Copper homeostasis and aging in the fungal model system Podospora anserina: Differential expression of PaCtr3 encoding a copper transporter

International Journal of Biochemistry and Cell Biology

Volumn 34, Issue 11, 2002, Pages 1355-1371

  Borghouts, Corina ^a   Scheckhuber, Christian Q ^a   Stephan, Oliver ^a   Osiewacz, Heinz D ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Aging; Copper homeostasis; Podospora anserina

Indexed keywords

COPPER; CYTOCHROME C OXIDASE; DIMER; IRON; MANGANESE; PERMEASE; PROTEIN; PROTEIN PACTR3; PROTEIN PASOD2; TRANSCRIPTION FACTOR GRISEA; UNCLASSIFIED DRUG; ZINC;

AGING; ARTICLE; CELL AGING; CELL CULTURE; CELL RESPIRATION; CONTROLLED STUDY; DOWN REGULATION; HOMEOSTASIS; LIFESPAN; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOSPORA ANSERINA; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; TWO HYBRID SYSTEM; WILD TYPE;

AGING; AMINO ACID SEQUENCE; ANTIPORTERS; COPPER; DIMERIZATION; FUNGAL PROTEINS; GENES, FUNGAL; HOMEOSTASIS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROMOTER REGIONS (GENETICS); SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SORDARIALES; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

PODOSPORA ANSERINA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0036830418     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1357-2725(02)00078-X     Document Type: Article

References (54)

