Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria

Eukaryotic Cell

Volumn 3, Issue 2, 2004, Pages 483-494

  Šlapeta, Jan ^a,b   Keithly, Janet S ^a  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITÉ PARIS SUD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN 70; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; CRYPTOSPORIDIUM PARVUM; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; PHYLOGENY; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SPOROZOITE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CRYPTOSPORIDIUM PARVUM; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SPOROZOITES;

ANIMALIA; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; PROTEOBACTERIA; PROTOZOA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; TOXOPLASMA GONDII;

EID: 2342622026     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.3.2.483-494.2004     Document Type: Article

References (52)

1. Abe, Y., T. Shodai, T. Muto, K. Mihara, H. Torii, S. Nishikawa, T. Endo, and D. Kohda. 2000. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100:551-560.
2. Abrahamsen, M. S., and A. A. Schroeder. 1999. Characterization of intracellular Cryptosporidium parvum gene expression. Mol. Biochem. Parasitol. 104:141-146.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Alvarez-Pellitero, P., and A. Sitja-Bobadilla. 2002. Cryptosporidium molnari n. sp. (Apicomplexa: Cryptosporidiidae) infecting two marine fish species, Sparus aurata L. and Dicentrarchus labrax L. Int. J. Parasitol. 32:1007-1021.
5. Arisue, N, L. B. Sánchez, L. M. Weiss, M. Müller, and T. Hashimoto. 2002. Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol. Int. 51:9-16.
6. Bankier, A. T., H. F. Spriggs, B. Fartmann, B. A. Konfortov, M. Madera, C. Vogel, S. A. Teichmann, A. Ivens, and P. H. Dear. 2003. Integrated mapping, chromosomal sequencing and sequence analysis of Cryptosporidium parvum. Genome Res. 13:1787-1799.
7. Beyer, T. V., N. V. Svezhova, N. V. Sidorenko, and S. E. Khokhlov. 2000. Cryptosporidium parvum (Coccidia, apicomplexa): some new ultrastructural observations on its endogenous development. Eur. J. Protistol. 36:151-159.
8. Bukau, B., and A. L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92:351-366.
9. Cavalier-Smith, T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
10. Cummings, L., L. Riley, L. Black, A. Souvorov, S. Resenchuk, I. Dondoshansky, and T. Tatusova. 2002. Genomic BLAST: custom-defined virtual databases for complete and unfinished genomes. FEMS Microbiol. Lett. 216:133-138.
11. Dieffenbach, C. W., and G. S. Dvecksler. 1995. PCR primer: laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
12. Diekert, K., I. P. M. de Kroon, G. Kispal, and R. Lill. 2001. Isolation and subfractionization of mitochondria from the yeast Saccharomyces cerevisiae, p. 37-51. In L. A. Pon and E. A. Schon (ed.), Methods in cell biology: mitochondria, vol. 65. Academic Press, San Diego, Calif.
13. Duby, G., M. Oufattole, and M. Boutry. 2001. Hydrophobic residues within the predicted N-terminal amphiphilic alpha-helix of a plant mitochondrial targeting presequence play a major role in in vivo import. Plant J. 27:539-549.
14. Emanuelsson, O., and G. von Heijne. 2001. Prediction of organellar targeting signals. Biochim. Biophys. Acta 1541:114-119.
15. Fayer, R., C. Speer, and J. Dubey. 1997. The general biology of Cryptosporidium, p. 1-41. In R. Fayer (ed.), Cryptosporidium and cryptosporidiosis. CRC Press, Boca Raton, Fla.
16. Felselstein, J. 2003. PHYLIP: Phylogeny inference package (version 3.6a3). Department of Genome Sciences, University of Washington, Seattle, Wash.
17. Foth, B. J., and G. I. McFadden. 2003. The apicoplast: a plastid in Plasmodium falciparum and other apicomplexan parasites. Int. Rev. Cytol. 224:57-110.
18. Foth, B. J., S. A. Ralph, C. J. Tonkin, N. S. Struck, M. Fraunholz, D. S. Roos, A. F. Cowman, and G. I. McFadden. 2003. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299:705-708.
19. Gabaldon, T., and M. A. Huynen. 2003. Reconstruction of the proto-mitochondrial metabolism. Science 301:609.
20. Gakh, O., P. Cavadini, and G. Isaya. 2002. Mitochondrial processing peptidases. Biochim. Biophys. Acta 1592:63-77.
21. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, I. T. Paulsen, K. James, J. A. Eisen, K. Rutherford, S. L. Salzberg, A. Craig, S. Kyes, M. S. Chan, V. Nene, S. J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M. W. Mather, A. B. Vaidya, D. M. Martin, A. H. Fairlamb, M. J. Fraunholz, D. S. Roos, S. A. Ralph, G. I. McFadden, L. M. Cummings, G. M. Subramanian, C. Mungall, J. C. Venter, D. J. Carucci, S. L. Hoffman, C. Newbold, R. W. Davis, C. M. Fraser, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
