Hsp60 is targeted to a cryptic mitochondrion-derived organelle ('Crypton') in the microaerophilic protozoan parasite Entamoeba histolytica

Molecular and Cellular Biology

Volumn 19, Issue 3, 1999, Pages 2198-2205

  Mai, Zhiming ^a   Ghosh, Sudip ^a   Frisardi, Marta ^a   Rosenthal, Ben ^a   Rogers, Rick ^a   Samuelson, John ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; CHAPERONIN; COMPLEMENTARY DNA; FERREDOXIN; HEAT SHOCK PROTEIN 60;

ARTICLE; BACTERIUM MUTANT; CELL ORGANELLE; CELLULAR DISTRIBUTION; CYTOSOL; ENTAMOEBA HISTOLYTICA; ESCHERICHIA COLI; GENE AMPLIFICATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN TARGETING;

BACTERIA (MICROORGANISMS); ENTAMOEBA HISTOLYTICA; ESCHERICHIA COLI; PROTOZOA;

EID: 0033020661     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.3.2198     Document Type: Article

References (59)

1. Alam, R., N. Hachiya, M. Sakaguchi, S. Kawabata, S. Iwanaga, M. Kitajima, K. Mihara, and T. Omura. 1994. cDNA cloning and characterization of mitochondrial import stimulation factor (MSF) purified from rat liver cytosol. J. Biochem. 116:416-425.
2. 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.
3. Bradley, P. J., C. J. Lahti, E. Plumper, and P. J. Johnson. 1997. Targeting and translocation of proteins into the hydrogenosome of the protist Trichomonas: similarities with mitochondrial protein import. EMBO J. 16: 3484-3493.
4. Bringaud, F., S. Peyrucaud, D. Baltz, C. Giroud, L. Simpson, and T. Baltz. 1995. Molecular characterization of the mitochondrial heat shock protein 60 gene from Trypanosoma brucei. Mol. Biochem. Parasitol. 74:119-123.
5. Bui, E. T. N., P. J. Bradley, and P. J. Johnson. 1996. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. USA 93:9651-9656.
6. Chen, L. B. 1989. Fluorescent labeling of mitochondria. Methods Cell Biol. 29:103-123.
7. Clark, C. G., and A. J. Roger. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92:6518-6521.
8. Claros, M. G., and P. Vincens. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241:779-786.
9. De la Vega, H., C. A. Specht, C. E. Semino, P. W. Robbins, D. Eichinger, D. Caplivski, S. Ghosh, and J. Samuelson. 1996. Cloning and expression of chitinases of Entamoebae. Mol. Biochem. Parasitol. 85:139-147.
10. Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
11. Frohman, M. A., M. K. Dush, and G. R. Martin. 1988. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85:8998-9002.
12. Ghosh, S. K., A. Lohia, A. Kumar, and J. Samuelson. 1996. Overexpression of P-glycoprotein gene 1 by transfected Entamoeba histolytica confers emetine-resistance. Mol. Biochem. Parasitol. 82:257-260.
13. Ghosh, S. K., J. Samuelson, and A. Lohia. Unpublished data.
14. Gray, M. W. 1989. The evolutionary origins of organelles. Trends Genet. 5:294-299.
15. Grivell, L. A. 1995. Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit. Rev. Biochem. Mol. Biol. 30:121-164.
16. Gupta, R. S. 1995. Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15:1-11.
17. Hartl, F. U. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-580.
18. Hashimoto, T., L. B. Sanchez, T. Shirakura, M. Muller, and M. Hasegawa. 1998. Secondary loss of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valy1-tRNA synthetase phylogeny. Proc. Natl. Acad. Sci. USA 95:6860-6865.
19. Hemmingsen, S. M., C. Woolford, S. M. van der Vies, K. Tilly, D. T. Dennis, C. P. Georgopoulos, R. W. Hendrix, and R. J. Ellis. 1988. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333: 330-334.
