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PMID: 8995623 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The role of eukaryotic subtilisin-like endoproteases for the activation of human immunodeficiency virus glycoproteins in natural host cells.

Journal of virology ·Vol. 71 ·No. 2 ·1997-02-00 ·Pages 1036-45

Hallenberger S, Moulard M, Sordel M, Klenk HD, Garten W

Abstract

Proteolytic activation of the precursor envelope glycoproteins gp160 of human immunodeficiency virus type 1 (HIV-1) and gp140 of HIV-2, a prerequisite for viral infection, results in the formation of gp120/gp41 and gp125/gp36, respectively. Cleavage is mediated by cellular proteases. Furin, a member of the eukaryotic subtilisin family, has been shown to be an activating protease for HIV. Here, we compared the presence of furin and other mammalian subtilisins in lymphatic cells and tissues. Northern blot analyses revealed that furin and the recently discovered protease LPC/PC7 were the only subtilisin-like enzymes transcribed in such cells. Furin was identified as an enzymatically active endoprotease present in different lymphocytic, as well as monocytic, cell lines. When expressed from vaccinia virus vectors, the proprotein convertases were correctly processed, transported, and secreted into the media and enzymatically active. Coexpression of different subtilisins with the HIV envelope precursors revealed that furin and LPC/PC7 are able to cleave HIV-1 gp160. Moreover, both enzymes proteolytically processed the envelope precursor of HIV-2. gp140 was also cleaved to some extent by PC1, which is not, however, present in lymphatic cells. Furin- and LPC/PC7-catalyzed cleavage of HIV-1 gp160 resulted in biologically active envelope protein. In conclusion, among the known members of the subtilisin family, only furin and LPC/PC7 fulfill the requirements of a protease responsible for in vivo activation of HIV envelope glycoproteins.

