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PMID: 8194519 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A C-terminal domain conserved in precursor processing proteases is required for intramolecular N-terminal maturation of pro-Kex2 protease.

The EMBO journal ·Vol. 13 ·No. 10 ·1994-05-15 ·Pages 2280-8

Gluschankof P, Fuller RS

Abstract

The Kex2 protease of the yeast Saccharomyces cerevisiae is the prototype of a family of eukaryotic subtilisin homologs thought to process prohormones and other precursors in the secretory pathway. Deletion analysis of Kex2 protease shows that a sequence of 154-159 residues carboxyl to the subtilisin domain is essential for the formation of active enzyme. Disruption of this region, termed the 'P-domain', blocks the normally rapid intra-molecular cleavage of the N-terminal pro-segment of pro-Kex2 protease in the endoplasmic reticulum (ER). The C-terminal boundary of the P-domain coincides closely with the endpoint of similarity between Kex2 protease and its mammalian homologues. The conservation of and functional requirement for the P-domain sharpens the distinction between a 'Kex2 family' of processing enzymes and degradative 'subtilases', and implies that the Kex2-related enzymes have in common entirely novel structural features that are important in the maturation of precursor polypeptide substrates. Failure to cleave the N-terminal pro-domain, due either to truncation of the P-domain or to mutation of the active site histidine or serine, results in stable, intracellular retention of pro-enzyme, apparently in the ER. Thus pro-Kex2 protease appears to contain an ER retention signal which is removed or destroyed by cleavage of the pro-domain.

