Home LiteratureArticle Details
PMID: 7806387 Published · ppublish English Journal Article

Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases.

Infection and immunity ·Vol. 63 ·No. 1 ·1995-01-00 ·Pages 82-7

Gordon VM, Klimpel KR, Arora N, Henderson MA, Leppla SH

Abstract

Before intoxication can occur, anthrax toxin protective antigen (PA), Pseudomonas exotoxin A (PE), and diphtheria toxin (DT) must be activated by proteolytic cleavage at specific amino acid sequences. Previously, it was shown that PA and DT can be activated by furin. In Chinese hamster ovary (CHO) cells, wild-type (RKKR) and cleavage site mutants of PA, each administered with a modified form of anthrax toxin lethal factor (the N terminus of lethal factor fused to PE domain III), had the following potencies: RKKR (wild type) (concentration causing 50% cell death [EC50] = 12 ng/ml) > or = RAAR (EC50 = 18 ng/ml) > FTKR (EC50 = 24 ng/ml) > STRR (EC50 = 49 ng/ml). In vitro cleavage of PA and cleavage site mutants of PA by furin demonstrated that native PA (RKKR) and PA with the cleavage sequence RAAR are substrates for furin. To characterize eukaryotic proteases that play a role in activating bacterial toxins, furin-deficient CHO cells were selected after chemical mutagenesis. Furin-deficient cells were resistant to PE, whose cleavage site, RQPR, constitutes a furin recognition site and to all PA cleavage site mutants, but were sensitive to DT (EC50 = 2.9 ng/ml) and PA (EC50 = 23 ng/ml), whose respective cleavage sites, RKKR and RVRR, contain additional basic residues. Furin-deficient cells that were transfected with the furin gene regained sensitivity to PE and PA cleavage site mutants. These studies provide evidence that furin can activate the three toxins and that one or more additional proteases contribute to the activation of DT and PA.

