1887

Abstract

Several reports have indicated that the iron–sulfur cluster [Fe–S] assembly machinery in most eukaryotes is confined to the mitochondria and chloroplasts. The best-characterized and most highly conserved [Fe–S] assembly proteins are a pyridoxal-5′-phosphate-dependent cysteine desulfurase (IscS), and IscU, a protein functioning as a scaffold for the assembly of [Fe–S] prior to their incorporation into apoproteins. In this work, genes encoding IscS and IscU homologues have been isolated and characterized from the apicomplexan parasite , an opportunistic pathogen in AIDS patients, for which no effective treatment is available. Primary sequence analysis (CpIscS and CpIscU) and phylogenetic studies (CpIscS) indicate that both genes are most closely related to mitochondrial homologues from other organisms. Moreover, the N-terminal signal sequences of CpIscS and CpIscU predicted specifically target green fluorescent protein to the mitochondrial network of the yeast . Overall, these findings suggest that the previously identified mitochondrial relict of may have been retained by the parasite as an intracellular site for [Fe–S] assembly.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26365-0
2003-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/12/mic1493519.html?itemId=/content/journal/micro/10.1099/mic.0.26365-0&mimeType=html&fmt=ahah

References

  1. Abrahamsen M. S., Schroeder A. A. 1999; Characterization of intracellular Cryptosporidium parvum gene expression. Mol Biochem Parasitol 104:141–146
    [Google Scholar]
  2. Adachi J., Hasegawa M. 1996; molphy version 2.3: programs for molecular phylogenetics based on maximum likelihood. Comput Sci Monogr 28:1–150
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J. H., Zhang Z., Miller W., Lipman D. J. 1997; Gapped Blast and Psi-Blast – a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
    [Google Scholar]
  4. Burke D., Dawson D., Stearns T. Cold Spring Harbor Laboratory 2000 Methods Yeast Genetics: a Cold Spring Harbor Laboratory Course Manual, 2000 Edition Plainview, NY: Cold Spring Harbor Laboratory;
  5. Caccio S., Larosa G., Pozio E. 1997; The beta-tubulin gene of Cryptosporidium parvum . Mol Biochem Parasitol 89:307–311
    [Google Scholar]
  6. Cammack R. 1971; Role for ferredoxin in the origin of life and biological evolution. Nature 233:136–138
    [Google Scholar]
  7. Cammack R. 1983; Evolution and diversity in the iron-sulfur proteins. Chem Scr 21:87–95
    [Google Scholar]
  8. Chen X. M., Keithly J. S., Paya C. V., LaRusso N. F. 2002; Current concepts: cryptosporidiosis. N Engl J Med 346:1723–1731
    [Google Scholar]
  9. Claros M. G., Vincens P. 1996; Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779–786
    [Google Scholar]
  10. Dutkiewicz R., Schilke B., Knieszner H., Walter W., Craig E. A., Marszalek J. 2003; Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis: similarities to and differences from its bacterial counterpart. J Biol Chem 278:29719–29727
    [Google Scholar]
  11. Dyall S., Johnson P. J. 2000; Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol 3:404–411
    [Google Scholar]
  12. Emanuelsson O., von Heijne G. 2001; Prediction of organellar targeting signals. Biochim Biophys Acta Mol Cell Res 1541114–119
    [Google Scholar]
  13. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. 2000; Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016
    [Google Scholar]
  14. Fayer R. 1997 Cryptosporidium and Cryptosporidiosis Boca Raton, FL: CRC Press;
  15. Felsenstein J. 1989; phylip – phylogeny inference package (version 3.2. Cladistics 5:164–166
    [Google Scholar]
  16. Garland S. A., Hoff K., Vickery L. E., Culotta V. C. 1999; Saccharomyces cerevisiae ISU1 and ISU2 : members of a well-conserved gene family for iron-sulfur cluster assembly. J Mol Biol 294:897–907
    [Google Scholar]
  17. Gaxiola R. A., Yuan D. S., Klausner R. D., Fink G. R. 1998; The yeast clc chloride channel functions in cation homeostasis. Proc Natl Acad Sci U S A 95:4046–4050
    [Google Scholar]
  18. Gerber J., Lill R. 2002; Biogenesis of iron-sulfur proteins in eukaryotes: components, mechanism, and pathology. Mitochondrion 2:71–86
    [Google Scholar]
