Home LiteratureArticle Details
PMID: 22362782 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis.

The Journal of biological chemistry ·Vol. 287 ·No. 15 ·2012-04-06 ·Pages 12455-68

Young MM, Takahashi Y, Khan O, Park S, Hori T, Yun J, Sharma AK, Amin S, Hu CD, Zhang J, Kester M, Wang HG

Abstract

Autophagy and apoptosis are two evolutionarily conserved processes that regulate cell fate in response to cytotoxic stress. However, the functional relationship between these two processes remains far from clear. Here, we demonstrate an autophagy-dependent mechanism of caspase-8 activation and initiation of the apoptotic cascade in response to SKI-I, a pan-sphingosine kinase inhibitor, and bortezomib, a proteasome inhibitor. Autophagy is induced concomitantly with caspase-8 activation, which is responsible for initiation of the caspase cascade and the mitochondrial amplification loop that is required for full execution of apoptosis. Inhibition of autophagosome formation by depletion of Atg5 or Atg3 results in a marked suppression of caspase-8 activation and apoptosis. Although caspase-8 self-association depends on p62/SQSTM1, its self-processing requires the autophagosomal membrane. Caspase-8 forms a complex with Atg5 and colocalizes with LC3 and p62. Moreover, FADD, an adaptor protein for caspase-8 activation, associates with Atg5 on Atg16L- and LC3-positive autophagosomal membranes and loss of FADD suppresses cell death. Taken together, these results indicate that the autophagosomal membrane serves as a platform for an intracellular death-inducing signaling complex (iDISC) that recruits self-associated caspase-8 to initiate the caspase-8/-3 cascade.

