Home LiteratureArticle Details
PMID: 1831458 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes.

The Journal of cell biology ·Vol. 114 ·No. 5 ·1991-09-00 ·Pages 893-904

Keller GA, Krisans S, Gould SJ, Sommer JM, Wang CC, Schliebs W, Kunau W, Brody S, Subramani S

Abstract

Peroxisomes, glyoxysomes, glycosomes, and hydrogenosomes have each been classified as microbodies, i.e., subcellular organelles with an electron-dense matrix that is bound by a single membrane. We investigated whether these organelles might share a common evolutionary origin by asking if targeting signals used for translocation of proteins into these microbodies are related. A peroxisomal targeting signal (PTS) consisting of the COOH-terminal tripeptide serine-lysine-leucine-COOH has been identified in a number of peroxisomal proteins (Gould, S.J., G.-A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. J. Cell Biol. 108:1657-1664). Antibodies raised to a peptide ending in this sequence (SKL-COOH) recognize a number of peroxisomal proteins. Immunocryoelectron microscopy experiments using this anti-SKL antibody revealed the presence of proteins containing the PTS within glyoxysomes of cells from Pichia pastoris, germinating castor bean seeds, and Neurospora crassa, as well as within the glycosomes of Trypanosoma brucei. Western blot analysis of purified organelle fractions revealed the presence of many proteins containing this PTS in both glyoxysomes and glycosomes. These results indicate that at least one of the signals, and therefore the mechanism, for protein translocation into peroxisomes, glyoxysomes, and glycosomes has been conserved, lending support to a common evolutionary origin for these microbodies. Hydrogenosomes, the fourth type of microbody, did not contain proteins that cross-reacted with the anti-PTS antibody, suggesting that this organelle is unrelated to microbodies.