1. Prillinger H., Esser K. The phenoloxidases of the ascomycete Podospora anserina. XIII. Action and interaction of genes controlling the formation of laccase. Mol. Gen. Genet. 156:1977;333-345.
2. Belcour L., Begel O., Picard-Bennoun M. A site-specific deletion in mitochondrial DNA of Podospora is under the control of nuclear genes. Proc. Natl. Acad. Sci. U.S.A. 88:1991;3579-3583.
3. Contamine V., Lecellier G., Belcour L., Picard-Bennoun M. Premature death in Podospora anserina: sporadic accumulation of the deleted mitochondrial genome, translational parameters and innocuity of the mating types. Genetics. 144:1996;541-555.
4. Stahl U., Lemke P.A., Tudzynski P., Kück U., Esser K. Evidence for plasmid like DNA in a filamentous fungus, the ascomycete Podospora anserina. Mol. Gen. Genet. 162:1978;341-343.
5. Cummings D.J., Belcour L., Grandchamp C. Mitochondrial DNA from Podospora anserina. II. Properties of mutant DNA and multimeric circular DNA from senescent cultures. Mol. Gen. Genet. 171:1979;239-250.
6. Osiewacz H.D., Esser K. The mitochondrial plasmid of Podospora anserina: A mobile intron of a mitochondrial gene. Curr. Genet. 8:1984;299-305.
7. Kück U., Osiewacz H.D., Schmidt U., Kappelhoff B., Schulte E., Stahl U., Esser K. The onset of senescence is affected by DNA rearrangements of a discontinuous mitochondrial gene in Podospora anserina. Curr. Genet. 9:1985;373-382.
8. Silliker M.E., Cummings D.J. Genetic and molecular analysis of a long-lived strain of Podospora anserina. Genetics. 125:1990;775-781.
9. Sellem C.H., Lecellier G., Belcour L. Transposition of a group II intron. Nature. 366:1993;176-178.
10. Schulte E., Kück U., Esser K. Extrachromosomal mutants from Podospora anserina: permanent vegetative growth in spite of multiple recombination events in the mitochondrial genome. Mol. Gen. Genet. 211:1988;342-349.
11. Borghouts C., Werner A., Elthon T., Osiewacz H.D. Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserina. Mol. Cell. Biol. 21:2001;390-399.
12. Osiewacz H.D., Nuber U. GRISEA, a putative copper-activated transcription factor from Podospora anserina involved in differentiation and senescence. Mol. Gen. Genet. 252:1996;115-124.
13. Borghouts C., Kimpel E., Osiewacz H.D. Mitochondrial DNA rearrangements of Podospora anserina are under the control of the nuclear gene grisea. Proc. Natl. Acad. Sci. U.S.A. 94:1997;10768-10773.
14. Borghouts C., Kerschner S., Osiewacz H.D. Copper-dependence of mitochondrial DNA rearrangements in Podospora anserina. Curr. Genet. 37:2000;268-275.
15. Vanlerberghe G.C., McIntosh L. Alternative oxidase: from gene to function. Ann. Rev. Plant Phys. Plant Mol. Biol. 48:1997;703-734.
16. Sluse F.E., Jarmuszkiewicz W. Alternative oxidase in the branched mitochondrial respiratory network: an overview on structure, function, regulation and role. Braz. J. Med. Biol. Res. 31:1998;733-747.
17. Marbach K., Fernandez-Larrea J., Stahl U. Reversion of a long-living, undifferentiated mutant of Podospora anserina by copper. Curr. Genet. 26:1994;184-186.
18. Jungmann J., Reins H.A., Lee J., Romeo A., Hassett R., Kosman D., Jentsch S. MAC1, a nuclear regulatory protein related to Cu-dependent transcription factors is involved in Cu/Fe utilization and stress resistance in yeast. EMBO J. 12:1993;5051-5056.
19. Graden J.A., Winge D.R. Copper-mediated repression of the activation domain in the yeast Mac1p transcription factor. Proc. Natl. Acad. Sci U.S.A. 94:1997;5550-5555.
20. Dancis A., Yuan D.S., Haile D., Askwith C.C., Eide D., Moehle C., Kaplan J., Klausner R.D. Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell. 76:1994;393-402.
21. Dancis A., Haile D., Yuan D.S., Klausner R.D. The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J. Biol. Chem. 269:1994;25660-25667.
22. Borghouts C., Osiewacz H.D. GRISEA, a copper-modulated transcription factor from Podospora anserina involved in senescence and morphogenesis, is an orthologue of MAC1 in Saccharomyces cerevisiae. Mol. Gen. Genet. 260:1998;492-502.
23. Kampfenkel K., Kushnir S., Babiychuk E., Inze D., Van Montagu M. Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J. Biol. Chem. 270:1995;28479-28486.
24. Knight S.A., Labbe S., Kwon L.F., Kosman D.J., Thiele D.J. A widespread transposable element masks expression of a yeast copper transport gene. Genes Dev. 10:1996;1917-1929.
25. Zhou B., Gitschier J. hCTR1: a human gene for copper uptake identified by complementation in yeast. Proc. Natl. Acad. Sci U.S.A. 94:1997;7481-7486.
26. Labbe S., Pena M.M., Fernandes A.R., Thiele D.J. A copper-sensing transcription factor regulates iron uptake genes in Schizosaccharomyces pombe. J. Biol. Chem. 274:1999;36252-36260.
27. Lee J., Prohaska J.R., Dagenais S.L., Glover T.W., Thiele D.J. Isolation of a murine copper transporter gene, tissue specific expression and functional complementation of a yeast copper transport mutant. Gene. 254:2000;87-96.
28. K. Esser, Podospora anserina, in: R.C. King (Ed.), Handbook of Genetics, Plenum Press, New York, 1974, pp. 531-551.
29. Finley D., Ozkaynak E., Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell. 48:1987;1035-1046.
30. F. Sherman, Getting started with yeast, in: C. Guthrie, G. Fink (Eds.), Guide to Yeast Genetics and Molecular Biology, Academic Press, San Diego, 1991, pp. 3-21.
31. R.D. Gietz, R.A. Woods, High efficiency transformation with lithium acetate, in: J.S. Johnston (Ed.), Molecular Genetics of Yeast, Oxford University Press, Oxford, 1994, pp. 121-134.
32. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:1997;3389-3402.
33. Jamet-Vierny C., Boulay J., Briand J.F. Intramolecular cross-overs generate deleted mitochondrial DNA molecules in Podospora anserina. Curr. Genet. 31:1997;162-170.
34. Punt P.J., Oliver R.P., Dingemanse M.A., Pouwels P.H., van den Hondel C.A. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene. 56:1987;117-124.
35. Flohe L., Ötting F. Superoxide dismutase assays. Methods Enzymol. 105:1984;93-104.
36. Durfee T., Becherer K., Chen P.L., Yeh S.H., Yang Y., Kilburn A.E., Lee W.H., Elledge S.J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic sub-unit. Genes Dev. 7:1993;555-569.
37. Odermatt A., Suter H., Krapf R., Solioz M. Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J. Biol. Chem. 268:1993;12775-12779.
38. Cha J.S., Cooksey D.A. Copper resistance in Pseudomonas syringae mediated by periplasmic and outer membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 88:1991;8915-8919.
39. Sturtz L.A., Diekert K., Jensen L.T., Lill R., Culotta V.C. A fraction of yeast Cu, Zn superoxide dismutase and its metallochaperone, CCS, localize to the inter-membrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276:2001;38084-38089.
40. Askwith C.C., Eide D., Van Ho A., Bernard P.S., Li L., Davis-Kaplan S., Sipe D.M., Kaplan J. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell. 76:1994;403-410.
41. de Silva D.M., Askwith C.C., Eide D., Kaplan J. The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J. Biol. Chem. 270:1995;1098-1101.
42. Martins L.J., Jensen L.T., Simon J.R., Keller G.L., Winge D.R., Simons J.R. Metalloregulation of FRE1 and FRE2 homologues in Saccharomyces cerevisiae. J. Biol. Chem. 273:1998;23716-23721.
43. Joshi A., Serpe M., Kosman D.J. Evidence for (Mac1p)2. DNA ternary complex formation in Mac1p-dependent transactivation at the CTR1 promoter. J. Biol. Chem. 274:1999;218-226.
44. Labbe S., Zhu Z., Thiele D.J. Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. J. Biol. Chem. 272:1997;15951-15958.
45. Averbeck N.B., Borghouts C., Hamann A., Specke V., Osiewacz H.D. Molecular control of copper homeostasis in filamentous fungi: increased expression of a metallothionein gene during aging of Podospora anserina. Mol. Gen. Genet. 264:2001;604-612.
46. Dufour E., Boulay J., Rincheval V., Sainsard-Chanet A. A causal link between respiration and senescence in Podospora anserina. Proc. Natl. Acad. Sci U.S.A. 97:2000;4138-4143.
47. D. van der Helm, G. Winkelman, Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi, in: G. Winkelmann, D.R. Winge (Eds.), Metal Ions in Fungi, Marcel Dekker, New York, 1994, pp. 39-98.
48. + coordination-dependent DNA binding of the transcription factor Mac1p in the regulation of copper transport. J. Biol. Chem. 276:2001;8793-8797.
49. Hamann A., Feller F., Osiewacz H.D. The degenerate DNA transposon Pat and repeat-induced point mutation (RIP) in Podospora anserina. Mol. Gen. Genet. 263:2000;1061-1069.
50. Remacle J., Raes M., Toussaint O., Renard P., Rao G. Low levels of reactive oxygen species as modulators of cell function. Mutat. Res. 316:1995;103-122.
51. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of aging. Nature. 408:2000;239-247.
52. Harman D. Role of free radicals in aging and disease. Ann. N.Y. Acad. Sci. 673:1992;126-141.
53. Maxwell D.P., Wang Y., McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. U.S.A. 96:1999;8271-8276.
54. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:1982;105-132.