato, Y. Omori, Y. Tani, and K. Ogata Alcohol oxidases of Kloeckera sp. and Hansenula polymorpha. Catalytic properties and subunit structures Eur. J. Biochem. 64 1976 341 350
3. K.N. Faber, W. Harder, G. Ab, and M. Veenhuis Review: methylotrophic yeasts as factories for the production of foreign proteins Yeast 11 1995 1331 1344
4. L. Rodriguez, R.E. Narciandi, H. Roca, J. Cremata, R. Montesinos, E. Rodriguez, J.M. Grillo, V. Muzio, L.S. Herrera, and J.M. Delgado Invertase secretion in Hansenula polymorpha under the AOX1 promoter from Pichia pastoris Yeast 12 1996 815 822
5. W.C. Raschke, B.R. Neiditch, M. Hendricks, and J.M. Cregg Inducible expression of a heterologous protein in Hansenula polymorpha using the alcohol oxidase 1 promoter of Pichia pastoris Gene 177 1996 163 167
6. K.N. Faber, S. Westra, H.R. Waterham, I. Keizer-Gunnink, W. Harder, and M. Veenhuis Foreign gene expression in Hansenula polymorpha. A system for the synthesis of small functional peptides Appl. Microbiol. Biotechnol. 45 1996 72 79
7. A.G. de Prada, N. Pena, M.L. Mena, A.J. Reviejo, and J.M. Pingarron Graphite-teflon composite bienzyme amperometric biosensors for monitoring of alcohols Biosens. Bioelectron. 18 2003 1279 1288
8. T. Hasunuma, S. Kuwabata, E. Fukusaki, and A. Kobayashi Real-time quantification of methanol in plants using a hybrid alcohol oxidase-peroxidase biosensor Anal. Chem. 76 2004 1500 1506
9. K. Mitsubayashi, H. Matsunaga, G. Nishio, S. Toda, and Y. Nakanishi Bioelectronic sniffers for ethanol and acetaldehyde in breath air after drinking Biosens. Bioelectron. 20 2005 1573 1579
10. J.P. van Dijken, R. Otto, and W. Harder Growth of Hansenula polymorpha in a methanol-limited chemostat. Physiological responses due to the involvement of methanol oxidase as a key enzyme in methanol metabolism Arch. Microbiol. 111 1976 137 144
11. M. Veenhuis, J.P. van Dijken, and W. Harder The significance of peroxisomes in the metabolism of one-carbon compounds in yeasts Adv. Microb. Physiol 24 1983 1 82
12. M.L.F. Guiseppin, H.M.L. van Eijk, and B.C.M. Bes Molecular regulation of alcohol oxidase in Hansenula polymorpha in continuous cultures Biotechnol. Bioeng. 32 1988 577 583
13. S. Godecke, M. Eckart, Z.A. Janowicz, and C.P. Hollenberg Identification of sequences responsible for transcriptional regulation of the strongly expressed methanol oxidase-encoding gene in Hansenula polymorpha Gene 139 1994 35 42
14. G. Costanzo, E. Di Mauro, R. Negri, G. Pereira, and C. Hollenberg Multiple overlapping positions of nucleosomes with single in vivo rotational setting in the Hansenula polymorpha RNA polymerase II MOX promoter J. Biol. Chem. 270 1995 11091 11097
15. V. Genu, S. Godecke, C.P. Hollenberg, and G.G. Pereira The Hansenula polymorpha MOX gene presents two alternative transcription start points differentially utilized and sensitive to respiratory activity Eur. J. Biochem. 270 2003 2467 2475
16. R. Roggenkamp, Z. Janowicz, B. Stanikowski, and C.P. Hollenberg Biosynthesis and regulation of the peroxisomal methanol oxidase from the methylotrophic yeast Hansenula polymorpha Mol. Gen. Genet. 194 1984 489 493
17. A.A. Sibirny, V. Titorenko, B.D. Efremov, and I.I. Tolstorukov Multiplicity of mechanisms of carbon catabolite repression involved in the synthesis of alcohol oxidase in the methylotrophic yeast Pichia pinus Yeast 3 1987 233 241
18. P. Ozimek, K. Lahtchev, J.A. Kiel, M. Veenhuis, and I.J. van der Klei Hansenula polymorpha Swi1p and Snf2p are essential for methanol utilisation FEMS Yeast Res. 4 2004 673 682
19. J.M. Cregg, K.R. Madden, K.J. Barringer, G.P. Thill, and C.A. Stillman Functional characterization of the two alcohol oxidase genes from the yeast Pichia pastoris Mol. Cell Biol. 9 1989 1316 1323