MeSH Terms
Adaptor Proteins, Signal Transducing/genetics,metabolism Animals Apoptosis Autophagy Autophagy-Related Protein 5 Autophagy-Related Proteins Caspase 3/metabolism Caspase 8/metabolism Cell Membrane/enzymology,metabolism Cell Survival/drug effects Cells, Cultured Death Domain Receptor Signaling Adaptor Proteins/physiology Enzyme Activation Fas-Associated Death Domain Protein/metabolism Gene Knockout Techniques Heat-Shock Proteins/genetics,metabolism Humans Hydrazines/pharmacology Leukemia, Myeloid, Acute Lysosome-Associated Membrane Glycoproteins/metabolism Mice Microtubule-Associated Proteins/genetics,metabolism Mitochondria/drug effects,metabolism Phosphotransferases (Alcohol Group Acceptor)/antagonists & inhibitors,metabolism Protein Binding Protein Multimerization Protein Transport Pyrazoles/pharmacology Sequestosome-1 Protein Tumor Cells, Cultured Ubiquitin-Conjugating Enzymes/genetics,metabolism
Chemicals
Adaptor Proteins, Signal Transducing Atg5 protein, mouse Autophagy-Related Protein 5 Autophagy-Related Proteins Death Domain Receptor Signaling Adaptor Proteins Fadd protein, mouse Fas-Associated Death Domain Protein Heat-Shock Proteins Hydrazines Lamp1 protein, mouse Lysosome-Associated Membrane Glycoproteins Microtubule-Associated Proteins N'-((2-hydroxy-1-naphthyl)methylene)-3-(2-naphthyl)-1H-pyrazole-5-carbohydrazide Pyrazoles Sequestosome-1 Protein Sqstm1 protein, mouse Ubiquitin-Conjugating Enzymes Phosphotransferases (Alcohol Group Acceptor) sphingosine kinase Casp3 protein, mouse Casp8 protein, mouse Caspase 3 Caspase 8 Atg3 protein, mouse
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Young Megan M
Department of Pharmacology and Penn State Hershey Cancer Institute, The Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033, USA.
Takahashi Yoshinori
Khan Osman
Park Sungman
Hori Tsukasa
Yun Jong
Sharma Arun K
Amin Shantu
Hu Chang-Deng
Zhang Jianke
Kester Mark
Wang Hong-Gang
References (60)
60 references, click to expand
  1. The sphingosine kinase 1 inhibitor 2-(p-hydroxyanilino)-4-(p-chlorophenyl)thiazole induces proteasomal degradation of sphingosine kinase 1 in mammalian cells.
    J Biol Chem. 2010 Dec 10;285(50):38841-52 PMID: 20926375
  2. Autophagy and the integrated stress response.
    Mol Cell. 2010 Oct 22;40(2):280-93 PMID: 20965422
  3. Sphingolipid metabolites differentially regulate extracellular signal-regulated kinase and stress-activated protein kinase cascades.
    Biochem J. 1996 May 15;316 ( Pt 1):13-7 PMID: 8645194
  4. Inhibition of protein degradation induces apoptosis through a microtubule-associated protein 1 light chain 3-mediated activation of caspase-8 at intracellular membranes.
    Mol Cell Biol. 2011 Aug;31(15):3158-70 PMID: 21628531
  5. An improved bimolecular fluorescence complementation assay with a high signal-to-noise ratio.
    Biotechniques. 2010 Nov;49(5):793-805 PMID: 21091444
  6. Synthesis and bioactivity of sphingosine kinase inhibitors and their novel aspirinyl conjugated analogs.
    Eur J Med Chem. 2010 Sep;45(9):4149-56 PMID: 20598402
  7. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents.
    J Cell Biol. 2008 Oct 6;183(1):101-16 PMID: 18838554
  8. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells.
    J Cell Biol. 2001 Feb 19;152(4):657-68 PMID: 11266458
  9. Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members.
    Blood. 2005 Apr 15;105(8):3169-77 PMID: 15632208
  10. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate.
    Nature. 1996 Jun 27;381(6585):800-3 PMID: 8657285
  11. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial.
    Ann Intern Med. 2006 Mar 7;144(5):337-43 PMID: 16520474
  12. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes.
    Nat Cell Biol. 2004 Dec;6(12):1221-8 PMID: 15558033
  13. Ceramide and apoptosis: exploring the enigmatic connections between sphingolipid metabolism and programmed cell death.
    Anticancer Agents Med Chem. 2012 May;12(4):340-63 PMID: 21707511
  14. Human adenovirus type 5 induces cell lysis through autophagy and autophagy-triggered caspase activity.
    J Virol. 2011 May;85(10):4720-9 PMID: 21367888
  15. FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells.
    Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16677-82 PMID: 18946037
  16. Proteasome inhibition can induce an autophagy-dependent apical activation of caspase-8.
    Cell Death Differ. 2011 Oct;18(10):1584-97 PMID: 21455219
  17. Mammalian autophagy: core molecular machinery and signaling regulation.
    Curr Opin Cell Biol. 2010 Apr;22(2):124-31 PMID: 20034776
  18. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8.
    Science. 2004 Jun 4;304(5676):1500-2 PMID: 15131264
  19. Caspase-mediated cleavage of ATG6/Beclin-1 links apoptosis to autophagy in HeLa cells.
    Cancer Lett. 2009 Feb 8;274(1):95-100 PMID: 18842334
  20. The efficacy and selectivity of tumor cell killing by Akt inhibitors are substantially increased by chloroquine.
    Bioorg Med Chem. 2008 Sep 1;16(17):7888-93 PMID: 18691894
  21. Discovery and evaluation of inhibitors of human sphingosine kinase.
    Cancer Res. 2003 Sep 15;63(18):5962-9 PMID: 14522923
  22. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1.
    J Biol Chem. 2004 Apr 30;279(18):18384-91 PMID: 14970205