MeSH Terms
Animals Cell Line Gene Products, env/metabolism HIV Antigens/metabolism HIV Envelope Protein gp120/metabolism HIV Envelope Protein gp41/metabolism HIV-1/physiology HIV-2/physiology Humans Lymphatic System/virology Subtilisins/genetics,metabolism Virus Activation env Gene Products, Human Immunodeficiency Virus
Chemicals
Gene Products, env HIV Antigens HIV Envelope Protein gp120 HIV Envelope Protein gp41 env Gene Products, Human Immunodeficiency Virus env protein gp36, Human immunodeficiency virus Subtilisins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hallenberger S
Institut für Virologie, Philipps-Universität Marburg, Germany.
Moulard M
Sordel M
Klenk H D
Garten W
References (62)
62 references, click to expand
  1. cDNA structure, tissue distribution, and chromosomal localization of rat PC7, a novel mammalian proprotein convertase closest to yeast kexin-like proteinases.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3388-93 PMID: 8622945
  2. 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
  3. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus.
    Nature. 1984 Dec 20-1985 Jan 2;312(5996):763-7 PMID: 6096719
  4. Inhibition of proteolytic cleavage of the hemagglutinin of influenza virus by the calcium-specific ionophore A23187.
    EMBO J. 1984 Dec 1;3(12):2911-5 PMID: 6441705
  5. Characterization of gp41 as the transmembrane protein coded by the HTLV-III/LAV envelope gene.
    Science. 1985 Sep 27;229(4720):1402-5 PMID: 2994223
  6. Detection of a fusion peptide sequence in the transmembrane protein of human immunodeficiency virus.
    Cell. 1987 Jul 31;50(3):327-8 PMID: 3496970
  7. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus.
    Cell. 1988 Apr 8;53(1):55-67 PMID: 2450679
  8. West African HIV-2-related human retrovirus with attenuated cytopathicity.
    Science. 1988 Jun 10;240(4858):1525-9 PMID: 3375832
  9. Mutational analysis of the cleavage sequence of the human immunodeficiency virus type 1 envelope glycoprotein precursor gp160.
    J Virol. 1989 Nov;63(11):4670-5 PMID: 2677400
  10. Role of conserved glycosylation sites in maturation and transport of influenza A virus hemagglutinin.
    J Virol. 1993 Jun;67(6):3048-60 PMID: 8497042
  11. Legitimate and illegitimate cleavage of human immunodeficiency virus glycoproteins by furin.
    J Virol. 1993 Jun;67(6):3601-4 PMID: 8497067
  12. Reduction of background problems in nonradioactive northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations.
    Anal Biochem. 1993 May 1;210(2):235-44 PMID: 7685563
  13. Processing protease for gp160 human immunodeficiency virus type I envelope glycoprotein precursor in human T4+ lymphocytes. Purification and characterization.
    J Biol Chem. 1993 Jun 25;268(18):13406-13 PMID: 8099909
  14. Identification of an isoform with an extremely large Cys-rich region of PC6, a Kex2-like processing endoprotease.
    FEBS Lett. 1993 Jul 26;327(2):165-71 PMID: 8335106
  15. Kex2p: a model for cellular endoprotease processing human immunodeficiency virus type 1 envelope glycoprotein precursor.
    Eur J Biochem. 1994 Oct 15;225(2):565-72 PMID: 7957171
  16. Correlation of proteolytic cleavage of F protein precursors in paramyxoviruses with expression of the fur, PACE4 and PC6 genes in mammalian cells.
    J Gen Virol. 1994 Oct;75 ( Pt 10):2821-7 PMID: 7931173
  17. Characterization of a secreted form of human furin endoprotease.
    Biochem Biophys Res Commun. 1993 Sep 15;195(2):1011-8 PMID: 8373381
  18. Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation.
    J Cell Biol. 1994 Dec;127(6 Pt 2):1829-42 PMID: 7806563
  19. The family of subtilisin/kexin like pro-protein and pro-hormone convertases: divergent or shared functions.
    Biochimie. 1994;76(3-4):197-209 PMID: 7819324
  20. Processing of viral glycoproteins by the subtilisin-like endoprotease furin and its inhibition by specific peptidylchloroalkylketones.
    Biochimie. 1994;76(3-4):217-25 PMID: 7819326
  21. T4-lymphocyte endoprotease responsible for the proteolytic processing of HIV-1 gp160, like Kex2p endoprotease, is a calcium-dependent enzyme.
    Biochimie. 1994;76(3-4):251-6 PMID: 7819331
  22. Proteolytic processing of human cytomegalovirus glycoprotein B (gpUL55) is mediated by the human endoprotease furin.
    Virology. 1995 Jan 10;206(1):746-9 PMID: 7726996
  23. Endoproteolytic cleavage of its propeptide is a prerequisite for efficient transport of furin out of the endoplasmic reticulum.
    J Biol Chem. 1995 Feb 10;270(6):2695-702 PMID: 7852339
  24. Biochemical and genetic definition of the cellular protease required for HIV-1 gp160 processing.
    J Biol Chem. 1995 Feb 17;270(7):3154-9 PMID: 7852398
  25. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion.
    J Virol. 1995 Jun;69(6):3308-14 PMID: 7745678
  26. Furin is important but not essential for the proteolytic maturation of gp160 of HIV-1.
    FEBS Lett. 1995 May 22;365(1):95-7 PMID: 7774724
  27. Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin.
    EMBO J. 1995 Jun 1;14(11):2424-35 PMID: 7781597
  28. A second mutant allele of furin in the processing-incompetent cell line, LoVo. Evidence for involvement of the homo B domain in autocatalytic activation.
    J Biol Chem. 1995 Nov 3;270(44):26565-9 PMID: 7592877