MeSH Terms
Amino Acid Sequence Animals Biological Evolution Biological Transport Blotting, Western Cell Compartmentation Microbodies/metabolism Microscopy, Electron Molecular Sequence Data Molecular Weight Neurospora crassa Organelles/metabolism Peptides/chemistry Plants, Toxic Proteins/metabolism Ricinus Trypanosoma brucei brucei/analysis Yeasts
Chemicals
Peptides Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Keller G A
Department of Preclinical Pharmacology, Genentech Inc., South San Francisco, California 94080.
Krisans S
Gould S J
Sommer J M
Wang C C
Schliebs W
Kunau W
Brody S
Subramani S
References (40)
40 references, click to expand
  1. Biogenesis of peroxisomes.
    Annu Rev Cell Biol. 1985;1:489-530 PMID: 3916321
  2. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies.
    Ann N Y Acad Sci. 1987;503:55-71 PMID: 3304084
  3. The ERD2 gene determines the specificity of the luminal ER protein retention system.
    Cell. 1990 Jun 29;61(7):1359-63 PMID: 2194671
  4. Peroxisomal protein import is conserved between yeast, plants, insects and mammals.
    EMBO J. 1990 Jan;9(1):85-90 PMID: 2104803
  5. Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6097-101 PMID: 1696716
  6. Characterization of an in vitro assay for import of 3-phosphoglycerate kinase into the glycosomes of Trypanosoma brucei.
    Mol Cell Biol. 1990 Sep;10(9):4545-54 PMID: 2388617
  7. Two types of microbodies in Neurospora crassa.
    Ann N Y Acad Sci. 1982;386:269-84 PMID: 6212014
  8. Fine structure and cytochemistry of the hydrogenosome of Tritrichomonas foetus.
    J Protozool. 1983 May;30(2):422-5 PMID: 6631782
  9. A technique for ultracryotomy of cell suspensions and tissues.
    J Cell Biol. 1973 May;57(2):551-65 PMID: 4121290
  10. Cytochemical and developmental changes in microbodies (glyoxysomes) and related organelles of castor bean endosperm.
    J Cell Biol. 1970 Sep;46(3):435-54 PMID: 4121486
  11. Proteinaceous hexagonal inclusions in hyphae of Whetzelinia sclerotiorum and Neurospora crassa.
    Can J Microbiol. 1974 Jul;20(7):1029-35 PMID: 4366209
  12. Circular DNA and cardiolipin in hydrogenosomes, microbody-like organelles of trichomonads.
    Folia Parasitol (Praha). 1976;23(1):33-7 PMID: 950181
  13. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  14. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  15. Association of the glyoxylate cycle enzymes in a novel subcellular particle from castor bean endosperm.
    Biochem Biophys Res Commun. 1967 May 25;27(4):462-9 PMID: 6052476
  16. Glyoxysomal Malate Synthase of Cucumber: Molecular Cloning of a cDNA and Regulation of Enzyme Synthesis during Germination.
    Plant Physiol. 1986 Jul;81(3):762-7 PMID: 16664899
  17. Glycoproteins in the matrix of glyoxysomes in endosperm of castor bean seedlings.
    Plant Physiol. 1986 Apr;80(4):950-5 PMID: 16664747
  18. Microbodies (Glyoxysomes and Peroxisomes) in Cucumber Cotyledons: Correlative Biochemical and Ultrastructural Study in Light- and Dark-grown Seedlings.
    Plant Physiol. 1971 Oct;48(4):461-75 PMID: 16657820
  19. The establishment of various trichomonads of animals and man in axenic cultures.
    J Parasitol. 1957 Aug;43(4):488-90 PMID: 13463700
  20. Recognition of a peroxisomal tripeptide entry signal by the glycosomes of Trypanosoma brucei.
    Mol Biochem Parasitol. 1991 Apr;45(2):261-4 PMID: 2038359
  21. A conserved tripeptide sorts proteins to peroxisomes.
    J Cell Biol. 1989 May;108(5):1657-64 PMID: 2654139
  22. cDNA cloning and primary structure determination of the peroxisomal trifunctional enzyme hydratase-dehydrogenase-epimerase from the yeast Candida tropicalis pK233.
    Gene. 1988 Sep 30;69(2):171-80 PMID: 3267241
  23. Acyl-CoA oxidase contains two targeting sequences each of which can mediate protein import into peroxisomes.
    EMBO J. 1988 Apr;7(4):1167-73 PMID: 3402435
  24. The topogenic signal of the glycosomal (microbody) phosphoglycerate kinase of Crithidia fasciculata resides in a carboxy-terminal extension.
    EMBO J. 1988 Apr;7(4):1159-65 PMID: 3402434
  25. Two tandemly linked identical genes code for the glycosomal glyceraldehyde-phosphate dehydrogenase in Trypanosoma brucei.
    EMBO J. 1986 May;5(5):1049-56 PMID: 3013612
  26. Glucosephosphate isomerase from Trypanosoma brucei. Cloning and characterization of the gene and analysis of the enzyme.
    Eur J Biochem. 1989 Sep 15;184(2):455-64 PMID: 2792108
  27. Two genes encode the major membrane-associated protein of methanol-induced peroxisomes from Candida boidinii.
    J Biol Chem. 1989 Aug 15;264(23):13929-37 PMID: 2760051
  28. Common elements on the surface of glycolytic enzymes from Trypanosoma brucei may serve as topogenic signals for import into glycosomes.
    EMBO J. 1987 Jan;6(1):215-21 PMID: 3582360
  29. Expression of the lacZ gene from two methanol-regulated promoters in Pichia pastoris.
    Nucleic Acids Res. 1987 May 11;15(9):3859-76 PMID: 3108861
  30. Deduced sequence of a malate synthase polypeptide encoded by a subclass of the gene family.
    J Biol Chem. 1989 Feb 15;264(5):2778-82 PMID: 2914930
  31. Investigation of the glyoxysome-peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy.
    J Cell Biol. 1985 Oct;101(4):1288-99 PMID: 3930507
  32. Inducible beta-oxidation pathway in Neurospora crassa.
    J Bacteriol. 1985 Jan;161(1):153-7 PMID: 3155714
  33. How proteins get into microbodies (peroxisomes, glyoxysomes, glycosomes).
    Biochim Biophys Acta. 1986 May 5;866(4):179-203 PMID: 3516224
  34. The primary structure of spinach glycolate oxidase deduced from the DNA sequence of a cDNA clone.
    J Biol Chem. 1987 Nov 25;262(33):15825-8 PMID: 2824469
  35. Compartmentation of carbohydrate metabolism in trypanosomes.
    Annu Rev Microbiol. 1987;41:127-51 PMID: 3120638
  36. Energy metabolism of protozoa without mitochondria.
    Annu Rev Microbiol. 1988;42:465-88 PMID: 3059999
  37. Peroxisome biogenesis revisited.
    Biochim Biophys Acta. 1989 Jun 1;1008(1):1-13 PMID: 2655706
  38. Proliferation of microbodies in Saccharomyces cerevisiae.
    Yeast. 1987 Jun;3(2):77-84 PMID: 3332968
  39. An improved procedure for immunoelectron microscopy: ultrathin plastic embedding of immunolabeled ultrathin frozen sections.
    Proc Natl Acad Sci U S A. 1984 Sep;81(18):5744-7 PMID: 6435119
  40. Antibodies directed against the peroxisomal targeting signal of firefly luciferase recognize multiple mammalian peroxisomal proteins.
    J Cell Biol. 1990 Jan;110(1):27-34 PMID: 1688562
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1991-09-00
Pages
893-904
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289121
Subset
IM
Grants
NIDDK NIH HHS · DK41737 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com