20. Horner, D. S., R. P. Hirt, S. Kilvington, D. Lloyd, and T. M. Embley. 1996. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. Lond. Ser. B 263:1053-1059.
21. Hrdy, I., and M. Muller. 1995. Primary structure and eubacterial relationship of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote, Trichomonas vaginalis. J. Mol. Evol. 41:388-396.
22. Huber, M., L. Garfinkel, C. Gitler, D. Mirelman, M. Revel, and S. Rozenblatt. 1988. Nucleotide sequence analysis of an Entamoeba histolytica ferredoxin gene. Mol. Biochem. Parasitol. 31:27-34.
23. Johnson, P. J. 1993. Metronidazole and drug resistance. Parasitol. Today 9:183-186.
24. Johnson, R. B., K. Fearon, T. Mason, and S. Jindal. 1989. Cloning and characterization of the yeast chaperonin HSP60 gene. Gene 84:295-302.
25. Kohler, S., C. F. Delwiche, P. W. Denny, L. G. Tilney, P. Webster, R. J. Wilson, J. D. Palmer, and D. S. Roos. 1997. A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485-1489.
26. +-dependent alcohol dehydrogenase gene of Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 85:1782-1786.
27. Leipe, D. D., J. H. Gunderson, T. A. Nerad, and M. L. Sogin. 1993. Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol. Biochem. Parasitol. 59:41-48.
28. Leippe, M., E. Tannich, R. Nickel, R. D. Horstmann, and H. J. Muller-Eberhard. 1992. Primary structure of the pore-forming peptide of pathogenic Entamoeba histolytica. EMBO J. 11:3501-3506.
29. Martinez-Palomo, A. 1982. Cell biology, p. 5-59. In K. N. Brown (ed.), The biology of Entamoeba histolytica. John Wiley, Research Studies Press, New York, N.Y.
30. McLennan, N. F., A. S. Girshovich, N. M. Lissin, Y. Charters, and M. Masters. 1993. The strongly conserved carboxyl-terminus glycine-methionine motif of the Escherichia coli GroEL chaperonin is dispensable. Mol. Microbiol. 71:49-58.
31. Muller, M. 1993. The hydrogenosome. J. Gen. Microbiol. 139:2879-2889.
32. O'Farrell, P. Z., H. M. Goodman, and P. H. O'Farrell. 1977. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12:1133-1141.
33. Orozco, E., R. Gharaibeh, A. M. Riveron, D. M. Delgadillo, M. Mercado, T. Sanchez, E. Gomez Conde, M. A. Vargas, and R. Lopez-Revilla. 1997. A novel cytoplasmic structure containing DNA networks in Entamoeba histolytica trophozoites. Mol. Gen. Genet. 254:250-257.
34. Ortner, S., B. Plaimauer, M. Binder, G. Wiedermann, O. Scheiner, and M. Duchene. 1992. Humoral immune response against a 70-kilodalton heat shock protein of Entamoeba histolytica in a group of patients with invasive amoebiasis. Mol. Biochem. Parasitol. 54:175-183.
35. Ravdin, J. I. 1995. Amebiasis. State-of-the-art clinical article. Clin. Infect. Dis. 20:1453-1464.
36. Reers, M., S. T. Smiley, C. Mottola-Hartshorn, A. Chen, M. Lin, and L. B. Chen. 1995. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260:406-417.
37. Reeves, R. E. 1984. Metabolism of Entamoeba histolytica Schaudinn, 1903. Adv. Parasitol. 23:105-142.
38. Rey-Ladino, J. A., P. B. Joshi, B. Singh, R. Gupta, and N. E. Reiner. 1997. Leishmania major: molecular cloning, sequencing, and expression of the heat shock protein 60 gene reveals unique carboxyl terminal peptide sequences. Exp. Parasitol. 85:249-263.