20. K.B. Zwart, M. Veenhuis, and W. Harder Significance of yeast peroxisomes in the metabolism of choline and ethanolamine Antonie Van Leeuwenhoek 49 1983 369 385
21. T. Egli, O. Kappeli, and A. Fiechter Regulatory flexibility of methylotrophic yeast in chemostat cultures: simultaneous assimilation of glucose and methanol at fixed dilution rate Arch. Microbiol. 131 1982 1 7
22. M.B. Gruzman, V.I. Titorenko, V.V. Ashin, K.A. Lusta, and Y.A. Trotsenko Multiple molecular forms of alcohol oxidase from the methylotrophic yeast Pichia methanolica Biochemistry (Moscow) 61 1996 1537 1544
23. T. Nakagawa, H. Mukaiyama, H. Yurimoto, Y. Sakai, and N. Kato Alcohol oxidase hybrid oligomers formed in vivo and in vitro Yeast 15 1999 1223 1230
24. P. Koutz, G.R. Davis, C. Stillman, K. Barringer, J. Cregg, and G. Thill Structural comparison of the Pichia pastoris alcohol oxidase genes Yeast 5 1989 167 177
25. O.V. Stasyk, O.G. Stasyk, J. Komduur, M. Veenhuis, J.M. Cregg, and A.A. Sibirny A hexose transporter homologue controls glucose repression in the methylotrophic yeast Hansenula polymorpha J. Biol. Chem. 279 2004 8116 8125
26. T. Kramarenko, H. Karp, A. Jarviste, and T. Alamäe Sugar repression in the methylotrophic yeast Hansenula polymorpha studied by using hexokinase-negative, glucokinase-negative and double kinase-negative mutants Folia Microbiol. (Praha) 45 2000 521 529
27. S. Laht, H. Karp, P. Kotka, A. Jarviste, and T. Alamäe Cloning and characterization of glucokinase from a methylotrophic yeast Hansenula polymorpha: different effects on glucose repression in H. polymorpha and Saccharomyces cerevisiae Gene 296 2002 195 203
28. H. Karp, A. Jarviste, T.M. Kriegel, and T. Alamäe Cloning and biochemical characterization of hexokinase from the methylotrophic yeast Hansenula polymorpha Curr. Genet. 44 2003 268 276
29. A.R. Kulachkovsky, O.M. Moroz, and A.A. Sibirny Impairment of peroxisome degradation in Pichia methanolica mutants defective in acetyl-CoA synthetase or isocitrate lyase Yeast 13 1997 1043 1052
30. O.M. Moroz, M.V. Gonchar, and A.A. Sibirny Efficient bioconversion of ethanol to acetaldehyde using a novel mutant strain of the methylotrophic yeast Hansenula polymorpha Biotechnol. Bioeng. 68 2000 44 51
31. Y. Tani, T. Sawai, and Y. Sakai Production of catalytic cells for formaldehyde production and alcohol oxidase by a catabolite repression- insensitive mutant of a methanol yeast Candida boidinii A5 Biotechnol. Bioeng. 32 1988 1165 1169
32. R. Roggenkamp Constitutive appearance of peroxisomes in a regulatory mutant of the methylotrophic yeast Hansenula polymorpha Mol. Gen. Genet. 213 1988 535 540
33. T. Alamäe, and J. Simisker Isolation and preliminary characterization of Pichia pinus mutants insensitive to glucose repression Yeast 10 1994 1459 1466
34. T. Alamäe, and L. Liiv Glucose repression of maltase and methanol-oxidizing enzymes in the methylotrophic yeast Hansenula polymorpha: isolation and study of regulatory mutants Folia Microbiol. (Praha) 43 1998 443 452
35. G. Parpinello, E. Berardi, and R. Strabbioli A regulatory mutant of Hansenula polymorpha exhibiting methanol utilization metabolism and peroxisome proliferation in glucose J. Bacteriol. 180 1998 2958 2967
36. T. Hristozova, L. Michailova, D. Tuneva, V. Gotcheva, A. Angelov, and Z. Roshkova Mutant Hansenula polymorpha strain with constitutive alcohol oxidase and peroxisome biosynthesis Z. Naturforsch. 57c 2002 858 862
37. L.V. Bystrykh, L. Dijkhuizen, and W. Harder Modification of flavin adenine dinucleotide in alcohol oxidase of the yeast Hansenula polymorpha J. Gen. Microbiol. 137 1991 2381 2386
38. R.M. Kellog, W. Kruizinga, L.V. Bystrykh, L. Dijkhuizen, and W. Harder Structural analysis of a stereochemical modification of flavin adenine dinucleotide in alcohol oxidase from methylotrophic yeast Tetrahedron 48 1992 4147 4162
