Mechanisms of copper loading on the Schizosaccharomyces pombe copper amine oxidase 1 expressed in Saccharomyces cerevisiae

Microbiology

Volumn 152, Issue 9, 2006, Pages 2819-2830

  Laliberté, Julie ^a   Labbé, Simon ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE OXIDASE (COPPER CONTAINING); CARRIER PROTEIN; CD11B ANTIGEN; CHAPERONE; COPPER; COPPER TRANSPORTER 1; COPPER TRANSPORTER 3; ETHYLAMINE; GREEN FLUORESCENT PROTEIN; PROTEIN ATX1; SCHIZOSACCHAROMYCES POMBE COPPER AMINE OXIDASE 1; SCHIZOSACCHAROMYCES POMBE COPPER AMINE OXIDASE 2; SCHIZOSACCHAROMYCES POMBE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATION FUNCTION; CULTURE MEDIUM; CYTOSOL; DEAMINATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; FUNGAL GENETICS; FUNGUS CULTURE; FUNGUS GROWTH; FUNGUS MUTANT; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ALLELES; AMINE OXIDASE (COPPER-CONTAINING); COPPER; CULTURE MEDIA; CYTOSOL; ETHYLAMINES; GENE DELETION; GENES, BACTERIAL; GREEN FLUORESCENT PROTEINS; NITROGEN; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 33748809517     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.28998-0     Document Type: Article

References (60)

