1887

Abstract

Here the identification and characterization of a gene encoding a copper-trafficking enzyme, (opper-ransporting TPase), from the basidiomycete are described. This P-type copper ATPase gene has two alleles, differing primarily in the length of the second, unusually long intron, and encodes a 983 aa protein with 40 % sequence identity to yeast Ccc2p. Overexpression of in yeast grown in the presence of copper led to a 15-fold increase in laccase yields, while overexpression of and , a previously identified copper homeostasis gene of . , was additive, leading to a 20-fold increase in laccase production. In . , overexpression of and led to an eightfold increase in laccase expression, and a cotransformant still expressed laccase at 3000 μM copper when hardly any laccase activity is detected in the wild-type strain. Apparently, at low to moderate levels of copper and overexpression disturbs the normal hierarchy of copper distribution, resulting in more being directed to the Golgi, while with high copper amounts that normally switch on the copper detoxification processes, and gene products seem to out-compete the metallothionein copper chaperones, meaning laccase is still supplied with copper. These results may lead to a better understanding of copper trafficking and the hierarchy of copper distribution in the cell, and possibly be useful for constructing laccase-overproducing strains for biotechnological purposes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26177-0
2003-08-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/8/mic1492039.html?itemId=/content/journal/micro/10.1099/mic.0.26177-0&mimeType=html&fmt=ahah