39. W.J. van Berkel, M.H. Eppink, and H.A. Schreuder Crystal structure of p-hydroxybenzoate hydroxylase reconstituted with the modified FAD present in alcohol oxidase from methylotrophic yeasts: evidence for an arabinoflavin Protein Sci. 3 1994 2245 2253
40. V.V. Ashin, and Y.A. Trotsenko Formation and distribution of modified FAD between isozymes of alcohol oxidase in the methylotrophic yeast Pichia methanolica Biochemistry (Mosc.) 63 1998 1407 1413
41. T. Nakagawa, T. Mizumura, H. Mukaiyama, T. Miyaji, H. Yurimoto, N. Kato, Y. Sakai, and N. Tomizuka Physiological role of the second alcohol oxidase gene MOD2 in the methylotrophic growth of Pichia methanolica Yeast 19 2002 1067 1073
42. T. Mincey, G. Tayrien, A.S. Mildvan, and R.H. Abeles Presence of a flavin semiquinone in methanol oxidase Proc. Natl. Acad. Sci. USA 77 1980 7099 7101
43. P.G. Bruinenberg, M. Veenhuis, J.P. van Dijken, J.A. Duine, and W. Harder A quantitative analysis of selective inactivation of peroxisomal enzymes in the yeast Hansenula polymorpha by high-performance liquid chromatography FEMS Microbiol. Lett. 15 1982 45 50
44. M. Veenhuis, A.C. Douma, W. Harder, and M. Osumi Degradation and turnover of peroxisomes in the yeast Hansenula polymorpha induced by selective inactivation of peroxisomal enzymes Arch. Microbiol. 134 1983 193 203
45. I.J. van der Klei, W. Harder, and M. Veenhuis Selective inactivation of alcohol oxidase in two peroxisome-deficient mutants of the yeast Hansenula polymorpha Yeast 7 1991 813 821
46. W.D. Murray, and S.J. Duff Catabolite inactivation in the methylotrophic yeast Pichia pastoris Appl. Environ. Microbiol. 56 1990 2378 2383
47. M. Veenhuis, J.P. van Dijken, and W. Harder Cytochemical studies on the localization of methanol oxidase and other oxidases in peroxisomes of methanol-grown Hansenula polymorpha Arch. Microbiol. 111 1976 123 135
48. A.N. Leão, and J.A. Kiel Peroxisome homeostasis in Hansenula polymorpha FEMS Yeast Res. 4 2003 131 139
49. A.R. Bellu, and J.A. Kiel Selective degradation of peroxisomes in yeasts Microsc. Res. Tech. 61 2003 161 170
50. C.W. Boys, D.J. Hill, P.G. Stockley, and J.R. Woodward Crystallization of alcohol oxidase from Pichia pastoris J. Mol. Biol. 208 1989 211 212
51. I.J. van der Klei, C.L. Lawson, H. Rozeboom, B.W. Dijkstra, M. Veenhuis, W. Harder, and W.G. Hol Use of electron microscopy in the examination of lattice defects in crystals of alcohol oxidase FEBS Lett. 244 1989 213 216
52. E. Tykarska, L. Lebioda, E. Marchut, J. Steczko, and B. Stec Crystallization of alcohol oxidase from Pichia pastoris. Secondary structure predictions indicate a domain with the eightfold beta/alpha-barrel fold J. Protein Chem. 9 1990 83 86
53. R. Boteva, A.J. Visser, B. Filippi, G. Vriend, M. Veenhuis, and I.J. van der Klei Conformational transitions accompanying oligomerization of yeast alcohol oxidase, a peroxisomal flavoenzyme Biochemistry 38 1999 5034 5044
54. H.J. Hecht, H.M. Kalisz, J. Hendle, R.D. Schmid, and D. Schomburg Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3 Å resolution J. Mol. Biol. 229 1993 153 172
55. T. Zlateva, R. Boteva, B. Filippi, M. Veenhuis, and I.J. van der Klei Deflavination of flavo-oxidases by nucleophilic reagents Biochim. Biophys. Acta 1548 2001 213 219
56. M. Veenhuis, W. Harder, J.P. van Dijken, and F. Mayer Substructure of crystalline peroxisomes in methanol-grown Hansenula polymorpha: evidence for an in vivo crystal of alcohol oxidase Mol. Cell Biol. 1 1981 949 957
57. J. Vonck, and E.F. van Bruggen Architecture of peroxisomal alcohol oxidase crystals from the methylotrophic yeast Hansenula polymorpha as deduced by electron microscopy J. Bacteriol. 174 1992 5391 5399