1. Abajian, C., Yatsunyk, L. A., Ramirez, B. E. & Rosenzweig, A. C. (2004). Yeast Cox17 solution structure and copper(I) binding. J Biol Chem 279, 53584-53592.
2. Banci, L., Bertini, I., Ciofi-Baffoni, S., Huffman, D. L. & O'Halloran, T. V. (2001). Solution structure of the yeast copper transporter domain Ccc2a in the apo and Cu(I)-loaded states. J Biol Chem 276, 8415-8426.
3. Beaudoin, J. & Labbé, S. (2001). The fission yeast copper-sensing transcription factor Cuf1 regulates the copper transporter gene expression through an Ace1/Amt1-like recognition sequence. J Biol Chem 276, 15472-15480.
4. Beaudoin, J., Laliberté, J. & Labbé, S. (2006). Functional dissection of Ctr4 and Ctr5 amino-terminal regions reveals motifs with redundant roles in copper transport. Microbiology 152, 209-222.
5. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P. & Boeke, J. D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
6. Brazeau, B. J., Johnson, B. J. & Wilmot, C. M. (2004). Copper-containing amine oxidases. Biogenesis and catalysis; a structural perspective. Arch Biochem Biophys 428, 22-31.
7. Brocard, C., Kragler, F., Simon, M. M., Schuster, T. & Hartig, A. (1994). The tetratricopeptide repeat-domain of the PAS10 protein of Saccharomyces cerevisiae is essential for binding the peroxisomal targeting signal-SKL. Biochem Biophys Res Commun 204, 1016-1022.
8. Bruun, L. & Houen, G. (1996). In situ detection of diamine oxidase activity using enhanced chemiluminescence. Anal Biochem 233, 130-136.
9. Cai, D. & Klinman, J. P. (1994a). Copper amine oxidase: heterologous expression, purification, and characterization of an active enzyme in Saccharomyces cerevisiae. Biochemistry 33, 7647-7653.
10. Cai, D. & Klinman, J. P. (1994b). Evidence of a self-catalytic mechanism of 2,4,5-trihydroxyphenylalanine quinone biogenesis in yeast copper amine oxidase. J Biol Chem 269, 32039-32042.
11. Cai, D., Williams, N. K. & Klinman, J. P. (1997). Effect of metal on 2,4,5-trihydroxyphenylalanine (topa) quinone biogenesis in the Hansenula polymorpha copper amine oxidase. J Biol Chem 272, 19277-19281.
12. Carr, H. S. & Winge, D. R. (2003). Assembly of cytochrome c oxidase within the mitochondrion. Acc Chem Res 36, 309-316.
13. Culotta, V. C., Klomp, L. W., Strain, J., Casareno, R. L., Krems, B. & Gitlin, J. D. (1997). The copper chaperone for superoxide dismutase. J Biol Chem 272, 23469-23472.
14. Dancis, A., Klausner, R. D., Hinnebusch, A. G. & Barriocanal, J. G. (1990). Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 10, 2294-2301.
15. Dancis, A., Yuan, D. S., Haile, D., Askwith, C., Eide, D., Moehle, C., Kaplan, J. & Klausner, R. D. (1994a). Molecular characterization of a copper transport protein in Saccharomyces cerevisiae: an unexpected role for copper in iron transport. Cell 76, 393-402.
16. Dancis, A., Haile, D., Yuan, D. S. & Klausner, R. D. (1994b). The Saccharomyces cerevisiae copper transport protein (Ctrlp): biochemical characterization, regulation by copper, and physiological role in copper uptake. J Biol Chem 269, 25660-25667.
17. Dawkes, H. C. & Phillips, S. E. (2001). Copper amine oxidase: cunning cofactor and controversial copper. Curr Opin Struct Biol 11, 666-673.
18. Duff, A. P., Cohen, A. E., Ellis, P. J., Kuchar, J. A., Langley, D. B., Shepard, E. M., Dooley, D. M., Freeman, H. C. & Guss, J. M. (2003). The crystal structure of Pichia pastoris lysyl oxidase. Biochemistry 42, 15148-15157.
19. Faber, K. N., Haima, P., Gietl, C., Harder, W., Ab, G. & Veenhuis, M. (1994). The methylotrophic yeast Hansenula polymorpha contains an inducible import pathway for peroxisomal matrix proteins with an N-terminal targeting signal (PTS2 proteins). Proc Natl Acad Sci U S A 91, 12985-12989.
20. Forsburg, S. L., Sherman, D. A., Ottilie, S., Yasuda, J. R. & Hodson, J. A. (1997). Mutational analysis of Cdc19p, a Schizosaccharomyces pombe MCM protein. Genetics 147, 1025-1041.
21. Georgatsou, E. & Alexandraki, D. (1994). Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 14, 3065-3073.
22. Glerum, D. M., Shtanko, A. & Tzagoloff, A. (1996). Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 271, 14504-14509.
23. Gurvitz, A., Rottensteiner, H., Kilpelainen, S. H., Hartig, A., Hiltunen, J. K., Binder, M., Dawes, I. W. & Hamilton, B. (1997). The Saccharomyces cerevisiae peroxisomal 2,4-dienoyl-CoA reductase is encoded by the oleate-inducible gene SPS19. J Biol Chem 272, 22140-22147.
24. Harding, T. M., Morano, K. A., Scott, S. V. & Klionsky, D. J. (1995). Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J Cell Biol 131, 591-602.
25. Hassett, R. & Kosman, D. J. (1995). Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J Biol Chem 270, 128-134.
26. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
27. Horng, Y. C., Cobine, P. A., Maxfield, A. B., Carr, H. S. & Winge, D. R. (2004). Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome c oxidase. J Biol Chem 279, 35334-35340.
28. Jalkanen, S. & Salmi, M. (2001). Cell surface monoamine oxidases: enzymes in search of a function. EMBO J 20, 3893-3901.
29. Knight, S. A., Labbé, S., Kwon, L. F., Kosman, D. J. & Thiele, D. J. (1996). A widespread transposable element masks expression of a yeast copper transport gene. Genes Dev 10, 1917-1929.
30. Kumar, V., Dooley, D. M., Freeman, H. C., Guss, J. M., Harvey, I., McGuirl, M. A., Wilce, M. C. & Zubak, V. M. (1996). Crystal structure of a eukaryotic (pea seedling) copper-containing amine oxidase at 2.2 A resolution. Structure 4, 943-955.
