Home LiteratureArticle Details
PMID: 19109422 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Autophagy provides nutrients but can lead to Chop-dependent induction of Bim to sensitize growth factor-deprived cells to apoptosis.

Molecular biology of the cell ·Vol. 20 ·No. 4 ·2009-02-00 ·Pages 1180-91

Altman BJ, Wofford JA, Zhao Y, Coloff JL, Ferguson EC, Wieman HL, Day AE, Ilkayeva O, Rathmell JC

Abstract

Tissue homeostasis is controlled by the availability of growth factors, which sustain exogenous nutrient uptake and prevent apoptosis. Although autophagy can provide an alternate intracellular nutrient source to support essential basal metabolism of apoptosis-resistant growth factor-withdrawn cells, antiapoptotic Bcl-2 family proteins can suppress autophagy in some settings. Thus, the role of autophagy and interactions between autophagy and apoptosis in growth factor-withdrawn cells expressing Bcl-2 or Bcl-xL were unclear. Here we show autophagy was rapidly induced in hematopoietic cells upon growth factor withdrawal regardless of Bcl-2 or Bcl-xL expression and led to increased mitochondrial lipid oxidation. Deficiency in autophagy-essential gene expression, however, did not lead to metabolic catastrophe and rapid death of growth factor-deprived cells. Rather, inhibition of autophagy enhanced survival of cells with moderate Bcl-2 expression for greater than 1 wk, indicating that autophagy promoted cell death in this time frame. Cell death was not autophagic, but apoptotic, and relied on Chop-dependent induction of the proapoptotic Bcl-2 family protein Bim. Therefore, although ultimately important, autophagy-derived nutrients appear initially nonessential after growth factor withdrawal. Instead, autophagy promotes tissue homeostasis by sensitizing cells to apoptosis to ensure only the most apoptosis-resistant cells survive long-term using autophagy-derived nutrients when growth factor deprived.