22. Germot, A., H. Philippe, and H. Le Guyader. 1996. Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc. Natl. Acad. Sci. USA 93:14614-14617.
23. Hager, K. M., B. Striepen, L. G. Tilney, and D. S. Roos. 1999. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112:2631-2638.
24. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
25. Karlin, S., and L. Brocchieri. 1998. Heat shock protein 70 family: multiple sequence comparisons, function, and evolution. J. Mol. Evol. 47:565-577.
26. Khramtsov, N. V., M. Tilley, D. S. Blunt, B. A. Montelone, and S. J. Upton. 1995. Cloning and analysis of a Cryptosporidium parvum gene encoding a protein with homology to cytoplasmic form Hsp70. J. Eukaryot. Microbiol. 42:416-422.
27. Kim, K., M. S. Eaton, W. Schubert, S. Wu, and J. Tang. 2001. Optimized expression of green fluorescent protein in Toxoplasma gondii using thermostable green fluorescent protein mutants. Mol. Biochem. Parasitol. 113:309-313.
28. LaGier, M. J., J. Tachezy, F. Stejskal, K. Kutisova, and J. S. Keithly. 2003. Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology 149:3519-3530.
29. Lang, B. F., M. W. Gray, and G. Burger. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33:351-397.
30. Macasev, D., E. Newbigin, J. Whelan, and T. Lithgow. 2000. How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol. 123:811-816.
31. Martin, W. 2003. Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc. Natl. Acad. Sci. USA 100:8612-8614.
32. Martin, W., and M. J. Russell. 2003. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:59-83; discussion, 83-85.
33. Melo, E. J., M. Attias, and W. De Souza. 2000. The single mitochondrion of tachyzoites of Toxoplasma gondii. J. Struct. Biol. 130:27-33.
34. Morgan, B. A., B. A. Mittman, and M. M. Smith. 1991. The highly conserved N-terminal domains of histones H3 and H4 are required for normal cell cycle progression. Mol. Cell. Biol. 11:4111-4120.
35. Morrison, H. G., A. J. Roger, T. G. Nystul, F. D. Gillin, and M. L. Sogin. 2001. Giardia lamblia expresses a proteobacterial-like DnaK homolog. Mol. Biol. Evol. 18:530-541.
36. Neupert, W. 1997. Protein import into mitochondria. Annu. Rev. Biochem. 66:863-917.
37. Palade, G. 1975. Intracellular aspects of the process of protein synthesis. Science 189:347-358.
38. Philippe, H., P. Lopez, H. Brinkmann, K. Budin, A. Germot, J. Laurent, D. Moreira, M. Müller, and H. Le Guyader. 2000. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc. R. Soc. Lond. B Biol. Sci. 267:1213-1221.
39. Prinz, T., N. Pfanner, and K. N. Truscott. 2002. Translocation of proteins into mitochondria, p. 214-239. In R. E. Dalbey and G. von Heijne (ed.), Protein targeting, transport & translocation. Academic Press, Amsterdam, The Netherlands.
40. Riordan, C. E., J. G. Ault, S. G. Langreth, and J. S. Keithly. 2003. Cryptosporidium parvum Cpn60 targets a relict organelle. Curr. Genet. 44:138-147.
41. Riordan, C. E., S. G. Langreth, L. B. Sanchez, O. Kayser, and J. S. Keithly. 1999. Preliminary evidence for a mitochondrion in Cryptosporidium parvum: phylogenetic and therapeutic implications. J. Eukaryot. Microbiol. 46:52s-55s.
42. Rost, B. 2001. Review: protein secondary structure prediction continues to rise. J. Struct. Biol. 134:204-218.
43. Scherer, P. E., U. C. Krieg, S. T. Hwang, D. Vestweber, and G. Schatz. 1990. A precursor protein partly translocated into yeast mitochondria is bound to a 70 kd mitochondrial stress protein. EMBO J. 9:4315-4322.
44. Tetley, L., S. M. Brown, V. McDonald, and G. H. Coombs. 1998. Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144:3249-3255.
45. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
46. Tovar, J., A. Fischer, and C. G. Clark. 1999. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32:1013-1021.
47. Tovar, J., G. Leon-Avila, L. B. Sánchez, R. Sutak, J. Tachezy, M. van der Giezen, M. Hernández, M. Müller, and J. M. Lucocq. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
48. Uni, S., M. Iseki, T. Maekawa, K. Moriya, and S. Takada. 1987. Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitol. Res. 74:123-132.
49. Westermann, B., and W. Neupert. 2000. Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyccs cerevisiae. Yeast 16:1421-1427.
50. Williams, B. A., R. P. Hirt, J. M. Lucocq, and T. M. Embley. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.
51. Zhu, G., and J. S. Keithly. 1997. Molecular analysis of a P-type ATPase from Cryptosporidium parvum. Mol. Biochem. Parasitol. 90:307-316.
52. Zhu, G., M. J. Marchewka, and J. S. Keithly. 2000. Cryptosporidium parvum appears to lack a plastid genome. Microbiology 146:315-321.