  23. Pro-caspase-8 is predominantly localized in mitochondria and released into cytoplasm upon apoptotic stimulation.
    J Biol Chem. 2001 Mar 16;276(11):8079-86 PMID: 11102441
  24. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1.
    Nat Cell Biol. 2010 Mar;12(3):213-23 PMID: 20173742
  25. The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agents-induced autophagy in cancer cells.
    Oncogene. 2009 Feb 12;28(6):886-98 PMID: 19060920
  26. Conversation between apoptosis and autophagy: "Is it your turn or mine?".
    Apoptosis. 2011 Apr;16(4):321-33 PMID: 21404107
  27. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series.
    EMBO Rep. 2008 Sep;9(9):859-64 PMID: 18704115
  28. Sphingosine kinase expression regulates apoptosis and caspase activation in PC12 cells.
    J Neurochem. 2001 Mar;76(5):1573-84 PMID: 11238741
  29. Chloroquine-mediated radiosensitization is due to the destabilization of the lysosomal membrane and subsequent induction of cell death by necrosis.
    Radiat Res. 2005 Sep;164(3):250-7 PMID: 16137197
  30. Loss of Bif-1 suppresses Bax/Bak conformational change and mitochondrial apoptosis.
    Mol Cell Biol. 2005 Nov;25(21):9369-82 PMID: 16227588
  31. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy.
    Oncogene. 2006 Aug 7;25(34):4798-811 PMID: 16892092
  32. p62 at the crossroads of autophagy, apoptosis, and cancer.
    Cell. 2009 Jun 12;137(6):1001-4 PMID: 19524504
  33. Development of a sphingosine kinase 1 specific small-molecule inhibitor.
    Bioorg Med Chem Lett. 2010 Dec 15;20(24):7498-502 PMID: 21050755
  34. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy.
    J Biol Chem. 2009 Jan 30;284(5):2719-2728 PMID: 19029119
  35. Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL.
    Cell Death Differ. 2010 Feb;17(2):268-77 PMID: 19713971
  36. Autophagy fights disease through cellular self-digestion.
    Nature. 2008 Feb 28;451(7182):1069-75 PMID: 18305538
  37. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice.
    Mol Biol Cell. 2008 Nov;19(11):4762-75 PMID: 18768753
  38. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes.
    Autophagy. 2008 Feb;4(2):151-75 PMID: 18188003
  39. Antitumor activity of sphingosine kinase inhibitors.
    J Pharmacol Exp Ther. 2006 Aug;318(2):596-603 PMID: 16632640
  40. Overcoming MDR-associated chemoresistance in HL-60 acute myeloid leukemia cells by targeting sphingosine kinase-1.
    Leukemia. 2006 Jan;20(1):95-102 PMID: 16281067
  41. Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHalpha1) death signal.
    J Biol Chem. 1998 Feb 20;273(8):4345-9 PMID: 9468483
  42. Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy: association with sequestosome 1/p62.
    J Biol Chem. 2011 Jun 24;286(25):22426-40 PMID: 21536669
  43. Self-eating and self-killing: crosstalk between autophagy and apoptosis.
    Nat Rev Mol Cell Biol. 2007 Sep;8(9):741-52 PMID: 17717517
  44. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling.
    J Biol Chem. 2002 Mar 8;277(10):7996-8003 PMID: 11777919
  45. Life and death by death receptors.
    FASEB J. 2009 Jun;23(6):1625-37 PMID: 19141537
  46. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy.
    J Biol Chem. 2007 Aug 17;282(33):24131-45 PMID: 17580304
  47. SRC directly phosphorylates Bif-1 and prevents its interaction with Bax and the initiation of anoikis.
    J Biol Chem. 2008 Jul 4;283(27):19112-8 PMID: 18474606
  48. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis.
    Nat Cell Biol. 2006 Oct;8(10):1124-32 PMID: 16998475
  49. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death.
    J Cell Biol. 2005 Nov 21;171(4):603-14 PMID: 16286508
  50. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling.
    Cell. 2009 May 15;137(4):721-35 PMID: 19427028
  51. Caspases in apoptosis and beyond.
    Oncogene. 2008 Oct 20;27(48):6194-206 PMID: 18931687
  52. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure.
    Mol Biol Cell. 2008 Nov;19(11):4651-9 PMID: 18768752
  53. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria.
    Cell Death Dis. 2010;1:e18 PMID: 21364619
  54. A novel sphingosine kinase inhibitor induces autophagy in tumor cells.
    J Pharmacol Exp Ther. 2010 May;333(2):454-64 PMID: 20179157
  55. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis.
    Nat Cell Biol. 2007 Oct;9(10):1142-51 PMID: 17891140
  56. Exploiting different ways to die.
    Genes Dev. 2004 Jun 1;18(11):1223-6 PMID: 15175258
  57. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy.
    Mol Biol Cell. 2008 May;19(5):2092-100 PMID: 18321988
  58. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death.
    Cell. 1996 Jun 14;85(6):803-15 PMID: 8681376
  59. Caspases: pharmacological manipulation of cell death.
    J Clin Invest. 2005 Oct;115(10):2665-72 PMID: 16200200
  60. Therapy of glioblastoma multiforme improved by the antimutagenic chloroquine.
    Neurosurg Focus. 2003 Feb 15;14(2):e3 PMID: 15727424
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2012-04-06
Epub
2012-00-23
Pages
12455-68
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3320995
Subset
IM
Grants
NCI NIH HHS · R01 CA082197 · United States
NCI NIH HHS · R01 CA129682 · United States
NCI NIH HHS · CA82197 · United States
NCI NIH HHS · CA129682 · 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