  19. Hoffmann H. P., Avers C. J. 1973; Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell. Science 181:749–750
    [Google Scholar]
  20. Johnson M. K., Staples C. R., Duin E. C., Lafferty M. E., Duderstadt R. E. 1998; Novel roles for Fe–S clusters in stabilizing or generating radical intermediates. Pure Appl Chem 70:939–946
    [Google Scholar]
  21. Kaiser J. T., Clausen T., Bourenkow G. P., Bartunik H. D., Steinbacher S., Huber R. 2000; Crystal structure of a NifS-like protein from Thermotoga maritima : implications for iron sulphur cluster assembly. J Mol Biol 297:451–464
    [Google Scholar]
  22. Katinka M. D., Duprat S., Cornillot E. 14 other authors 2001; Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi . Nature 414:450–453
    [Google Scholar]
  23. Keithly J. S., Zhu G., Upton S. J., Woods K. M., Martinez M. P., Yarlett N. 1997; Polyamine biosynthesis in Cryptosporidium parvum and its implications for chemotherapy. Mol Biochem Parasitol 88:35–42
    [Google Scholar]
  24. Kishino H., Hasegawa M. 1989; Evaluation of the maximum likelihood estimate of the evolutionary tree topology from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170–179
    [Google Scholar]
  25. Kozak M. 1989; The scanning model for translation: an update. J Cell Biol 108:229–241
    [Google Scholar]
  26. LaGier M. J., Zhu G., Keithly J. S. 2001; Characterization of a heavy metal ATPase from the apicomplexan Cryptosporidium parvum . Gene 266:25–34
    [Google Scholar]
  27. Land T., Rouault T. A. 1998; Targeting of a human iron-sulfur cluster assembly enzyme, NifS, to different subcellular compartments is regulated through alternative AUG utilization. Mol Cell 2:807–815
    [Google Scholar]
  28. Lange H., Kaut A., Kispal G., Lill R. 2000; A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. Proc Natl Acad Sci U S A 97:1050–1055
    [Google Scholar]
  29. Leon S., Touraine B., Brait J. F., Lobreaux S. 2002; The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulfurase. Biochem J 366:557–564
    [Google Scholar]
  30. Lill R., Kispal G. 2000; Maturation of cellular Fe–S proteins: an essential function of mitochondria. Trends Biochem Sci 25:352–356
    [Google Scholar]
  31. Mai Z. M., Ghosh S., Frisardi M., Rosenthal B., Rogers R., Samuelson J. 1999; Hsp60 is targeted to a cryptic mitochondrion-derived organelle (“crypton”) in the microaerophilic protozoan parasite Entamoeba histolytica . Mol Cell Biol 19:2198–2205
    [Google Scholar]
  32. Maniatis T., Fritsch E. F., Sambrook J. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  33. Martin W., Müller M. 1998; The hydrogen hypothesis for the first eukaryote. Nature 392:37–41
    [Google Scholar]
  34. Martin W., Hoffmeister M., Rotte C., Henze K. 2001; An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem 382:1521–1539
    [Google Scholar]
  35. McArthur A. G., Morrison H. G., Nixon J. E. 12 other authors 2000; The Giardia genome project database. FEMS Microbiol Lett 189:271–273
    [Google Scholar]
  36. Mühlenhoff U., Lill R. 2000; Biogenesis of iron-sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochim Biophys Acta 1459370–382
    [Google Scholar]
  37. Paschen S. A., Neupert W. 2001; Protein import into mitochondria. IUBMB Life 52:101–112
    [Google Scholar]
  38. Pfanner N. 2000; Protein sorting: recognizing mitochondrial presequences. Curr Biol 10:R412–R415
    [Google Scholar]
  39. Philippe H. 1993; Must, a computer package of management utilities for sequences and trees. Nucleic Acids Res 21:5264–5272
    [Google Scholar]
  40. Philippe H., Laurent J. 1998; How good are deep phylogenetic trees?. Curr Opin Genet Dev 8:616–623
    [Google Scholar]
  41. Pilon-Smits E. A., Garifullina G. F., Abdel-Ghany S. 7 other authors 2002; Characterization of a NifS-like chloroplast protein from Arabidopsis . Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318
    [Google Scholar]
  42. Riordan C. E., Langreth S. G., Sanchez L. B., Kayser O., Keithly J. S. 1999; Preliminary evidence for a mitochondrion in Cryptosporidium parvum : phylogenetic and therapeutic implications. J Eukaryot Microbiol 46:52S–55S
    [Google Scholar]