31. Labbé, S., Zhu, Z. & Thiele, D. J. (1997). Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. J Biol Chem 272, 15951-15958.
32. Laliberté, J., Whitson, L. J., Beaudoin, J., Holloway, S. P., Hart, P. J. & Labbé, S. (2004). The Schizosaccharomyces pombe pccs protein functions in both copper trafficking and metal detoxification pathways. J Biol Chem 279, 28744-28755.
33. Large, P. J. (1986). Degradation of organic nitrogen compounds by yeasts. Yeast 2, 1-34.
34. Li, R., Klinman, J. P. & Mathews, F. S. (1998). Copper amine oxidase from Hansenula polymorpha: the crystal structure determined at 2.4 A resolution reveals the active conformation. Structure 6, 293-307.
35. Lin, S. J., Pufahl, R. A., Dancis, A., O'Halloran, T. V. & Culotta, V. C. (1997). A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J Biol Chem 272, 9215-9220.
36. Lunelli, M., Di Paolo, M. L., Biadene, M., Calderone, V., Battistutta, R., Scarpa, M., Rigo, A. & Zanotti, G. (2005). Crystal structure of amine oxidase from bovine serum. J Mol Biol 346, 991-1004.
37. Martins, L. J., Jensen, L. T., Simon, J. R., Keller, G. L. & Winge, D. R. (1998). Metalloregulation of FRE1 and FRE2 homologs in Saccharomyces cerevisiae. J Biol Chem 273, 23716-23721.
38. Matsunami, H., Okajima, T., Hirota, S., Yamaguchi, H., Hori, H., Mure, M., Kuroda, S. & Tanizawa, K. (2004). Chemical rescue of a site-specific mutant of bacterial copper amine oxidase for generation of the topa quinine cofactor. Biochemistry 43, 2178-2187.
39. Mumberg, D., Muller, R. & Funk, M. (1995). Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122.
40. Mure, M., Brown, D. E., Saysell, C. & 7 other authors (2005). Role of the interactions between the active site base and the substrate Schiff base in amine oxidase catalysis. Evidence from structural and spectroscopic studies of the 2-hydrazinopyridine adduct of Escherichia coli amine oxidase. Biochemistry 44, 1568-1582.
41. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A. & Eisenhaber, F. (2003a). Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328, 567-579.
42. Neuberger, G., Maurer-Stroh, S., Eisenhaber, B., Hartig, A. & Eisenhaber, F. (2003b). Prediction of peroxisomal targeting signal 1 containing proteins from amino acid sequence. J Mol Biol 328, 581-592.
43. O'Halloran, T. V. & Culotta, V. C. (2000). Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275, 25057-25060.
44. Parsons, M. R., Convery, M. A., Wilmot, C. M., Yadav, K. D., Blakeley, V., Corner, A. S., Phillips, S. E., McPherson, M. J. & Knowles, P. F. (1995). Crystal structure of a quinoenzyme: copper amine oxidase of Escherichia coli at 2 A resolution. Structure 3, 1171-1184.
45. Peña, M. M., Lee, J. & Thiele, D. J. (1999). A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129, 1251-1260.
46. Peña, M. M., Puig, S. & Thiele, D. J. (2000). Characterization of the Saccharomyces cerevisiae high-affinity copper transporter Ctr3. J Biol Chem 275, 33244-33251.
47. Petriv, O. I., Tang, L., Titorenko, V. I. & Rachubinski, R. A. (2004). A new definition for the consensus sequence of the peroxisome targeting signal type 2. J Mol Biol 341, 119-134.
48. Portnoy, M. E., Rosenzweig, A. C., Rae, T., Huffman, D. L., O'Halloran, T. V. & Culotta, V. C. (1999). Structure-function analyses of the Atx1 metallochaperone. J Biol Chem 274, 15041-15045.
49. Pufahl, R. A., Singer, C. P., Peariso, K. L., Lin, S. J., Schmidt, P. J., Fahrni, C. J., Culotta, V. C., Penner-Hahn, J. E. & O'Halloran, T. V. (1997). Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278, 853-856.
50. Puig, S. & Thiele, D. J. (2002a). Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6, 171-180.
51. Puig, S., Lee, J., Lau, M. & Thiele, D. J. (2002b). Biochemical and genetic analyses of yeast and human high-affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem 277, 26021-26030.
52. Rees, E. M. & Thiele, D. J. (2004). From aging to virulence: forging connections through the study of copper homeostasis in eukaryotic microorganisms. Curr Opin Microbiol 7, 175-184.
53. Rehling, P., Marzioch, M., Niesen, F., Wittke, E., Veenhuis, M. & Kunau, W. H. (1996). The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J 15, 2901-2913.
54. Reumann, S. (2004). Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135, 783-800.
55. Rosenzweig, A. C., Huffman, D. L., Hou, M. Y., Wernimont, A. K., Pufahl, R. A. & O'Halloran, T. V. (1999). Crystal structure of the Atx1 metallochaperone protein at 1.02 A resolution. Structure 7, 605-617.
56. Rymond, B. C., Zitomer, R. S., Schumperli, D. & Rosenberg, M. (1983). The expression in yeast of the Escherichia coli galK gene on CYC1::GalK fusion plasmids. Gene 25, 249-262.
57. Samuels, N. M. & Klinman, J. P. (2005). 2,4,5-trihydroxyphenylalanine quinone biogenesis in the copper amine oxidase from Hansenula polymorpha with the alternate metal nickel. Biochemistry 44, 14308-14317.
58. Sherman, F. (1991). Getting started with yeast. Methods Enzymol 194, 3-21.
59. Veenhuis, M., Mateblowski, M., Kunau, W. H. & Harder, W. (1987). Proliferation of microbodies in Saccharomyces cerevisiae. Yeast 3, 77-84.
60. Yu, P. H., Wright, S., Fan, E. H., Lun, Z. R. & Gubisne-Harberle, D. (2003). Physiological and pathological implications of semicarbazide-sensitive amine oxidase. Biochim Biophys Acta 1647, 193-199.