Functional identification of a Leishmania gene related to the peroxin 2 gene reveals common ancestry of glycosomes and peroxisomes

Molecular and Cellular Biology

Volumn 17, Issue 3, 1997, Pages 1093-1101

  Flaspohler, John A ^a,b   Rickoll, Wayne L ^c   Beverley, Stephen M ^d   Parsons, Marilyn ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF PUGET SOUND   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL ORGANELLE; ENZYME MECHANISM; GENETIC ANALYSIS; GENETIC SELECTION; GLYCOLYSIS; LEISHMANIA; MICROBODY; MUTANT; NONSENSE MUTATION; PEROXISOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STOP CODON;

EUKARYOTA; TRYPANOSOMATIDAE;

EID: 0031018416     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.3.1093     Document Type: Article

References (60)

1. Alexander, K., and M. Parsons. 1991. A phosphoglycerate kinase-like molecule localized to glycosomal microbodies: evidence that the topogenic signal is not at the C-terminus. Mol. Biochem. Parasitol. 46:1-10.
2. Allen, T. E., H. Y. Hwang, A. Jardim, R. Olafson, and B. Ullman. 1995. Cloning and expression of the hypoxanthine-guanine phosphoribosyltransferase from Leishmania donovani. Mol. Biochem. Parasitol. 73:133-143.
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Ashford, R. W., P. Desjeux, and P. deRaadt. 1996. Estimation of population at risk of infection and number of cases of leishmaniasis. Parasitol. Today 8:104-105.
5. Berteaux-Lecellier, V., M. Picard, C. Thompson-Coffe, D. Zickler, A. Panvier-Adoutte, and J.-M. Simonet. 1995. A nonmammalian homolog of the PAF1 gene (Zellweger syndrome) discovered as a gene involved in caryogamy in the fungus Podospora anserina. Cell 81:1043-1051.
6. Blattner, J., H. Dörsam, and C. E. Clayton. 1995. Function of N-terminal import signals in trypanosome microbodies. FEBS Lett. 360:310-314.
7. Blattner, J., B. Swinkels, H. Dörsam, T. Prospero, S. Subramani, and C. Clayton. 1992. Glycosome assembly in trypanosomes: Variations in the acceptable degeneracy of a COOH-terminal microbody targeting signal. J. Cell Biol. 119:1129-1136.
8. Borst, P. 1989. Peroxisome biogenesis revisited. Biochim. Biophys. Acta 1008:1-13.
9. Court, D. A., R. Kleene, W. Neupert, and R. Lill. 1996. Role of the N- and C-termini of porin in import into the outer membrane of Neurospora mitochondria. FEBS Lett. 390:73-77.
10. Cruz, A., C. M. Coburn, and S. M. Beverley. 1991. Double targeted gene replacement for creating null mutants. Proc. Natl. Acad. Sci. USA 88:7170-7174.
11. Distel, B., R. Erdmann, S. J. Gould, G. Blobel, D. I. Crane, J. M. Cregg, G. Dodt, Y. Pujiki, J. M. Goodman, W. W. Just, J. A. K. W. Kiel, W.-H. Kunau, P. B. Lazarow, G. P. Mannaerts, H. W. Moser, T. Osumi, R. A. Rachubinski, A. Roscher, S. Subramani, H. F. Tabak, T. Tsukamoto, D. Valle, I. van der Klei, P. P. Van Veldhoven, and M. Veenhuis. 1996. A unified nomenclature for peroxisome biogenesis factors. J. Cell Biol. 135:1-3.
12. Elgersma, Y., M. Van den Berg, H. F. Tabak, and B. Distel. 1993. An efficient positive selection procedure for the isolation of peroxisomal import and peroxisome assembly mutants of Saccharomyces cerevisiae. Genetics 135: 731-740.
13. Erdmann, R., M. Veenhuis, D. Mertens, and W.-H. Kunau. 1996. Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 86:5419-5423.
14. Freemont, P. S., I. M. Hanson, and J. Trowsdale. 1991. A novel cysteine-rich sequence motif. Cell 64:483-484.
15. Gatignol, A., M. Baron, and G. Tiraby. 1987. Phleomycin resistance encoded by the ble gene from transposon Tn5 as a dominant selectable marker in Saccharomyces cerevisiae. Mol. Gen. Genet. 207:342-348.
16. Gish, W., and D. J. States. 1993. Identification of protein coding regions by database similarity search. Nat. Genet. 3:266-272.
17. Gould, S. J., G. A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. Conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108:1657-1664.
