Mutation of an unusual mitochondrial targeting sequence of SODB2 produces multiple targeting fates in Toxoplasma gondii

Journal of Cell Science

Volumn 116, Issue 22, 2003, Pages 4675-4685

  Brydges, Susannah D ^a   Carruthers, Vern B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Apicomplexa; Apicoplast; Mitochondrion; Presequence; Targeting; Toxoplasma gondii

Indexed keywords

MITOCHONDRIAL ENZYME; SIGNAL PEPTIDE; SUPEROXIDE DISMUTASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; APICOMPLEXA; APICOPLAST; CELL FATE; CELL ORGANELLE; CELLULAR DISTRIBUTION; CHLOROPLAST; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; FEMALE; GENE MUTATION; HYDROPHOBICITY; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEAR IMPORT; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SEQUENCE HOMOLOGY; TOXOPLASMA GONDII;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CLONING, MOLECULAR; ENDOPLASMIC RETICULUM; EPIDERMIS; EXPRESSED SEQUENCE TAGS; FIBROBLASTS; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; ORGANELLES; PROTEIN BINDING; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUPEROXIDE DISMUTASE; TOXOPLASMA;

APICOMPLEXA; MAMMALIA; PROTOZOA; TOXOPLASMA GONDII;

EID: 0344897610     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00750     Document Type: Review

References (56)