  29. Assembly of SIV virus-like particles containing envelope proteins using a baculovirus expression system.
    Virology. 1995 Dec 1;214(1):50-8 PMID: 8525638
  30. Calcium requirement and inhibitor spectrum for intracellular HIV type 1 gp160 processing in cultured HeLa cells and CD4+ lymphocytes: similarity to those of viral envelope glycoprotein maturase.
    J Biochem. 1995 Jun;117(6):1244-53 PMID: 7490267
  31. A mutation of furin causes the lack of precursor-processing activity in human colon carcinoma LoVo cells.
    Biochem Biophys Res Commun. 1993 Sep 15;195(2):1019-26 PMID: 7690548
  32. Inhibition of HIV-1 gp160-dependent membrane fusion by a furin-directed alpha 1-antitrypsin variant.
    J Biol Chem. 1993 Nov 25;268(33):24887-91 PMID: 8227051
  33. Proprotein processing activity and cleavage site selectivity of the Kex2-like endoprotease PACE4.
    FEBS Lett. 1993 Dec 20;336(1):65-9 PMID: 8262218
  34. Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus.
    J Virol. 1994 Feb;68(2):1213-8 PMID: 8289354
  35. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface.
    EMBO J. 1994 Jan 1;13(1):18-33 PMID: 7508380
  36. Proteolytic cleavage of wild type and mutants of the F protein of human parainfluenza virus type 3 by two subtilisin-like endoproteases, furin and Kex2.
    J Virol. 1994 Apr;68(4):2772-6 PMID: 8139055
  37. The convertases furin and PC1 can both cleave the human immunodeficiency virus (HIV)-1 envelope glycoprotein gp160 into gp120 (HIV-1 SU) and gp41 (HIV-I TM).
    J Biol Chem. 1994 Apr 22;269(16):12240-7 PMID: 8163529
  38. 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
  39. Activation of an influenza virus A/turkey/Oregon/71 HA insertion variant by the subtilisin-like endoprotease furin.
    Virology. 1994 Aug 1;202(2):988-91 PMID: 8030261
  40. Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses.
    J Virol. 1994 Sep;68(9):6074-8 PMID: 8057485
  41. A new member of the proprotein convertase gene family (LPC) is located at a chromosome translocation breakpoint in lymphomas.
    Cancer Res. 1996 Feb 1;56(3):448-51 PMID: 8564950
  42. PC8 [corrected], a new member of the convertase family.
    Biochem J. 1996 Mar 15;314 ( Pt 3):727-31 PMID: 8615762
  43. 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
  44. Mutational analysis of the human immunodeficiency virus type 1 env gene product proteolytic cleavage site.
    J Virol. 1990 May;64(5):2337-44 PMID: 2182911
  45. Expression of a human proprotein processing enzyme: correct cleavage of the von Willebrand factor precursor at a paired basic amino acid site.
    Proc Natl Acad Sci U S A. 1990 Dec;87(23):9378-82 PMID: 2251280
  46. 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
  47. The V3 loops of the HIV-1 and HIV-2 surface glycoproteins contain proteolytic cleavage sites: a possible function in viral fusion?
    AIDS Res Hum Retroviruses. 1991 Jan;7(1):3-16 PMID: 2015114
  48. Immunopathogenesis of HIV infection.
    FASEB J. 1991 Jul;5(10):2382-90 PMID: 1676689
  49. Mammalian subtilisins: the long-sought dibasic processing endoproteases.
    Cell. 1991 Jul 12;66(1):1-3 PMID: 2070411
  50. 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
  51. Immunological analysis of human immunodeficiency virus type 1 envelope glycoprotein proteolytic cleavage.
    Virology. 1992 Apr;187(2):825-8 PMID: 1372142
  52. 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
  53. Cytoplasmic domain truncation enhances fusion activity by the exterior glycoprotein complex of human immunodeficiency virus type 2 in selected cell types.
    J Virol. 1992 Jun;66(6):3971-5 PMID: 1583738
  54. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease.
    EMBO J. 1992 Jul;11(7):2407-14 PMID: 1628614
  55. Identification and characterization of fusion and processing domains of the human immunodeficiency virus type 2 envelope glycoprotein.
    J Virol. 1992 Sep;66(9):5472-8 PMID: 1501283
  56. Mammalian subtilisin-related proteinases in cleavage activation of the paramyxovirus fusion glycoprotein: superiority of furin/PACE to PC2 or PC1/PC3.
    J Virol. 1992 Nov;66(11):6391-7 PMID: 1404596
  57. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160.
    Nature. 1992 Nov 26;360(6402):358-61 PMID: 1360148
  58. Structure and function of eukaryotic proprotein processing enzymes of the subtilisin family of serine proteases.
    Crit Rev Oncog. 1993;4(2):115-36 PMID: 8420571
  59. Analysis of protein expression and virus-like particle formation in mammalian cell lines stably expressing HIV-1 gag and env gene products with or without active HIV proteinase.
    Virology. 1993 Feb;192(2):605-17 PMID: 8421902
  60. 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
  61. Effect of mutations in the V3 loop of HIV-1 gp120 on infectivity and susceptibility to proteolytic cleavage.
    AIDS Res Hum Retroviruses. 1993 Feb;9(2):159-66 PMID: 8457383
  62. Comparative cellular processing of the human immunodeficiency virus (HIV-1) envelope glycoprotein gp160 by the mammalian subtilisin/kexin-like convertases.
    Biochem J. 1996 Mar 1;314 ( Pt 2):521-32 PMID: 8670066
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1997-02-00
Pages
1036-45
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC191154
Subset
IM
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