MeSH Terms
Animals Apoptosis Apoptosis Regulatory Proteins/metabolism Autophagy Bcl-2-Like Protein 11 Fatty Acids/metabolism Glucose/metabolism Humans Intercellular Signaling Peptides and Proteins/deficiency Membrane Proteins/metabolism Mice Proto-Oncogene Proteins/metabolism Rats Transcription Factor CHOP/metabolism Up-Regulation bcl-X Protein/metabolism
Chemicals
Apoptosis Regulatory Proteins BCL2L11 protein, human Bcl-2-Like Protein 11 Bcl2l11 protein, mouse Bcl2l11 protein, rat Fatty Acids Intercellular Signaling Peptides and Proteins Membrane Proteins Proto-Oncogene Proteins bcl-X Protein Transcription Factor CHOP Glucose
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Altman Brian J
Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, NC 27710, USA.
Wofford Jessica A
Zhao Yuxing
Coloff Jonathan L
Ferguson Emily C
Wieman Heather L
Day Amanda E
Ilkayeva Olga
Rathmell Jeffrey C
References (48)
48 references, click to expand
  1. 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
  2. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8.
    Science. 2004 Jun 4;304(5676):1500-2 PMID: 15131264
  3. Steroid regulation of autophagic programmed cell death during development.
    Development. 2001 Apr;128(8):1443-55 PMID: 11262243
  4. Cytokines direct the regulation of Bim mRNA stability by heat-shock cognate protein 70.
    Mol Cell. 2007 Jan 12;25(1):99-112 PMID: 17218274
  5. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1.
    EMBO J. 2007 May 16;26(10):2527-39 PMID: 17446862
  6. Autophagy occurs upstream or parallel to the apoptosome during histolytic cell death.
    Development. 2006 Apr;133(8):1457-65 PMID: 16540507
  7. Involvement of up-regulation of PUMA in non-steroidal anti-inflammatory drug-induced apoptosis.
    Biochem Biophys Res Commun. 2007 May 11;356(3):711-7 PMID: 17368424
  8. Induction of autophagy during extracellular matrix detachment promotes cell survival.
    Mol Biol Cell. 2008 Mar;19(3):797-806 PMID: 18094039
  9. Chaperone-mediated autophagy.
    Autophagy. 2007 Jul-Aug;3(4):295-9 PMID: 17404494
  10. Metabolic regulation of oocyte cell death through the CaMKII-mediated phosphorylation of caspase-2.
    Cell. 2005 Oct 7;123(1):89-103 PMID: 16213215
  11. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium.
    Cell Death Differ. 2007 Sep;14(9):1576-82 PMID: 17612585
  12. Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus.
    J Biol Chem. 2008 Feb 22;283(8):4766-77 PMID: 18073215
  13. Glycogen synthase kinase 3alpha and 3beta mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1.
    Mol Cell Biol. 2007 Jun;27(12):4328-39 PMID: 17371841
  14. Roles of CHOP/GADD153 in endoplasmic reticulum stress.
    Cell Death Differ. 2004 Apr;11(4):381-9 PMID: 14685163
  15. Growth factor regulation of autophagy and cell survival in the absence of apoptosis.
    Cell. 2005 Jan 28;120(2):237-48 PMID: 15680329
  16. Autophagy gene-dependent clearance of apoptotic cells during embryonic development.
    Cell. 2007 Mar 9;128(5):931-46 PMID: 17350577
  17. An autophagic mechanism is involved in apoptotic death of rat striatal neurons induced by the non-N-methyl-D-aspartate receptor agonist kainic acid.
    Autophagy. 2008 Feb;4(2):214-26 PMID: 18094625
  18. ER stress triggers apoptosis by activating BH3-only protein Bim.
    Cell. 2007 Jun 29;129(7):1337-49 PMID: 17604722
  19. Autophagy in the pathogenesis of disease.
    Cell. 2008 Jan 11;132(1):27-42 PMID: 18191218
  20. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy.
    Mol Biol Cell. 2008 May;19(5):2179-92 PMID: 18337468
  21. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity.
    Science. 1999 Nov 26;286(5445):1735-8 PMID: 10576740
  22. BCL-2 in the crosshairs: tipping the balance of life and death.
    Cell Death Differ. 2006 Aug;13(8):1339-50 PMID: 16763614
  23. The phosphatidylinositol 3-Kinase AKT pathway in human cancer.
    Nat Rev Cancer. 2002 Jul;2(7):489-501 PMID: 12094235
  24. In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability.
    Mol Cell. 2000 Sep;6(3):683-92 PMID: 11030347
  25. Social controls on cell survival and cell death.
    Nature. 1992 Apr 2;356(6368):397-400 PMID: 1557121
  26. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation.
    Cell. 2007 Jun 1;129(5):983-97 PMID: 17540177
  27. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis.
    Cancer Cell. 2006 Jul;10(1):51-64 PMID: 16843265
  28. Autophagy in metazoans: cell survival in the land of plenty.
    Nat Rev Mol Cell Biol. 2005 Jun;6(6):439-48 PMID: 15928708
  29. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size.
    FEBS Lett. 2006 May 15;580(11):2623-9 PMID: 16647067
  30. Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein.
    J Biol Chem. 2007 Apr 27;282(17):13123-32 PMID: 17337444
  31. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy.
    Cell. 2005 Sep 23;122(6):927-39 PMID: 16179260
  32. Hepatic expression of malonyl-CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance.
    Nat Med. 2004 Mar;10(3):268-74 PMID: 14770177
  33. Tandem mass spectrometry: a new method for acylcarnitine profiling with potential for neonatal screening for inborn errors of metabolism.
    J Inherit Metab Dis. 1990;13(3):321-4 PMID: 2122093
  34. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction.
    J Exp Med. 2006 Dec 25;203(13):2939-51 PMID: 17178918
  35. Maturation of autophagic vacuoles in Mammalian cells.
    Autophagy. 2005 Apr;1(1):1-10 PMID: 16874026
  36. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis.
    Nat Cell Biol. 2006 Oct;8(10):1124-32 PMID: 16998475
  37. Apoptosis inhibition by Bcl-2 gives way to autophagy in glucocorticoid-treated lymphocytes.
    Autophagy. 2008 Jul;4(5):612-20 PMID: 18362516
  38. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG.
    Nat Cell Biol. 2006 Jul;8(7):688-99 PMID: 16799551
  39. Autophagic death of adult hippocampal neural stem cells following insulin withdrawal.
    Stem Cells. 2008 Oct;26(10):2602-10 PMID: 18653772
  40. Autophagy delays apoptotic death in breast cancer cells following DNA damage.
    Cell Death Differ. 2007 Mar;14(3):500-10 PMID: 16990848
  41. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
    EMBO J. 2000 Nov 1;19(21):5720-8 PMID: 11060023
  42. Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology.
    J Biol Chem. 2001 Apr 13;276(15):12041-8 PMID: 11278698
  43. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking.
    Mol Biol Cell. 2007 Apr;18(4):1437-46 PMID: 17301289
  44. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor.
    Genes Dev. 2003 Aug 1;17(15):1841-54 PMID: 12869584
  45. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death.
    Curr Biol. 2007 Jan 9;17(1):1-11 PMID: 17208179
  46. Another way to die: autophagic programmed cell death.
    Cell Death Differ. 2005 Nov;12 Suppl 2:1528-34 PMID: 16247500
  47. Role of autophagy in cancer.
    Nat Rev Cancer. 2007 Dec;7(12):961-7 PMID: 17972889
  48. LC3 conjugation system in mammalian autophagy.
    Int J Biochem Cell Biol. 2004 Dec;36(12):2503-18 PMID: 15325588
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
Published
2009-02-00
Epub
2008-00-24
Pages
1180-91
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2642748
Subset
IM
Grants
NCI NIH HHS · R01 CA123350 · United States
NCI NIH HHS · R01 CA123350-03 · 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