Home LiteratureArticle Details
PMID: 12441076 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Murine coronavirus-induced apoptosis in 17Cl-1 cells involves a mitochondria-mediated pathway and its downstream caspase-8 activation and bid cleavage.

Virology ·Vol. 302 ·No. 2 ·2002-10-25 ·Pages 321-32

Chen CJ, Makino S

Abstract

Mouse hepatitis virus (MHV) infection in murine 17Cl-1 cells results in apoptotic cell death. Inhibition of MHV-induced apoptosis by the pancaspase inhibitor Z-VAD-FMK promoted virus production late in infection, indicating that apoptosis could be a host response to limit the production of viral progeny. Activation of the mitochondria-mediated apoptotic pathway was indicated by the activation of caspase-9 and delay of apoptosis by Bcl-2 overexpression. Analyses of the subcellular distribution of cytochrome c, procaspase-9, and Apaf-1 suggested an aberrant apoptosome formation in the vicinity of the mitochondria, which could be a cell type-specific event. An increase in the amount of Fas (APO-1/CD95), caspase-8 activation, caspase-8-mediated Bid cleavage, and subsequent translocation of truncated Bid to mitochondria, all of which relate to the Fas-mediated pathway, also occurred in MHV-infected 17Cl-1 cells, whereas the formation of the death-inducing signaling complex, a direct indication of the activation of Fas-mediated pathway, was undetectable. Caspase-8 and Bid activation appeared to be downstream of mitochondria, because Bcl-2 overexpression suppressed both events, suggesting that infected 17Cl-1 cells might have activated a receptor-mediated "type II" signaling pathway, in which primary and low levels of receptor-mediated pathway activation lead to the activation of the mitochondria-mediated pathway. All our data indicate that a mitochondria-mediated pathway played a major regulatory role in apoptosis in MHV-infected 17Cl-1 cells.