Related Genes
MeSH Terms
Amino Acid Sequence Base Sequence Binding Sites/genetics Conserved Sequence DNA Mutational Analysis Endoplasmic Reticulum/metabolism Enzyme Precursors/genetics,metabolism Fungal Proteins/metabolism Molecular Sequence Data Proprotein Convertases Protein Precursors/genetics,metabolism Protein Processing, Post-Translational Saccharomyces cerevisiae/enzymology,metabolism Saccharomyces cerevisiae Proteins Sequence Deletion Sequence Homology, Amino Acid Structure-Activity Relationship Subtilisins/biosynthesis,genetics
Chemicals
Enzyme Precursors Fungal Proteins Protein Precursors Saccharomyces cerevisiae Proteins Proprotein Convertases Subtilisins KEX2 protein, S cerevisiae
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gluschankof P
Department of Biochemistry, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, CA 94305-5307.
Fuller R S
References (57)
57 references, click to expand
  1. Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae.
    Mol Cell Biol. 1984 Aug;4(8):1440-8 PMID: 6092912
  2. Polyprotein gene expression: generation of diversity of neuroendocrine peptides.
    Annu Rev Biochem. 1984;53:665-715 PMID: 6383203
  3. Structural and enzymatic characterization of a purified prohormone-processing enzyme: secreted, soluble Kex2 protease.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):922-6 PMID: 1736307
  4. cDNA sequence of a Drosophila melanogaster gene, Dfur1, encoding a protein structurally related to the subtilisin-like proprotein processing enzyme furin.
    FEBS Lett. 1991 Sep 9;289(2):133-7 PMID: 1915835
  5. Prohormone processing in Xenopus oocytes: characterization of cleavage signals and cleavage enzymes.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11393-7 PMID: 1722329
  6. Identification of a somatostatin-14-generating propeptide converting enzyme as a member of the kex2/furin/PC family.
    Endocrinology. 1991 Oct;129(4):2263-5 PMID: 1680673
  7. Yeast KEX2 genes encodes an endopeptidase homologous to subtilisin-like serine proteases.
    Biochem Biophys Res Commun. 1988 Oct 14;156(1):246-54 PMID: 2845974
  8. Biogenesis of the yeast vacuole (lysosome). Mutation in the active site of the vacuolar serine proteinase yscB abolishes proteolytic maturation of its 73-kDa precursor to the 41.5-kDa pro-enzyme and a newly detected 41-kDa peptide.
    Eur J Biochem. 1992 Feb 1;203(3):641-53 PMID: 1735447
  9. Mutation of a tyrosine localization signal in the cytosolic tail of yeast Kex2 protease disrupts Golgi retention and results in default transport to the vacuole.
    Mol Biol Cell. 1992 Dec;3(12):1353-71 PMID: 1493334
  10. Purification and characterization of furin, a Kex2-like processing endoprotease, produced in Chinese hamster ovary cells.
    J Biol Chem. 1992 Aug 15;267(23):16094-9 PMID: 1644796
  11. Localization of components involved in protein transport and processing through the yeast Golgi apparatus.
    J Cell Biol. 1991 Jan;112(1):27-37 PMID: 1986005
  12. In vitro processing of pro-subtilisin produced in Escherichia coli.
    J Biol Chem. 1988 Sep 15;263(26):12959-63 PMID: 3047114
  13. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Methods Enzymol. 1987;154:367-82 PMID: 3323813
  14. Cloning and functional expression of Dfurin2, a subtilisin-like proprotein processing enzyme of Drosophila melanogaster with multiple repeats of a cysteine motif.
    J Biol Chem. 1992 Aug 25;267(24):17208-15 PMID: 1512259
  15. Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2+-dependent serine protease.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1434-8 PMID: 2646633
  16. Dissecting the catalytic triad of a serine protease.
    Nature. 1988 Apr 7;332(6164):564-8 PMID: 3282170
  17. Identification of the fourth member of the mammalian endoprotease family homologous to the yeast Kex2 protease. Its testis-specific expression.
    J Biol Chem. 1992 Mar 25;267(9):5897-900 PMID: 1372895
  18. The new enzymology of precursor processing endoproteases.
    J Biol Chem. 1992 Nov 25;267(33):23435-8 PMID: 1429684
  19. Intracellular targeting and structural conservation of a prohormone-processing endoprotease.
    Science. 1989 Oct 27;246(4929):482-6 PMID: 2683070
  20. Pro-peptide as an intramolecular chaperone: renaturation of denatured subtilisin E with a synthetic pro-peptide [corrected].
    Mol Microbiol. 1991 Jun;5(6):1507-10 PMID: 1686294
  21. In-vitro processing of yeast alpha-factor leader fusion proteins using a soluble yscF (Kex2) variant.
    Appl Microbiol Biotechnol. 1991 Sep;35(6):771-6 PMID: 1367896
  22. The Kluyveromyces lactis KEX1 gene encodes a subtilisin-type serine proteinase.
    FEBS Lett. 1988 Jul 18;234(2):464-70 PMID: 3292294
  23. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160.
    Nature. 1992 Nov 26;360(6402):358-61 PMID: 1360148
  24. Cloning, sequencing, and secretion of Bacillus amyloliquefaciens subtilisin in Bacillus subtilis.
    Nucleic Acids Res. 1983 Nov 25;11(22):7911-25 PMID: 6316278
  25. Kex2-dependent processing of yeast K1 killer preprotoxin includes cleavage at ProArg-44.
    Mol Microbiol. 1992 Feb;6(4):511-20 PMID: 1560780
  26. A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae.
    Gene. 1988 Oct 30;70(2):303-12 PMID: 3063604