58. I. Keizer, R. Roggenkamp, W. Harder, and M. Veenhuis Location of catalase in crystalline peroxisomes of methanol-grown Hansenula polymorpha FEMS Microbiol. Lett. 72 1992 7 11
59. M. Osumi, M. Nagano, N. Yamada, J. Hosoi, and M. Yanagida Three-dimensional structure of the crystalloid in the microbody of Kloeckera sp.: composite crystal model J. Bacteriol. 151 1982 376 383
60. I.J. van der Klei, G.J. Sulter, W. Harder, and M. Veenhuis Assembly of alcohol oxidase in the cytosol of a peroxisome-deficient mutant of Hansenula polymorpha - properties of the protein and architecture of the crystals Yeast 7 1991 195 209
61. H.R. Waterham, V.I. Titorenko, G.J. Swaving, W. Harder, and M. Veenhuis Peroxisomes in the methylotrophic yeast Hansenula polymorpha do not necessarily derive from pre-existing organelles EMBO J. 12 1993 4785 4794
62. B. Distel, I. van der Ley, M. Veenhuis, and H.F. Tabak Alcohol oxidase expressed under nonmethylotrophic conditions is imported, assembled, and enzymatically active in peroxisomes of Hansenula polymorpha J. Cell Biol. 107 1988 1669 1675
63. M.E. Evers, V.I. Titorenko, I.J. van der Klei, W. Harder, and M. Veenhuis Assembly of alcohol oxidase in peroxisomes of the yeast Hansenula polymorpha requires the cofactor flavin adenine dinucleotide Mol. Biol. Cell 5 1994 829 837
64. M.E. Evers, V.I. Titorenko, W. Harder, I.J. van der Klei, and M. Veenhuis Flavin adenine dinucleotide binding is the crucial step in alcohol oxidase assembly in the yeast Hansenula polymorpha Yeast 12 1996 917 923
65. K. Gunkel, R. van Dijk, M. Veenhuis, and I.J. van der Klei Routing of Hansenula polymorpha alcohol oxidase: an alternative peroxisomal protein-sorting machinery Mol. Biol. Cell 15 2004 1347 1355
66. R. van Dijk, K.L. Lahtchev, A.M. Kram, I.J. van der Klei, and M. Veenhuis Isolation of mutants of Hansenula polymorpha defective in the assembly of octameric alcohol oxidase FEMS Yeast Res. 1 2002 257 263
67. P. Ozimek, R. van Dijk, K. Latchev, C. Gancedo, D.Y. Wang, I.J. van der Klei, and M. Veenhuis Pyruvate carboxylase is an essential protein in the assembly of yeast peroxisomal oligomeric alcohol oxidase Mol. Biol. Cell 14 2003 786 797
68. I.J. van der Klei, R.E. Hilbrands, G.J. Swaving, H.R. Waterham, E.G. Vrieling, V.I. Titorenko, J.M. Cregg, W. Harder, and M. Veenhuis The Hansenula polymorpha PER3 gene is essential for the import of PTS1 proteins into the peroxisomal matrix J. Biol. Chem. 270 1995 17229 17236
69. H.R. Waterham, K.A. Russell, Y. Vries, and J.M. Cregg Peroxisomal targeting, import, and assembly of alcohol oxidase in Pichia pastoris J. Cell Biol. 139 1997 1419 1431
70. S.J. Gould, G.A. Keller, and S. Subramani Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase J. Cell Biol. 105 1987 2923 2931
71. B.W. Swinkels, S.J. Gould, and S. Subramani Targeting efficiencies of various permutations of the consensus C-terminal tripeptide peroxisomal targeting signal FEBS Lett. 305 1992 133 136
72. S.R. Terlecky, W.M. Nuttley, D. McCollum, E. Sock, and S. Subramani The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal EMBO J. 14 1995 3627 3634
73. V.I. Titorenko, J.M. Nicaud, H. Wang, H. Chan, and R.A. Rachubinski Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica J. Cell Biol. 156 2002 481 494
74. A.T. Klein, M. van den Berg, G. Bottger, H.F. Tabak, and B. Distel Saccharomyces cerevisiae acyl-CoA oxidase follows a novel, non-PTS1, import pathway into peroxisomes that is dependent on Pex5p J. Biol. Chem. 277 2002 25011 25019
75. J.A. McNew, and J.M. Goodman The targeting and assembly of peroxisomal proteins: some old rules do not apply Trends Biochem. Sci. 21 1996 54 58
76. Gunkel, K., Veenhuis, M. and van der Klei, I.J. (in press). Protein translocation machineries: how organelles bring in matrix proteins. FEMS Yeast Res., doi:10.1016/j.femsyr.2005.03.004.