  43. Riordan C. E., Ault J. G., Langreth S. G., Keithly J. S. 2003; Cryptosporidium parvum Cpn60 targets a relict organelle. Curr Genet 44 in press; PMID 12928750
    [Google Scholar]
  44. Roger A. J., Svard S. G., Tovar J., Clark C. G., Smith M. W., Gillin F. D., Sogin M. L. 1998; A mitochondrial-like chaperonin 60 gene in Giardia lamblia - evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A 95:229–234
    [Google Scholar]
  45. Rotte C., Henze K., Müller M., Martin W. 2000; Origins of hydrogenosomes and mitochondria. Curr Opin Microbiol 3:481–486
    [Google Scholar]
  46. Scheffler I. E. 1999; Biogenesis and metabolic pathways inside mitochondria. In The Mitochondrion pp 118–133 New York, NY: Wiley-Liss;
    [Google Scholar]
  47. Seeber F. 2002; Biogenesis of iron-sulphur clusters in amitochondriate and apicomplexan protists. Int J Parasitol 32:1207–1217
    [Google Scholar]
  48. Spano F., Crisanti A. 2000; Cryptosporidium parvum : the many secrets of a small genome. Int J Parasitol 30:553–565
    [Google Scholar]
  49. Strong W. B., Nelson R. G. 2000; Preliminary profile of the Cryptosporidium parvum genome: an expressed sequence tag and genome survey sequence analysis. Mol Biochem Parasitol 107:1–32
    [Google Scholar]
  50. Suchan P., Vyoral D., Petrak J., Sut'ak R., Rasoloson D., Nohynkova E., Dolezal P., Tachezy J. 2003; Incorporation of iron into Tritrichomonas foetus cell compartments reveals ferredoxin as a major iron-binding protein in hydrogenosomes. Microbiology 149:1911–1921
    [Google Scholar]
  51. Tachezy J., Sanchez L. B., Müller M. 2001; Mitochondrial-type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis , as indicated by the phylogeny of IscS. Mol Biol Evol 18:1919–1928
    [Google Scholar]
  52. Taylor A. B., Smith B. S., Kitada S., Kojima K., Miyaura H., Otwinowshi Z., Ito A., Deisenhofer J. 2001; Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure 9:615–625
    [Google Scholar]
  53. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. J. 2000; The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
    [Google Scholar]
  54. Tokumoto U., Nomura S., Minami Y. 7 other authors 2002; Network of protein-protein interactions among iron-sulfur cluster assembly proteins in Escherichia coli . J Biochem (Tokyo 131:713–719
    [Google Scholar]
  55. Tong W. H., Rouault T. 2000; Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J 19:5692–5700
    [Google Scholar]
  56. Tovar J., Fischer A., Clark C. G. 1999; The mitosome, a novel organelle related to mitochondria in the amitochondriate parasite Entamoeba histolytica . Mol Microbiol 32:1013–1021
    [Google Scholar]
  57. Tovar J., Leon-Avila G., Sánchez L. B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M., Lucocq J. M. 2003; Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature in press
    [Google Scholar]
  58. Urbina H. D., Silberg J. J., Hoff K. G., Vickery L. E. 2001; Transfer of sulfur from IscS to IscU during Fe/S cluster assembly. J Biol Chem 276:44521–44526
    [Google Scholar]
  59. Westermann B., Neupert W. 2000; Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae . Yeast 16:1421–1427
    [Google Scholar]
  60. Williams B.-A. P., Hirt R. P., Lucocq J. M., Embley T. M. 2002; A mitochondrial remnant in the microsporidian Trachipleistophora hominis . Nature 418:865–869
    [Google Scholar]
  61. Zapata F., Perkins M. E., Riojas Y. A., Wu T. W., Le Blancq S. M. 2002; The Cryptosporidium parvum ABC protein family. Mol Biochem Parasitol 120:157–161
    [Google Scholar]
  62. Zheng L., White R. H., Cash V. L., Jack R. F., Dean D. R. 1993; Cysteine desulfurase activity indicates a role for NifS in metallocluster biosynthesis. Proc Natl Acad Sci U S A 90:2754–2758
    [Google Scholar]
  63. Zheng L. M., White R. H., Cash V. L., Dean D. R. 1994; Mechanism for the desulfurization of l-cysteine catalyzed by the NifS gene product. Biochem 33:4714–4720
    [Google Scholar]
  64. Zhu G., LaGier M. J., Hirose S., Keithly J. S. 2000; Cryptosporidium parvum : functional complementation of a parasite transcriptional coactivator CpMBF1 in yeast. Exp Parasitol 96:195–201
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26365-0
Loading
/content/journal/micro/10.1099/mic.0.26365-0
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