1. Abe, Y., Shodai, T., Muto, T., Mihara, K., Torii, H., Nishikawa, S., Endo, T. and Kohda, D. (2000). Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100, 551-560.
2. Balzan, R., Bannister, W. H., Hunter, G. J. and Bannister, J. V. (1995). Escherichia coli iron superoxide dismutase targeted to the mitochondria of yeast cells protects the cells against oxidative stress. Proc. Natl. Acad. Sci. USA 92, 4219-4223.
3. Bannister, J. V., Bannister, W. H. and Rotilio, G. (1987). Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit. Rev. Biochem. 22, 111-180.
4. Beauchamp, C. and Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287.
5. Becuwe, P., Gratepanche, S., Fourmaux, M. N., van Beeumen, J., Samyn, B., Mercereau-Puijalon, O., Touzel, J. P., Slomianny, C., Camus, D. and Dive, D. (1996). Characterization of iron-dependent endogenous superoxide dismutase of Plasmodium falciparum. Mol. Biochem. Parasitol. 76, 125-134.
6. Beyer, W., Imlay, J. and Fridovich, I. (1991). Superoxide dismutases. Prog. Nucleic Acid Res. Mol. Biol. 40, 221-253.
7. Bhagwat, S. V., Biswas, G., Anandatheerthavarada, H. K., Addya, S., Pandak, W. and Avadhani, N. G. (1999). Dual targeting property of the N-terminal signal sequence of P4501A1. Targeting of heterologous proteins to endoplasmic reticulum and mitochondria. J. Biol. Chem. 274, 24014-24022.
8. Brix, J., Dietmeier, K. and Pfanner, N. (1997). Differential recognition of preproteins by the purified cytosolic domains of the mitochondrial import receptors Tom20, Tom22, and Tom70. J. Biol. Chem. 272, 20730-20735.
9. Carlioz, A. and Touati, D. (1986). Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 5, 623-630.
10. Fridovich, I. (1995). Superoxide radical and superoxide dismutases. Annu. Rev. Biochem. 64, 97-112.
11. 2-), superoxide dismutases, and related matters. J. Biol. Chem. 272, 18515-18517.
12. Hager, K. M., Striepen, B., Tilney, L. G. and Roos, D. S. (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.
13. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
14. Haverkos, H. W. (1987). Assessment of therapy for Toxoplasma encephalitis. The TE Study Group. Am. J. Med. 82, 907-914.
15. 2-terminal targeting motifs direct dual specificity A-kinase- anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J. Cell Biol. 145, 951-959.
16. Huang, P., Feng, L., Oldham, E. A., Keating, M. J. and Plunkett, W. (2000). Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407, 390-395.
17. Ismail, S. O., Paramchuk, W., Skeiky, Y. A., Reed, S. G., Bhatia, A. and Gedamu, L. (1997). Molecular cloning and characterization of two iron superoxide dismutase cDNAs from Trypanosoma cruzi. Mol. Biochem. Parasitol. 86, 187-197.
18. Jelenska, J., Crawford, M. J., Harb, O. S., Zuther, E., Haselkorn, R., Roos, D. S. and Gornicki, P, (2001). Subcellular localization of acetyl-CoA carboxylase in the apicomplexan parasite Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 98, 2723-2728.
19. Jensen, R. E. and Johnson, A. E. (1999). Protein translocation: is Hsp70 pulling my chain? Curr. Biol. 9, R779-782.
20. Kanematsu, S. and Asada, K. (1979). Ferric and manganic superoxide dismutases in Euglena gracilis. Arch. Biochem. Biophys. 195, 535-545.
21. Keele, B. B., Jr, McCord, J. M. and Fridovich, I. (1970). Superoxide dismutase from Escherichia coli B. A new manganese- containing enzyme. J. Biol. Chem. 245, 6176-6181.
22. Kohler, S., Delwiche, C. F., Denny, P. W., Tilney, L. G., Webster, P., Wilson, R. J., Palmer, J. D. and Roos, D. S. (1997). A plastid of probable green algal origin in apicomplexan parasites. Science 275, 1485-1489.
23. LeTrant, N., Meshnick, S., Kitchener, K., Eaton, J. and Cerami, A. (1983). Iron-containing superoxide dismutase from Crithidia fasciculata. J. Biol. Chem. 258, 125-130.
24. Luft, B. J. and Remington, J. S. (1988). AIDS commentary. Toxoplasmic encephalitis. J. Infec. Dis. 157, 1-6.
25. Luft, B. J. and Remington, J. S. (1992). Toxoplasmic encephalitis in AIDS. Clin. Infec. Dis. 15, 211-222.
26. Ma, Y. and Taylor, S. (2002). A 15-residue bifunctional element in D-AKAP1 is required for both endoplasmic reticulum and mitochondrial targeting. J. Biol. Chem. 277, 27328-27336.
27. McCord, J. M. and Fridovich, I. (1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244, 6049-6055.
28. McFadden, G. I., Reith, M. E., Munholland, J. and Lang-Unnasch, N. (1996). Plastid in human parasites. Nature 381, 482.
29. Melo, E. J., Attias, M. and de Souza, W. (2000). The single mitochondrion of tachyzoites of Toxoplasma gondii. J. Struct. Biol. 130, 27-33.
30. Meshnick, S. R., Kitchener, K. R. and Trang, N. L. (1985). Trypanosomatid iron-superoxide dismutase inhibitors. Selectivity and mechanism of N1,N6-bis (2,3-dihydroxybenzoyl)-1,6-diaminohexane. Biochem. Pharmacol. 34, 3147-3152.
31. Neupert, W. (1997). Protein import into mitochondria. Annu. Rev. Biochem. 66, 863-917.