18. Gould, S. J., D. McCollum, A. P. Spong, J. A. Heyman, and S. Subramani. 1992. Development of the yeast Pichia pastoris as a model organism for a genetic and molecular analysis of peroxisome assembly. Yeast 8:613-628.
19. Hajra, A. K. 1995. Glycerolipid biosynthesis in peroxisomes (microbodics). Prog. Lipid Res. 34:343-364.
20. Hannaert, V., M. Blaauw, L. Kohl, S. Allert, F. R. Opperdoes, and P. A. M. Michels. 1992. Molecular analysis of the cytosolic and glycosomal glyceral-dehyde-3-phosphate dehydrogenase in Leishmania mexicana. Mol. Biochem. Parasitol. 55:115-126.
21. Hart, D. T., and F. R. Opperdoes. 1984. The occurrence of glycosomes (microbodies) in the promastigote stage of four major Leishmania species. Mol. Biochem. Parasitol. 13:159-172.
22. Henikoff, S. 1987. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 155:156-165.
23. Heymans, H. S. A., R. B. H. Schutgens, R. Tan, H. Van den Bosch, and P. Borst. 1983. Severe plasmalogen deficiency in tissues of infants without peroxisomes (Zellweger syndrome). Nature 306:69-70.
24. Iovannisci, D. M., D. Goebel, K. Allen, K. Kaur, and B. Ullman. 1984. Genetic analysis of adenine metabolism in Leishmania donovani promastigotes. Evidence for diploidy at the adenine phosphoribosyltransferase locus. J. Biol. Chem. 259:14617-14623.
25. Iovannisci, D. M., and B. Ullman. 1984. Characterization of a mutant Leishmania donovani deficient in adenosine kinase activity. Mol. Biochem. Parasitol. 12:139-151.
26. Kapler, G. M., C. M. Coburn, and S. M. Beverly. 1990. Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression. Mol. Cell. Biol. 10: 1084-1094.
27. King, D. L., and S. J. Turco. 1988. A ricin agglutinin-resistant clone of Leishmania donovani deficient in lipophosphoglycan. Mol. Biochem. Parasitol. 28:285-293.
28. Kunau, W. H., V. Dommes, and H. Schulz. 1995. β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog. Lipid Res. 34:267-342.
29. LeBowitz, J. H., C. M. Coburn, D. McMahon-Pratt, and S. M. Beverley. 1990. Development of a stable Leishmania expression vector and application to the study of parasite surface antigen genes. Proc. Natl. Acad. Sci. USA 87:9736-9740.
30. Mallinson, D. J., and G. H. Coombs. 1989. Biochemical characteristics of the metacyclic forms of Leishmania major and L. mexicana mexicana. Parasitology 98:7-15.
31. Michels, P. A. 1988. Compartmentation of glycolysis in trypanosomes: a potential target for new trypanocidal drugs. Biol. Cell 64:157-164.
32. Opperdoes, F. R. 1984. Localization of the initial steps in alkoxyphospholipid biosynthesis in glycosomes (microbodies) of Trypanosoma brucei. FEBS Lett. 169:35-39.
33. Opperdoes, F. R. 1987. Compartmentation of carbohydrate metabolism in trypanosomes. Annu. Rev. Microbiol. 41:128-151.
34. Opperdoes, F. R., and P. A. M. Michels. 1993. The glycosomes of the Kinetoplastida. Biochimie 75:231-234.
35. Osinga, K. A., B. W. Swinkels, W. C. Gibson, P. Borst, G. H. Veeneman, J. H. Van Boom, P. A. M. Michels, and F. R. Opperdoes. 1985. Topogenesis of microbody enzymes: a sequence comparison of the genes for the glycosomal (microbody) and cytosolic phosphoglycerate kinases of Trypanosoma brucei. EMBO J. 4:3811-3817.
36. Parker, H. L., T. Hill, K. Alexander, N. B. Murphy, W. R. Fish, and M. Parsons. 1995. Three genes and two isozymes: gene conversion and the compartmentalization and expression of the phosphoglycerate kinases of Trypanosoma (Nannomonas) congolense. Mol. Biochem. Parasitol. 69:269-279.
37. Parsons, M., and T. Hill. 1989. Elevated phosphoglycerate kinase mRNA but not protein in monomorphic Trypanosoma brucei: implications for stage-regulation and post-transcriptional control. Mol. Biochem. Parasitol. 33:215-228.
38. Parsons, M., and B. Nielsen. 1990. Trypanosoma brucei: two-dimensional gel analysis of the major glycosomal proteins during the life cycle. Exp. Parasitol. 70:276-285.
39. Patarca, R., and M. A. Fletcher. 1992. Ring finger in the peroxisome assembly factor-1. FEBS Lett. 312:1-2.