77. K.N. Faber, R. van Dijk, I. Keizer-Gunnink, A. Koek, I.J. van der Klei, and M. Veenhuis Import of assembled PTS1 proteins into peroxisomes of the yeast Hansenula polymorpha: yes and no Biochim. Biophys. Acta 1591 2002 157 162
78. M.Q. Stewart, R.D. Esposito, J. Gowani, and J.M. Goodman Alcohol oxidase and dihydroxyacetone synthase, the abundant peroxisomal proteins of methylotrophic yeasts, assemble in different cellular compartments J. Cell Sci. 114 2001 2863 2868
79. I.J. van der Klei, W. Harder, and M. Veenhuis Methanol metabolism in a peroxisome-deficient mutant of Hansenula polymorpha: a physiological study Arch. Microbiol. 156 1991 15 23
80. I.J. van der Klei, and M. Veenhuis Peroxisome biogenesis in the yeast Hansenula polymorpha: a structural and functional analysis Ann. N.Y. Acad. Sci. 804 1996 47 59
81. V. Dammai, and S. Subramani The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol Cell 105 2001 187 196
82. M.Q. Stewart, R. van Dijk, M. Veenhuis, and J.M. Goodman Monomeric alcohol oxidase is preferentially digested by a novel protease from Candida boidinii Biochim. Biophys. Acta 1542 2002 160 172
83. M. Kikuchi, N. Hatano, S. Yokota, N. Shimozawa, T. Imanaka, and H. Taniguchi Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease J. Biol. Chem. 279 2004 421 428
84. F.W. Janssen, R.M. Kerwin, and H.W. Ruelius Alcohol oxidase, a novel enzyme from a basidiomycete Biochem. Biophys. Res. Commun. 20 1965 630 634
85. A.M. Ledeboer, L. Edens, J. Maat, C. Visser, J.W. Bos, C.T. Verrips, Z. Janowicz, M. Eckart, R. Roggenkamp, and C.P. Hollenberg Molecular cloning and characterization of a gene coding for methanol oxidase in Hansenula polymorpha Nucleic Acids Res. 13 1985 3063 3082
86. C.K. Raymond, T. Bukowski, S.D. Holderman, A.F. Ching, E. Vanaja, and M.R. Stamm Development of the methylotrophic yeast Pichia methanolica for the expression of the 65 kilodalton isoform of human glutamate decarboxylase Yeast 14 1998 11 23
87. Y. Sakai, and Y. Tani Cloning and sequencing of the alcohol oxidase-encoding gene (AOD1) from the formaldehyde-producing asporogeneous methylotrophic yeast, Candida boidinii S2 Gene 114 1992 67 73
88. K. Holzmann, E. Schreiner, and H. Schwab A Penicillium chrysogenum gene (AOX) identified by specific induction upon shifting pH encodes for a protein which shows high homology to fungal alcohol oxidases Curr. Genet. 40 2002 339 344
89. G. Segers, N. Bradshaw, D. Archer, K. Blissett, and R.P. Oliver Alcohol oxidase is a novel pathogenicity factor for Cladosporium fulvum, but aldehyde dehydrogenase is dispensable Mol. Plant Microbe Interact. 14 2001 367 377
90. A.I. Soldevila, and S.A. Ghabrial A novel alcohol oxidase/RNA-binding protein with affinity for mycovirus double-stranded RNA from the filamentous fungus Helminthosporium (Cochliobolus) victoriae: molecular and functional characterization J. Biol. Chem. 276 2001 4652 4661