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PMID: 24034250 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance.

Cell ·Vol. 154 ·No. 6 ·2013-09-12 ·Pages 1269-84

Wei Y, Zou Z, Becker N, Anderson M, Sumpter R, Xiao G, Kinch L, Koduru P, Christudass CS, Veltri RW, Grishin NV, Peyton M, Minna J, Bhagat G, Levine B

Abstract

Cell surface growth factor receptors couple environmental cues to the regulation of cytoplasmic homeostatic processes, including autophagy, and aberrant activation of such receptors is a common feature of human malignancies. Here, we defined the molecular basis by which the epidermal growth factor receptor (EGFR) tyrosine kinase regulates autophagy. Active EGFR binds the autophagy protein Beclin 1, leading to its multisite tyrosine phosphorylation, enhanced binding to inhibitors, and decreased Beclin 1-associated VPS34 kinase activity. EGFR tyrosine kinase inhibitor (TKI) therapy disrupts Beclin 1 tyrosine phosphorylation and binding to its inhibitors and restores autophagy in non-small-cell lung carcinoma (NSCLC) cells with a TKI-sensitive EGFR mutation. In NSCLC tumor xenografts, the expression of a tyrosine phosphomimetic Beclin 1 mutant leads to reduced autophagy, enhanced tumor growth, tumor dedifferentiation, and resistance to TKI therapy. Thus, oncogenic receptor tyrosine kinases directly regulate the core autophagy machinery, which may contribute to tumor progression and chemoresistance.

MeSH Terms
Animals Apoptosis Regulatory Proteins/genetics,metabolism Autophagy Beclin-1 Carcinoma, Non-Small-Cell Lung/drug therapy Cell Line, Tumor Drug Resistance, Neoplasm ErbB Receptors/genetics,metabolism Heterografts Humans Lung Neoplasms/drug therapy Membrane Proteins/genetics,metabolism Mice Mice, Inbred NOD Mice, SCID Neoplasm Transplantation Phosphorylation
Chemicals
Apoptosis Regulatory Proteins BECN1 protein, human Beclin-1 Membrane Proteins EGFR protein, human ErbB Receptors
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Wei Yongjie
Center for Autophagy Research, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
Zou Zhongju
Becker Nils
Anderson Matthew
Sumpter Rhea
Xiao Guanghua
Kinch Lisa
Koduru Prasad
Christudass Christhunesa S
Veltri Robert W
Grishin Nick V
Peyton Michael
Minna John
Bhagat Govind
Levine Beth
References (25)
25 references, click to expand
  1. Abnormalities of the TITF-1 lineage-specific oncogene in NSCLC: implications in lung cancer pathogenesis and prognosis.
    Clin Cancer Res. 2011 Apr 15;17(8):2434-43 PMID: 21257719
  2. Prognostic significance of thyroid transcription factor-1 expression in both early-stage conventional adenocarcinoma and bronchioloalveolar carcinoma of the lung.
    Hum Pathol. 2004 Jan;35(1):3-7 PMID: 14745718
  3. Principles and current strategies for targeting autophagy for cancer treatment.
    Clin Cancer Res. 2011 Feb 15;17(4):654-66 PMID: 21325294
  4. Cell signaling by receptor tyrosine kinases.
    Cell. 2010 Jun 25;141(7):1117-34 PMID: 20602996
  5. EGFR antagonists in cancer treatment.
    N Engl J Med. 2008 Mar 13;358(11):1160-74 PMID: 18337605
  6. Histopathologic characteristics of lung adenocarcinomas with epidermal growth factor receptor mutations in the International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society lung adenocarcinoma classification.
    Arch Pathol Lab Med. 2011 Oct;135(10):1329-34 PMID: 21970488
  7. Single amino-acid changes that confer constitutive activation of mTOR are discovered in human cancer.
    Oncogene. 2010 May 6;29(18):2746-52 PMID: 20190810
  8. Autophagy modulation as a potential therapeutic target for diverse diseases.
    Nat Rev Drug Discov. 2012 Sep;11(9):709-30 PMID: 22935804
  9. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation.
    Science. 2012 Nov 16;338(6109):956-9 PMID: 23112296
  10. Mitochondrially localized EGFR is independent of its endocytosis and associates with cell viability.
    Acta Biochim Biophys Sin (Shanghai). 2010 Nov;42(11):763-70 PMID: 20929928
  11. NCI series of cell lines: an historical perspective.
    J Cell Biochem Suppl. 1996;24:1-11 PMID: 8806089
  12. Combining an EGFR directed tyrosine kinase inhibitor with autophagy-inducing drugs: a beneficial strategy to combat non-small cell lung cancer.
    Cancer Lett. 2011 Nov 28;310(2):207-15 PMID: 21807458
  13. The Beclin 1 interactome.
    Curr Opin Cell Biol. 2010 Apr;22(2):140-9 PMID: 20097051
  14. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer.
    Nat Rev Cancer. 2010 Nov;10(11):760-74 PMID: 20966921
  15. Autophagy in the pathogenesis of disease.
    Cell. 2008 Jan 11;132(1):27-42 PMID: 18191218
  16. Immunohistochemical algorithm for differentiation of lung adenocarcinoma and squamous cell carcinoma based on large series of whole-tissue sections with validation in small specimens.
    Mod Pathol. 2011 Oct;24(10):1348-59 PMID: 21623384
  17. Laser capture microdissection and protein microarray analysis of human non-small cell lung cancer: differential epidermal growth factor receptor (EGPR) phosphorylation events associated with mutated EGFR compared with wild type.
    Mol Cell Proteomics. 2008 Oct;7(10):1902-24 PMID: 18687633
  18. Autophagy signaling and the cogwheels of cancer.
    Autophagy. 2006 Apr-Jun;2(2):67-73 PMID: 16874041
  19. Receptors for epidermal growth factor and other polypeptide mitogens.
    Annu Rev Biochem. 1987;56:881-914 PMID: 3039909
  20. EGFR tyrosine kinase inhibitors activate autophagy as a cytoprotective response in human lung cancer cells.
    PLoS One. 2011;6(6):e18691 PMID: 21655094
  21. Methods in mammalian autophagy research.
    Cell. 2010 Feb 5;140(3):313-26 PMID: 20144757
  22. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib.
    N Engl J Med. 2004 May 20;350(21):2129-39 PMID: 15118073
  23. EGFR tyrosine kinase inhibition induces autophagy in cancer cells.
    Cancer Biol Ther. 2012 Dec;13(14):1417-24 PMID: 22954701
  24. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages.
    Nat Cell Biol. 2009 Apr;11(4):385-96 PMID: 19270696
  25. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival.
    Mol Cell Biol. 2002 Oct;22(20):7279-90 PMID: 12242303
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2013-09-12
Pages
1269-84
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3917713
Subset
IM
Grants
PHS HHS · R01 109618 · United States
NCI NIH HHS · R01 CA084254 · United States
NCI NIH HHS · P50CA70907 · United States
NCI NIH HHS · P50 CA070907 · United States
NCI NIH HHS · R01 CA109618 · United States
PHS HHS · R01 84254 · United States
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