MeSH Terms
Animals Apoptosis BH3 Interacting Domain Death Agonist Protein Carrier Proteins/metabolism Caspase 8 Caspase 9 Caspase Inhibitors Caspases/metabolism Cell Line Enzyme Activation Mice Mitochondria/physiology Murine hepatitis virus/pathogenicity,physiology Proto-Oncogene Proteins c-bcl-2/metabolism
Chemicals
BH3 Interacting Domain Death Agonist Protein Bid protein, mouse Carrier Proteins Caspase Inhibitors Proto-Oncogene Proteins c-bcl-2 Casp8 protein, mouse Casp9 protein, mouse Caspase 8 Caspase 9 Caspases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Chen Chun-Jen
Department of Microbiology and Immunology, The University of Texas Medical Branch at Galveston, 77555-1019, USA.
Makino Shinji
References (54)
54 references, click to expand
  1. Lack of release of cytochrome C from mitochondria into cytosol early in the course of Fas-mediated apoptosis of Jurkat cells.
    J Biol Chem. 1998 Jul 31;273(31):19892-4 PMID: 9677426
  2. Solution structure of BID, an intracellular amplifier of apoptotic signaling.
    Cell. 1999 Mar 5;96(5):615-24 PMID: 10089877
  3. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene.
    Nature. 1993 Feb 25;361(6414):739-42 PMID: 8441470
  4. Enhanced growth of a murine coronavirus in transformed mouse cells.
    Infect Immun. 1972 Oct;6(4):501-7 PMID: 4564284
  5. Proapoptotic BH3-only Bcl-2 family members induce cytochrome c release, but not mitochondrial membrane potential loss, and do not directly modulate voltage-dependent anion channel activity.
    Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):577-82 PMID: 10639121
  6. The adapter protein apoptotic protease-activating factor-1 (Apaf-1) is proteolytically processed during apoptosis.
    J Biol Chem. 2001 Aug 10;276(32):29772-81 PMID: 11387322
  7. The cellular and molecular pathogenesis of coronaviruses.
    Lab Anim Sci. 1993 Feb;43(1):15-28 PMID: 8384676
  8. Mammalian caspases: structure, activation, substrates, and functions during apoptosis.
    Annu Rev Biochem. 1999;68:383-424 PMID: 10872455
  9. A MURINE VIRUS (JHM) CAUSING DISSEMINATED ENCEPHALOMYELITIS WITH EXTENSIVE DESTRUCTION OF MYELIN : II. PATHOLOGY.
    J Exp Med. 1949 Aug 31;90(3):195-212 PMID: 19871701
  10. BCL-2 family members and the mitochondria in apoptosis.
    Genes Dev. 1999 Aug 1;13(15):1899-911 PMID: 10444588
  11. The Bcl-2 protein family: arbiters of cell survival.
    Science. 1998 Aug 28;281(5381):1322-6 PMID: 9735050
  12. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis.
    Science. 1997 Feb 21;275(5303):1132-6 PMID: 9027315
  13. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3.
    Cell. 1997 Aug 8;90(3):405-13 PMID: 9267021
  14. Transmissible gastroenteritis coronavirus induces programmed cell death in infected cells through a caspase-dependent pathway.
    J Virol. 1998 Jun;72(6):4918-24 PMID: 9573259
  15. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation.
    J Biol Chem. 1999 Jun 18;274(25):17941-5 PMID: 10364241
  16. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor.
    EMBO J. 1995 Nov 15;14(22):5579-88 PMID: 8521815
  17. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death.
    Science. 2001 Apr 27;292(5517):727-30 PMID: 11326099
  18. Pathogenesis of mouse hepatitis virus-induced demyelination.
    J Neurovirol. 1996 Dec;2(6):361-76 PMID: 8972418
  19. Apoptosis and hematopoiesis in murine fetal liver.
    Blood. 1993 Jan 15;81(2):373-84 PMID: 7678514
  20. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade.
    Cell. 1997 Nov 14;91(4):479-89 PMID: 9390557
  21. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors.
    Cell. 1998 Aug 21;94(4):481-90 PMID: 9727491
  22. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane.
    Mol Cell Biol. 2000 Feb;20(3):929-35 PMID: 10629050
  23. Conversion of Bcl-2 to a Bax-like death effector by caspases.
    Science. 1997 Dec 12;278(5345):1966-8 PMID: 9395403
  24. Caspase-8 activation and bid cleavage contribute to MCF7 cellular execution in a caspase-3-dependent manner during staurosporine-mediated apoptosis.
    J Biol Chem. 2000 Mar 31;275(13):9303-7 PMID: 10734071
  25. Pathogenesis of coronavirus-induced infections. Review of pathological and immunological aspects.
    Adv Exp Med Biol. 1998;440:503-13 PMID: 9782322
  26. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner.
    J Cell Biol. 1999 Jan 25;144(2):281-92 PMID: 9922454
  27. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9.
    J Biol Chem. 1999 Apr 23;274(17):11549-56 PMID: 10206961
  28. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC).
    EMBO J. 1997 May 15;16(10):2794-804 PMID: 9184224
  29. Construction and applications of a highly transmissible murine retrovirus shuttle vector.
    Cell. 1984 Jul;37(3):1053-62 PMID: 6331674
  30. The biology and pathogenesis of coronaviruses.
    Curr Top Microbiol Immunol. 1982;99:165-200 PMID: 6178564
  31. Induction of caspase-dependent apoptosis in cultured cells by the avian coronavirus infectious bronchitis virus.
    J Virol. 2001 Jul;75(14):6402-9 PMID: 11413307
  32. Viral interference with apoptosis.
    Semin Cell Dev Biol. 1998 Jun;9(3):339-49 PMID: 9665871
  33. Caspase structure, proteolytic substrates, and function during apoptotic cell death.
    Cell Death Differ. 1999 Nov;6(11):1028-42 PMID: 10578171
  34. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c.
    Genes Dev. 2000 Aug 15;14(16):2060-71 PMID: 10950869
  35. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization.
    Mol Cell. 1998 Jun;1(7):949-57 PMID: 9651578
  36. Cytochrome c-dependent and -independent induction of apoptosis in multiple myeloma cells.
    J Biol Chem. 1997 Nov 28;272(48):29995-7 PMID: 9374472
  37. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis.
    Science. 2000 Dec 1;290(5497):1761-5 PMID: 11099414
  38. Molecular characterization of mitochondrial apoptosis-inducing factor.
    Nature. 1999 Feb 4;397(6718):441-6 PMID: 9989411
  39. Regulation of apoptosis by viral gene products.
    J Virol. 1997 Mar;71(3):1739-46 PMID: 9032302
  40. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked.
    Science. 1997 Feb 21;275(5303):1129-32 PMID: 9027314
  41. Induction of apoptosis in murine coronavirus-infected cultured cells and demonstration of E protein as an apoptosis inducer.
    J Virol. 1999 Sep;73(9):7853-9 PMID: 10438879
  42. Two CD95 (APO-1/Fas) signaling pathways.
    EMBO J. 1998 Mar 16;17(6):1675-87 PMID: 9501089
  43. Replication and plaque formation of mouse hepatitis virus (MHV-2) in mouse cell line DBT culture.
    Arch Gesamte Virusforsch. 1974;44(3):298-302 PMID: 4365902
  44. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells.
    J Biol Chem. 1999 Aug 6;274(32):22532-8 PMID: 10428830
  45. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL.
    J Biol Chem. 1999 Jan 22;274(4):2225-33 PMID: 9890985
  46. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis.
    Dev Cell. 2002 Jan;2(1):55-67 PMID: 11782314
  47. Bax directly induces release of cytochrome c from isolated mitochondria.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4997-5002 PMID: 9560217
  48. Apoptosis in the absence of cytochrome c accumulation in the cytosol.
    Biochem Biophys Res Commun. 1998 Jan 14;242(2):380-4 PMID: 9446803
  49. The viral nucleocapsid protein of transmissible gastroenteritis coronavirus (TGEV) is cleaved by caspase-6 and -7 during TGEV-induced apoptosis.
    J Virol. 2000 May;74(9):3975-83 PMID: 10756009
  50. Coronavirus MHV-3-induced apoptosis in macrophages.
    Virology. 1998 Oct 10;250(1):41-9 PMID: 9770418
  51. Mitochondrial release of caspase-2 and -9 during the apoptotic process.
    J Exp Med. 1999 Jan 18;189(2):381-94 PMID: 9892620
  52. Viruses and apoptosis.
    J Gen Virol. 1998 Aug;79 ( Pt 8):1833-45 PMID: 9714231
  53. The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling.
    J Cell Biol. 1998 Mar 23;140(6):1485-95 PMID: 9508780
  54. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis.
    Cell. 1998 Aug 21;94(4):491-501 PMID: 9727492
Article Info
Journal
Virology
Abbr.
Virology
ISSN
0042-6822
Published
2002-10-25
Pages
321-32
Language
English
Region
United States
NLM ID
0110674
PMCID
PMC7131008
Subset
IM
Grants
NIAID NIH HHS · AI29984 · 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