References

  1. Ballance, D. J. ( 1986; ). Sequences important for gene expression in filamentous fungi. Yeast 2, 229–236.[CrossRef]
    [Google Scholar]
  2. Bartholomew, K., Dos Santos, G., Dumonceaux, T., Charles, T. & Archibald, F. ( 2000; ). Genetic transformation of Trametes versicolor to phleomycin resistance with the dominant selectable marker shble. Appl Microbiol Biotechnol 56, 201–204.
    [Google Scholar]
  3. Beeler, T. J., Fu, D., Rivera, J., Monaghan, E., Gable, K. & Dunn, T. M. ( 1997; ). SUR1 (CSG1/BCL21), a gene necessary for growth of Saccharomyces cerevisiae in the presence of high Ca2+ concentrations at 37 °C, is required for mannosylation of inositolphosphorylceramide. Mol Gen Genet 255, 570–579.[CrossRef]
    [Google Scholar]
  4. Call, H. P. & Mücke, I. ( 1997; ). History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (Lignozyme®-process). J Biotechnol 53, 163–202.[CrossRef]
    [Google Scholar]
  5. Eide, D. J., Bridgham, J. T., Zhao, Z. & Mattoon, J. R. ( 1993; ). The vacuolar H(+)-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism. Mol Gen Genet 241, 447–456.
    [Google Scholar]
  6. Felby, C., Petersen, L. S. & Nielsen, B. R. ( 1997; ). Enhanced auto adhesion of wood fibers using phenol oxidases. Holzforschung 51, 281–286.[CrossRef]
    [Google Scholar]
  7. Feldmann, H., Driller, L., Meier, B., Mages, G., Kellermann, J. & Winnacker, E. L. ( 1996; ). HDF2, the second subunit of the Ku homologue from Saccharomyces cerevisiae. J Biol Chem 271, 27765–27769.[CrossRef]
    [Google Scholar]
  8. Forbes, J. R., Hsi, G. & Cox, D. W. ( 1999; ). Role of the copper-binding domain in the copper transport function of ATP7B, the P-type ATPase defective in Wilson disease. J Biol Chem 274, 12408–12413.[CrossRef]
    [Google Scholar]
  9. Froeliger, E. H., Ullrich, R. C. & Novotny, C. P. ( 1989; ). Sequence analysis of the URA1 gene encoding orotidine-5′-monophosphate decarboxylase of Schizophyllum commune. Gene 83, 387–393.[CrossRef]
    [Google Scholar]
  10. Gurr, S. J., Unkles, S. E. & Kinghorn, J. E. ( 1988; ). The structure and organization of nuclear genes of filamentous fungi. In Gene Structure in Eucaryotic Microbes, pp. 93–139. Edited by J. E. Kinghorn. Oxford: IRL Press.
  11. Haak, D., Gable, K., Beeler, T. & Dunn, T. ( 1997; ). Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. J Biol Chem 272, 29704–29710.[CrossRef]
    [Google Scholar]
  12. Hasler, D. W., Jensen, L. T., Zerbe, O., Winge, D. R. & Vasak, M. ( 2000; ). Effect of the two conserved prolines of human growth inhibitory factor (metallothionein-3) on its biological activity and structure fluctuation: comparison with a mutant protein. Biochemistry 39, 14567–14575.[CrossRef]
    [Google Scholar]
  13. Himelblau, E., Mira, H., Lin, S. J., Culotta, V. C., Penarrubia, L. & Amasino, R. M. ( 1998; ). Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol 117, 1227–1234.[CrossRef]
    [Google Scholar]
  14. Hirayama, T., Kieber, J. J. & Hirayama, N. & 7 other authors ( 1999; ). RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97, 383–393.[CrossRef]
    [Google Scholar]
  15. Huffman, D. L. & O'Halloran, T. V. ( 2000; ). Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J Biol Chem 275, 18611–18614.[CrossRef]
    [Google Scholar]
  16. Hung, I. H., Suzuki, M., Yamaguchi, Y., Yuan, D. S., Klausner, R. D. & Gitlin, J. D. ( 1997; ). Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J Biol Chem 272, 21461–21466.[CrossRef]
    [Google Scholar]
  17. Klomp, L. W., Lin, S. J., Yuan, D. S., Klausner, R. D., Culotta, V. C. & Gitlin, J. D. ( 1997; ). Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis. J Biol Chem 272, 9221–9226.[CrossRef]
    [Google Scholar]
  18. Logemann, J., Schell, J. & Willmitzer, L. ( 1987; ). Improved method for the isolation of RNA from plant tissues. Anal Biochem 163, 16–20.[CrossRef]
    [Google Scholar]
  19. O'Halloran, T. V. & Culotta, V. C. ( 2000; ). Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275, 25057–25060.[CrossRef]
    [Google Scholar]
  20. Oh, W. J., Kim, E. K., Ko, J. H., Yoo, S. H., Hahn, S. H. & Yoo, O. J. ( 2002; ). Nuclear proteins that bind to metal response element a (MREa) in the Wilson disease gene promoter are Ku autoantigens and the Ku-80 subunit is necessary for basal transcription of the WD gene. Eur J Biochem 269, 2151–2161.[CrossRef]
    [Google Scholar]
  21. Payne, A. S. & Gitlin, J. D. ( 1998; ). Functional expression of the Menkes disease protein reveals common biochemical mechanisms among the copper-transporting P-type ATPases. J Biol Chem 273, 3765–3770.[CrossRef]
    [Google Scholar]
  22. Pena, M. M., Lee, J. & Thiele, D. J. ( 1999; ). A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129, 1251–1260.
    [Google Scholar]
  23. Perego, P., Jimenez, G. & Howell, S. B. ( 1996; ). Isolation and characterization of a cisplatin-resistant strain of Schizosaccharomyces pombe. Mol Pharmacol 50, 1080–1086.
    [Google Scholar]
  24. Petris, M. J., Mercer, J. F., Culvenor, J. G., Lockhart, P., Gleeson, P. A. & Camakaris, J. ( 1996; ). Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J 15, 6084–6095.
    [Google Scholar]
  25. 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.[CrossRef]
    [Google Scholar]
  26. Pukkila, P. J. & Casselton, L. A. ( 1991; ). Molecular genetics of the agaric Coprinus cinerius. In More Gene Manipulations in Fungi, pp. 126–150. Edited by J. W. Bennett & L. L. Lasure. San Diego: Academic Press.
  27. Rosenau, T., Potthast, A., Chen, C. L. & Gratzl, J. S. ( 1996; ). A mild, simple and general procedure for the oxidation of benzyl alcohols to benzaldehydes. Synth Commun 26, 315–320.[CrossRef]
    [Google Scholar]
  28. Sariaslani, F. S. ( 1989; ). Microbial enzymes for oxidation of organic molecules. Crit Rev Biotechnol 9, 171–257.[CrossRef]
    [Google Scholar]
  29. Shatzman, A. R. & Kosman, D. J. ( 1978; ). The utilization of copper and its role in the biosynthesis of copper-containing proteins in the fungus, Dactylium dendroides. Biochim Biophys Acta 544, 163–179.[CrossRef]
    [Google Scholar]
  30. Uldschmid, A., Engel, M., Dombi, R. & Marbach, K. ( 2002; ). Identification and functional expression of tahA, a filamentous fungal gene involved in copper trafficking to the secretory pathway in Trametes versicolor. Microbiology 148, 4049–4058.
    [Google Scholar]
  31. Voskoboinik, I., Greenough, M., La Fontaine, S., Mercer, J. F. & Camakaris, J. ( 2001; ). Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochem Biophys Res Commun 281, 966–970.[CrossRef]
    [Google Scholar]
  32. Wakabayashi, T., Nakamura, N., Sambongi, Y., Wada, Y., Oka, T. & Futai, M. ( 1998; ). Identification of the copper chaperone, CUC-1, in Caenorhabditis elegans: tissue specific coexpression with the copper transporting ATPase, CUA-1. FEBS Lett 440, 141–146.[CrossRef]
    [Google Scholar]
  33. Yuan, D. S., Stearman, R., Dancis, A., Dunn, T., Beeler, T. & Klausner, R. D. ( 1995; ). The Menkes/Wilson disease gene homologue in yeast provides copper to a ceruloplasmin-like oxidase required for iron uptake. Proc Natl Acad Sci U S A 92, 2632–2636.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26177-0
Loading
/content/journal/micro/10.1099/mic.0.26177-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error