39. Rodriguez, M. A., R. M. Garcia-Perez, L. Mendoza, T. Sanchez, N. Guillen, and E. Orozco. 1998. The pyruvate:ferredoxin oxidoreductase is located in the plasma membrane and in a cytoplasmic structure in Entamoeba. Microb. Pathog. 25:1-10.
40. Roger, A. J., C. G. Clark, and W. F. Doolittle. 1996. A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc. Natl. Acad. Sci. USA 93:14618-14622.
41. Roger, A. J., S. G. Svard, J. Tovar, C. G. Clark, M. W. Smith, F. D. Gillen, and M. L. Sogin. 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. USA 95:229-234.
42. Rosenthal, B., Z. Mai, D. Caplivski, S. Ghosh, H. de la Vega, T. Graf, and J. Samuelson. 1997. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol. 179:3736-3745.
43. Ryan, K. R., and R. E. Jensen. 1995. Protein translocation across mitochondrial membranes: what a long strange trip it is. Cell 83:517-519.
44. Samarawickrema, N. A., D. M. Brown, J. A. Upcroft, N. Thammapalerd, and P. Upcroft. 1997. Involvement of superoxide dismutase and pyruvate:ferredoxin oxidoreductase in mechanisms of metronidazole resistance in Entamoeba histolytica. J. Antimicrob. Chemother. 40:833-840.
45. Schatz, G. 1987. Signals guiding proteins to their correct locations in mitochondria. Eur. J. Biochem. 165:1-6.
46. Singh, B., H. V. Patel, R. G. Ridley, K. B. Freeman, and R. S. Gupta. 1990. Mitochondrial import of the human chaperonin (HSP60) protein. Biochem. Biophys. Res. Commun. 169:391-396.
47. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
48. Smith, M. W., D.-F. Feng, and R. F. Doolittle. 1992. Evolution by acquisition: the case for horizontal gene transfers. Trends Biochem. Sci. 17:489-493.
49. Soltys, B. J., and R. S. Gupta. 1994. Presence and cellular distribution of a 60-kDa protein related to mitochondrial HSP60 in Giardia lamblia. J. Parasitol. 80:580-590.
50. Sullivan, M. A., C. L. Olson, A. G. Winquist, and D. M. Engman. 1994. Expression and localization of Trypanosoma cruzi hsp60. Mol. Biochem. Parasitol. 68:197-208.
51. Syin, C., and N. D. Goldman. 1996. Cloning of a Plasmodium falciparum gene related to the human 60-kDa heat shock protein. Mol. Biochem. Parasitol. 79:13-19.
52. Tsugeki, R., H. Mori, and M. Nishimura. 1992. Purification, cDNA cloning and Northern-blot analysis of mitochondrial chaperonin 60 from pumpkin cotyledons. Eur. J. Biochem. 209:453-458.
53. Tyler, K. M., K. R. Matthews, and K. Gull. 1997. The bloodstream differentiation-division of Trypanosoma brucei studied using mitochondrial markers. Proc. R. Soc. Lond. Ser. B. 264:1481-1490.
54. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
55. Yang, D., Y. Oyaizu, H. Oyaizu, G. J. Olsen, and C. R. Woese. 1985. Mitochondrial origins. Proc. Natl. Acad. Sci. USA 82:4443-4447.
56. Yang, W., E. Li, T. Kairong, and S. L. Stanley, Jr. 1994. Entamoeba histolytica has an alcohol dehydrogenase homologous to the multifunctional adhE gene product of Escherichia coli. Mol. Biochem. Parasitol. 64:253-260.
57. Yasuhira, S., and L. Simpson. 1990. Phylogenetic affinity of mitochondria of Euglena gracilis and kinetoplastids using cytochrome oxidase 1 and hsp60. J. Mol. Evol. 44:341-347.
58. Yoshida, H., H. Yanagi, and T. Yura. 1995. Cloning and characterization of the mitochondrial HSP60-encoding gene of Schizosaccharomyces pombe. Gene 167:163-166.
59. Yu, Y., and J. Samuelson. 1994. Primary structure of an Entamoeba histolytica nicotinamide nucleotide transhydrogenase. Mol. Biochem. Parasitol. 68:323-328.