  27. Regulation of PACE propeptide-processing activity: requirement for a post-endoplasmic reticulum compartment and autoproteolytic activation.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8235-9 PMID: 1325651
  28. Characterization of KEX2-encoded endopeptidase from yeast Saccharomyces cerevisiae.
    Biochem Biophys Res Commun. 1989 Feb 28;159(1):305-11 PMID: 2647083
  29. One-step site-directed mutagenesis of the Kex2 protease oxyanion hole.
    Curr Biol. 1993 Aug 1;3(8):498-506 PMID: 15335687
  30. Identification of kex2-related proteases in chromaffin granules by partial amino acid sequence analysis.
    J Biol Chem. 1991 Aug 25;266(24):15679-83 PMID: 1874725
  31. Pro-sequence of subtilisin can guide the refolding of denatured subtilisin in an intermolecular process.
    Nature. 1989 Jun 8;339(6224):483-4 PMID: 2657436
  32. Secretion and autoproteolytic maturation of subtilisin.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3096-100 PMID: 3517850
  33. Isolation of the putative structural gene for the lysine-arginine-cleaving endopeptidase required for processing of yeast prepro-alpha-factor.
    Cell. 1984 Jul;37(3):1075-89 PMID: 6430565
  34. Order of events in the yeast secretory pathway.
    Cell. 1981 Aug;25(2):461-9 PMID: 7026045
  35. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1991 May;113(3):527-38 PMID: 2016334
  36. Structural homology between the human fur gene product and the subtilisin-like protease encoded by yeast KEX2.
    Nucleic Acids Res. 1990 Feb 11;18(3):664 PMID: 2408021
  37. Identification of a human insulinoma cDNA encoding a novel mammalian protein structurally related to the yeast dibasic processing protease Kex2.
    J Biol Chem. 1990 Feb 25;265(6):2997-3000 PMID: 2154467
  38. A novel Kex2 enzyme can process the proregion of the yeast alpha-factor leader in the endoplasmic reticulum instead of in the Golgi.
    Biochem Biophys Res Commun. 1992 Feb 28;183(1):212-9 PMID: 1543492
  39. Homology modelling and protein engineering strategy of subtilases, the family of subtilisin-like serine proteinases.
    Protein Eng. 1991 Oct;4(7):719-37 PMID: 1798697
  40. Enzymes required for yeast prohormone processing.
    Annu Rev Physiol. 1988;50:345-62 PMID: 3288097
  41. Glycosylation and processing of prepro-alpha-factor through the yeast secretory pathway.
    Cell. 1984 Feb;36(2):309-18 PMID: 6420074
  42. Identification of a cDNA encoding a second putative prohormone convertase related to PC2 in AtT20 cells and islets of Langerhans.
    Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):340-4 PMID: 1988934
  43. Conservation of the prohormone convertase gene family in metazoa: analysis of cDNAs encoding a PC3-like protein from hydra.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6678-82 PMID: 1495957
  44. The pro-region of the Kex2 endoprotease of Saccharomyces cerevisiae is removed by self-processing.
    FEBS Lett. 1992 Mar 16;299(3):283-6 PMID: 1544507
  45. Folding of subtilisin BPN': characterization of a folding intermediate.
    Biochemistry. 1993 Jan 12;32(1):18-26 PMID: 8418836
  46. Production of single-stranded plasmid DNA.
    Methods Enzymol. 1987;153:3-11 PMID: 3323803
  47. CLUSTAL V: improved software for multiple sequence alignment.
    Comput Appl Biosci. 1992 Apr;8(2):189-91 PMID: 1591615
  48. Identification of a second human subtilisin-like protease gene in the fes/fps region of chromosome 15.
    DNA Cell Biol. 1991 Dec;10(10):757-69 PMID: 1741956
  49. Identification and functional expression of a new member of the mammalian Kex2-like processing endoprotease family: its striking structural similarity to PACE4.
    J Biochem. 1993 Feb;113(2):132-5 PMID: 8468318
  50. Posttranslational processing of the prohormone-cleaving Kex2 protease in the Saccharomyces cerevisiae secretory pathway.
    J Cell Biol. 1991 Oct;115(2):297-307 PMID: 1918142
  51. Activation of human furin precursor processing endoprotease occurs by an intramolecular autoproteolytic cleavage.
    J Biol Chem. 1992 Jul 15;267(20):14304-8 PMID: 1629222
  52. Activation of the proteinase B precursor of the yeast Saccharomyces cerevisiae by autocatalysis and by an internal sequence.
    J Biol Chem. 1991 Dec 5;266(34):22851-7 PMID: 1744078
  53. Molecular and enzymatic properties of furin, a Kex2-like endoprotease involved in precursor cleavage at Arg-X-Lys/Arg-Arg sites.
    J Biochem. 1992 Mar;111(3):296-301 PMID: 1587790
  54. Transformation of yeast spheroplasts without cell fusion.
    Anal Biochem. 1987 Jun;163(2):391-7 PMID: 3310730
  55. Expression of the Saccharomyces cerevisiae Kex2p endoprotease in inset cells. Evidence for a carboxy-terminal autoprocessing event.
    Eur J Biochem. 1992 Feb 15;204(1):121-6 PMID: 1740121
  56. Requirement of pro-sequence for the production of active subtilisin E in Escherichia coli.
    J Biol Chem. 1987 Jun 5;262(16):7859-64 PMID: 3108260
  57. Cloning and primary sequence of a mouse candidate prohormone convertase PC1 homologous to PC2, Furin, and Kex2: distinct chromosomal localization and messenger RNA distribution in brain and pituitary compared to PC2.
    Mol Endocrinol. 1991 Jan;5(1):111-22 PMID: 2017186
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1994-05-15
Pages
2280-8
Language
English
Region
England
NLM ID
8208664
PMCID
PMC395090
Subset
IM
Grants
NIGMS NIH HHS · GM39697 · United States
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