MeSH Terms
ADP Ribose Transferases Amino Acid Sequence Animals Antigens, Bacterial Bacterial Toxins/genetics,metabolism,toxicity CHO Cells Cathepsin B/metabolism Cricetinae Diphtheria Toxin/metabolism,toxicity Dose-Response Relationship, Drug Endopeptidases/deficiency,genetics,metabolism Exotoxins/genetics,metabolism,toxicity Furin Leupeptins/pharmacology Molecular Sequence Data Peptide Fragments/toxicity Substrate Specificity Subtilisins/deficiency,genetics,metabolism Virulence Factors
Chemicals
Antigens, Bacterial Bacterial Toxins Diphtheria Toxin Exotoxins Leupeptins Peptide Fragments Virulence Factors anthrax toxin ADP Ribose Transferases toxA protein, Pseudomonas aeruginosa Endopeptidases Subtilisins Furin Cathepsin B leupeptin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Gordon V M
Laboratory of Microbial Ecology, National Institute of Dental Research, Bethesda, Maryland 20892.
Klimpel K R
Arora N
Henderson M A
Leppla S H
References (39)
39 references, click to expand
  1. Proprotein processing activity and cleavage site selectivity of the Kex2-like endoprotease PACE4.
    FEBS Lett. 1993 Dec 20;336(1):65-9 PMID: 8262218
  2. Increased cytotoxic activity of Pseudomonas exotoxin and two chimeric toxins ending in KDEL.
    J Biol Chem. 1991 Sep 15;266(26):17376-81 PMID: 1910044
  3. Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases.
    Infect Immun. 1994 Feb;62(2):333-40 PMID: 8300195
  4. A furin-defective cell line is able to process correctly the gp160 of human immunodeficiency virus type 1.
    J Virol. 1994 Jun;68(6):4075-9 PMID: 8189547
  5. Genetic deficiency in low density lipoprotein receptor-related protein confers cellular resistance to Pseudomonas exotoxin A. Evidence that this protein is required for uptake and degradation of multiple ligands.
    J Cell Sci. 1994 Mar;107 ( Pt 3):719-26 PMID: 8006085
  6. Fusions of anthrax toxin lethal factor to the ADP-ribosylation domain of Pseudomonas exotoxin A are potent cytotoxins which are translocated to the cytosol of mammalian cells.
    J Biol Chem. 1992 Aug 5;267(22):15542-8 PMID: 1639793
  7. Positional and additive effects of basic amino acids on processing of precursor proteins within the constitutive secretory pathway.
    FEBS Lett. 1993 Apr 12;320(3):215-8 PMID: 8462689
  8. Role of beta-turn in proteolytic processing of peptide hormone precursors at dibasic sites.
    Biochemistry. 1993 May 11;32(18):4925-30 PMID: 8490028
  9. PACE4 is a member of the mammalian propeptidase family that has overlapping but not identical substrate specificity to PACE.
    Biochemistry. 1993 Nov 2;32(43):11586-90 PMID: 8218226
  10. Evidence for involvement of furin in cleavage and activation of diphtheria toxin.
    J Biol Chem. 1993 Dec 15;268(35):26461-5 PMID: 8253774
  11. 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
  12. Consensus sequence for precursor processing at mono-arginyl sites. Evidence for the involvement of a Kex2-like endoprotease in precursor cleavages at both dibasic and mono-arginyl sites.
    J Biol Chem. 1992 Aug 15;267(23):16335-40 PMID: 1644818
  13. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen.
    J Biol Chem. 1992 Aug 15;267(23):16396-402 PMID: 1644824
  14. Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10277-81 PMID: 1438214
  15. Cell-mediated cleavage of Pseudomonas exotoxin between Arg279 and Gly280 generates the enzymatically active fragment which translocates to the cytosol.
    J Biol Chem. 1992 Dec 15;267(35):25396-401 PMID: 1460035
  16. Differential processing of proenkephalin by prohormone convertases 1(3) and 2 and furin.
    J Biol Chem. 1993 Dec 25;268(36):27084-93 PMID: 8262946
  17. Functional mapping of anthrax toxin lethal factor by in-frame insertion mutagenesis.
    J Biol Chem. 1991 Oct 25;266(30):20124-30 PMID: 1939073
  18. Characterization of a cellular protease that cleaves Pseudomonas exotoxin.
    Infect Immun. 1992 Feb;60(2):497-502 PMID: 1730481
  19. Preferred sequence requirements for cleavage of pro-von Willebrand factor by propeptide-processing enzymes.
    Blood. 1992 May 1;79(9):2349-55 PMID: 1571548
  20. The alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A.
    J Biol Chem. 1992 Jun 25;267(18):12420-3 PMID: 1618748
  21. Selection of Pseudomonas exotoxin-resistant cells with altered expression of alpha 2MR/LRP.
    Ann N Y Acad Sci. 1994 Sep 10;737:138-44 PMID: 7944142
  22. Rapid entry of nicked diphtheria toxin into cells at low pH. Characterization of the entry process and effects of low pH on the toxin molecule.
    J Biol Chem. 1981 Sep 10;256(17):9068-76 PMID: 7263699
  23. Strains of CHO-K1 cells resistant to Pseudomonas exotoxin A and cross-resistant to diphtheria toxin and viruses.
    Infect Immun. 1983 Sep;41(3):998-1009 PMID: 6411625
  24. Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process.
    J Biol Chem. 1986 Jun 5;261(16):7123-6 PMID: 3711080
  25. Inhibitors of receptor-mediated endocytosis block the entry of Bacillus anthracis adenylate cyclase toxin but not that of Bordetella pertussis adenylate cyclase toxin.
    Infect Immun. 1988 May;56(5):1066-9 PMID: 2895741
  26. Specific cleavage of diphtheria toxin by human urokinase.
    Biochem Biophys Res Commun. 1988 Dec 15;157(2):747-54 PMID: 3144277
  27. Production and purification of anthrax toxin.
    Methods Enzymol. 1988;165:103-16 PMID: 3148094
  28. Translocation of diphtheria toxin A-fragment to the cytosol. Role of the site of interfragment cleavage.
    J Biol Chem. 1989 Sep 15;264(26):15709-13 PMID: 2768283
  29. Domain II mutants of Pseudomonas exotoxin deficient in translocation.
    J Biol Chem. 1989 Sep 25;264(27):15953-9 PMID: 2506173
  30. A deleted variant of Bacillus anthracis protective antigen is non-toxic and blocks anthrax toxin action in vivo.
    J Biol Chem. 1989 Nov 15;264(32):19103-7 PMID: 2509473
  31. Pseudomonas exotoxin contains a specific sequence at the carboxyl terminus that is required for cytotoxicity.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):308-12 PMID: 2104981
  32. Cellular processing of the interleukin-2 fusion toxin DAB486-IL-2 and efficient delivery of diphtheria fragment A to the cytosol of target cells requires Arg194.
    J Biol Chem. 1990 Nov 25;265(33):20673-7 PMID: 2243114
  33. Inhibitor studies indicate that active cathepsin L is probably essential to its own processing in cultured fibroblasts.
    Biochem J. 1990 Nov 15;272(1):39-44 PMID: 2264836
  34. Human fur gene encodes a yeast KEX2-like endoprotease that cleaves pro-beta-NGF in vivo.
    J Cell Biol. 1990 Dec;111(6 Pt 2):2851-9 PMID: 2269657
  35. Disruption of the Golgi apparatus by brefeldin A inhibits the cytotoxicity of ricin, modeccin, and Pseudomonas toxin.
    Exp Cell Res. 1991 Feb;192(2):389-95 PMID: 1899070
  36. A mutant CHO-K1 strain with resistance to Pseudomonas exotoxin A and alphaviruses fails to cleave Sindbis virus glycoprotein PE2.
    J Virol. 1991 May;65(5):2332-9 PMID: 1850015
  37. Mammalian subtilisins: the long-sought dibasic processing endoproteases.
    Cell. 1991 Jul 12;66(1):1-3 PMID: 2070411
  38. Functional expression of furin demonstrating its intracellular localization and endoprotease activity for processing of proalbumin and complement pro-C3.
    J Biol Chem. 1991 Sep 5;266(25):16954-9 PMID: 1885622
  39. Expression of mouse furin in a Chinese hamster cell resistant to Pseudomonas exotoxin A and viruses complements the genetic lesion.
    J Biol Chem. 1993 Feb 5;268(4):2590-4 PMID: 8381410
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1995-01-00
Pages
82-7
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC172960
Subset
IM
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