40. Purdue, P. E., and P. B. Lazarow. 1994. Peroxisomal biogenesis: multiple pathways of protein import. J. Biol. Chem. 269:30065-30068.
41. Ryan, K. A., S. Dasgupta, and S. M. Beverley. 1993. Shuttle cosmid vectors for the trypanosomatid parasite Leishmania. Gene 131:145-150.
42. Sato, T. 1968. A modified method for lead staining of thin sections. J. Electron Microsc. 17:158-159.
43. Schulz, I. 1990. Permeabilizing cells: some methods and applications for the study of intracellular processes. Methods Enzymol. 192:280-300.
44. Shimozawa, N., T. Tsukamoto, Y. Suzuki, T. Orii, Y. Shirayosni, T. Mori, and Y. Fujiki. 1992. A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science 255:1132-1134.
45. Skeiky, Y. A. W., D. R. Benson, M. Parsons, K. B. Elkon, and S. G. Reed. 1992. Cloning and expression of Trypanosoma cruzi ribosomal protein P0 and epitope analysis of anti-P0 autoantibodies in Chagas' disease patients. J. Exp. Med. 176:201-211.
46. Sommer, J. M., P. Bradley, C. C. Wang, and P. J. Johnson. 1996. Biogenesis of specialized organelles: glycosomes and hydrogenosomes, p. 159-180. In D. F. Smith and M. Parsons (ed.), Molecular biology of parasitic protozoa. IRL Press, Oxford, England.
47. Sommer, J. M., Q.-L. Cheng, G.-A. Keller, and C. C. Wang. 1992. In vivo import of firefly luciferase into the glycosomes of Trypanosoma brucei and mutational analysis of the C-terminal targeting signal. Mol. Biol. Cell 3:749-759.
48. Sommer, J. M., T. T. Nguyen, and C. C. Wang. 1994. Phosphoenolpyruvate carhoxykinase ot Trypanosoma brucei is targeted to the glycosomes by a C-terminal sequence. FEBS Lett. 350:125-129.
49. Sommer, J. M., G. Peterson, G.-A. Keller, M. Parsons, and C. C. Wang. 1993. The C-terminal tripeptide of glycosomal phosphoglycerate kinase is both necessary and sufficient for import into the glycosomes of Trypanosoma brucei. FEBS Lett. 316:53-58.
50. Sommer, J. M., and C. C. Wang. 1994. Targeting proteins to the glycosomes of African trypanosomes. Annu. Rev. Microbiol. 48:105-138.
51. Swinkels, B. W., A. Loiseau, F. R. Opperdoes, and P. Borst. 1992. A phosphoglycerate kinase-related gene conserved between Trypanosoma brucei and Crithidia fasciculata. Mol. Biochem. Parasitol. 50:69-78.
52. Szilard, R. K., V. I. Titorenko, M. Veenhuis, and R. A. Rachubinski. 1995. Pay32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocation machinery. J. Cell Biol. 131:1453-1469.
53. Tan, X., V. Titorenko, I. J. Van der Klei, G. J. Sulter, P. Haima, H. R. Waterham, M. Evers, W. Harder, M. Veenhuis, and J. Cregg. 1995. Characterization of peroxisome-deficient mutants of Hansenula polymorpha. Curr. Genet. 28:248-257.
54. Tsukamoto, T., S. Miura, and Y. Fujiki. 1991. Restoration by a 35K membrane protein of peroxisome assembly in a peroxisome-deficient mammalian cell mutant. Nature 350:77-81.
55. Tsukamoto, T., N. Shimozawa, and Y. Fujiki. 1994. Peroxisome assembly factor 1: nonsense mutation in a peroxisome-deficient Chinese hamster ovary cell mutant and deletion analysis. Mol. Cell. Biol. 14:5458-5465.
56. Turco, S. J. 1995. Surface constituents of kinetoplastid parasites, p. 177-202. In J. J. Marr and M. Muller (ed.). Biochemistry and molecular biology of parasites. Academic Press, San Diego, Calif.
57. Turco, S. J., and A. Descoteaux. 1992. The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46:65-94.
58. Van Der Leij, I., M. Van den Berg, R. Boot, M. Franse, B. Distel, and H. F. Tabak. 1992. Isolation of peroxisome assembly mutants from Saccharomyces cerevisiae with different morphologies using a novel positive selection procedure. J. Cell Biol. 119:153-162.
59. Waterham, H. R., Y. De Vries, K. A. Russell, W. Q. Xie, M. Veenhuis, and J. M. Cregg. 1996. The Pichia pastoris PER6 gene product is a peroxisomal integral membrane protein essential for peroxisome biogenesis and has sequence similarity to the Zellweger syndrome protein PAF-1. Mol. Cell. Biol. 16:2527-2536.
60. -) mutants of Hansenula polymorpha. Yeast 8:961-972.