32. Noren, F., Moestrup, O. and Rehnstam-Holm, A.-S. (1999). Parvilucifera infectans Noren et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Vet. Parasitol. 35, 233-254.
33. Odberg-Ferragut, C., Renault, J. P., Viscogliosi, E., Toursel, C., Briche, I., Engels, A., Lepage, G., Morgenstern-Badarau, I., Camus, D., Tomavo, S. et al. (2000). Molecular cloning, expression analysis and iron metal cofactor characterisation of a superoxide dismutase from Toxoplasma gondii. Mol. Biochem. Parasitol. 106, 121-129.
34. Paramchuk, W. J., Ismail, S. O., Bhatia, A. and Gedamu, L. (1997). Cloning, characterization and overexpression of two iron superoxide dismutase cDNAs from Leishmania chagasi: role in pathogenesis. Mol. Biochem. Parasitol. 90, 203-221.
35. Pfanner, N. (2000). Protein sorting: recognizing mitochondrial presequences. Curr. Biol. 10, R412-415.
36. Poot, M., Zhang, Y. Z., Kramer, J. A., Wells, K. S., Jones, L. J., Hanzel, D. K., Lugade, A. G., Singer, V. L. and Haugland, R. P. (1996). Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 44, 1363-1372.
37. Roise, D. and Schatz, G. (1988). Mitochondrial presequences. J. Biol. Chem. 263, 4509-4511.
38. Roos, D. S., Crawford, M. J., Donald, R. G., Kissinger, J. C., Klimczak, L. J. and Striepen, B. (1999). Origin, targeting, and function of the apicomplexan plastid. Curr. Opin. Microbiol. 2, 426-432.
39. Salin, M. L. and Bridges, S. M. (1980). Isolation and characterization of an iron-containing superoxide dismutase from a eucaryote, Brassica campestris. Arch. Biochem. Biophys. 201, 369-374.
40. Schatz, G. and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1526.
41. Schatz, G. (1997). Just follow the acid chain. Nature 388, 121-122.
42. Schott, E. J. and Vasta, G. R. (2003). The PmSOD1 gene of the protistan parasite Perkinsus marinus complements the sod2Delta mutant of Saccharomyces cerevisiae, and directs an iron superoxide dismutase to mitochondria. Mol. Biochem. Parasitol. 126, 81-92.
43. Seeber, F., Ferguson, D. J. and Gross, U. (1998). Toxoplasma gondii: a paraformaldehyde-insensitive diaphorase activity acts as a specific histochemical marker for the single mitochondrion. Exp. Parasitol. 89, 137-139.
44. Sinai, A., Webster, J. P. and Joiner, K. A. (1997). Association of host cell mitochondria and endoplasmic reticulum with the Toxoplasma gondii parasitophorous vacuole membrane - a high affinity interaction. J. Cell Sci. 110, 2117-2128.
45. Striepen, B., Crawford, M. J., Shaw, M. K., Tilney, L. G., Seeber, F. and Roos, D. S. (2000). The plastid of Toxoplasma gondii is divided by association with the centrosomes. J. Cell Biol. 151, 1423-1434.
46. Tannich, E., Bruchhaus, I., Walter, R. D. and Horstmann, R. D. (1991). Pathogenic and nonpathogenic Entamoeba histolytica: identification and molecular cloning of an iron-containing superoxide dismutase. Mol. Biochem. Parasitol. 49, 61-71.
47. Toursel, C., Dzierszinski, F., Bernigaud, A., Mortuaire, M. and Tomavo, S. (2000). Molecular cloning, organellar targeting and developmental expression of mitochondrial chaperone HSP60 in Toxoplasma gondii. Mol. Biochem. Parasitol. 111, 319-332.
48. Ukeda, H., Maeda, S., Ishii, T. and Sawamura, M. (1997). Spectrophotometric assay for superoxide dismutase based on tetrazolium salt 3′-1-(phenylamino)-carbonyl-3, 4-tetrazolium]-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate reduction by xanthine-xanthine oxidase. Anal. Biochem. 251, 206-209.
49. van Loon, A. P., Pesold-Hurt, B. and Schatz, G. (1986). A yeast mutant lacking mitochondrial manganese-superoxide dismutase is hypersensitive to oxygen. Proc. Natl. Acad. Sci. USA 83, 3820-3824.
50. Viscogliosi, E., Delgado-Viscogliosi, P., Gerbod, D., Dauchez, M., Gratepanche, S., Alix, A. J. and Dive, D. (1998). Cloning and expression of an iron-containing superoxide dismutase in the parasitic protist, Trichomonas vaginalis. FEMS Microbiol. Lett. 161, 115-123.
51. von Heijne, G., Steppuhn, J. and Herrmann, R. G. (1999). Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180, 535-545.
52. Voos, W., Martin, H., Krimmer, T. and Pfanner, N. (1999). Mechanisms of protein translocation into mitochondria. Biochim. Biophys. Acta 1422, 235-254.
53. Waller, R. F., Keeling, P. J., Donald, R. G. K., Striepen, B., Handman, E., Lang-Unnasch, N., Cowman, A. F., Besra, G. S., Roos, D. S. and McFadden, G. I. (1998). Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Nat. Acad. Sci. USA 95, 12352-12357.
54. Waller, R. E., Reed, M. B., Cowman, A. F. and McFadden, G. I. (2000). Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19, 1794-1802.
55. Wan, K. L., Carruthers, V. B., Sibley, L. D. and Ajioka, J. W. (1997). Molecular characterization of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol. Biochem. Parasitol. 84, 203-214.
56. Yost, F. J., Jr and Fridovich, I. (1973). An iron-containing superoxide dismutase from Escherichia coli. J. Biol. Chem. 248, 4905-4908.