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PMID: 18593912 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Genomic and proteomic analysis reveals a threshold level of MYC required for tumor maintenance.

Cancer research ·Vol. 68 ·No. 13 ·2008-07-01 ·Pages 5132-42

Shachaf CM, Gentles AJ, Elchuri S, Sahoo D, Soen Y, Sharpe O, Perez OD, Chang M, Mitchel D, Robinson WH, Dill D, Nolan GP, Plevritis SK, Felsher DW

Abstract

MYC overexpression has been implicated in the pathogenesis of most types of human cancers. MYC is likely to contribute to tumorigenesis by its effects on global gene expression. Previously, we have shown that the loss of MYC overexpression is sufficient to reverse tumorigenesis. Here, we show that there is a precise threshold level of MYC expression required for maintaining the tumor phenotype, whereupon there is a switch from a gene expression program of proliferation to a state of proliferative arrest and apoptosis. Oligonucleotide microarray analysis and quantitative PCR were used to identify changes in expression in 3,921 genes, of which 2,348 were down-regulated and 1,573 were up-regulated. Critical changes in gene expression occurred at or near the MYC threshold, including genes implicated in the regulation of the G(1)-S and G(2)-M cell cycle checkpoints and death receptor/apoptosis signaling. Using two-dimensional protein analysis followed by mass spectrometry, phospho-flow fluorescence-activated cell sorting, and antibody arrays, we also identified changes at the protein level that contributed to MYC-dependent tumor regression. Proteins involved in mRNA translation decreased below threshold levels of MYC. Thus, at the MYC threshold, there is a loss of its ability to maintain tumorigenesis, with associated shifts in gene and protein expression that reestablish cell cycle checkpoints, halt protein translation, and promote apoptosis.

MeSH Terms
Animals Apoptosis/genetics Cell Cycle/genetics Cell Line, Tumor Cluster Analysis Disease Progression Gene Expression Profiling Gene Expression Regulation, Neoplastic Gene Regulatory Networks Genomics Mice Mice, Transgenic Neoplasms/genetics,metabolism,pathology Oligonucleotide Array Sequence Analysis Proteomics Proto-Oncogene Proteins c-myc/antagonists & inhibitors,genetics,metabolism Tumor Burden
Chemicals
MYC protein, human Proto-Oncogene Proteins c-myc
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Shachaf Catherine M
Department of Medicine and Pathology, Division of Medical Oncology, Stanford University School of Medicine, Stanford University, Stanford, California 94305, USA.
Gentles Andrew J
Elchuri Sailaja
Sahoo Debashis
Soen Yoav
Sharpe Orr
Perez Omar D
Chang Maria
Mitchel Dennis
Robinson William H
Dill David
Nolan Garry P
Plevritis Sylvia K
Felsher Dean W
References (39)
39 references, click to expand
  1. High-throughput tissue microarray analysis of c-myc activation in chronic liver diseases and hepatocellular carcinoma.
    Hum Pathol. 2004 Nov;35(11):1324-31 PMID: 15668888
  2. Single cell profiling of potentiated phospho-protein networks in cancer cells.
    Cell. 2004 Jul 23;118(2):217-28 PMID: 15260991
  3. Cellular senescence is an important mechanism of tumor regression upon c-Myc inactivation.
    Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13028-33 PMID: 17664422
  4. Development of a real-time reverse transcription polymerase chain reaction assay for c-myc expression that allows the identification of a subset of c-myc+ diffuse large B-cell lymphoma.
    Lab Invest. 2003 Feb;83(2):143-52 PMID: 12594230
  5. Differential binding of c-Myc and Max to nucleosomal DNA.
    Mol Cell Biol. 1994 Jun;14(6):4097-107 PMID: 8196648
  6. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets.
    Genome Biol. 2003;4(10):R69 PMID: 14519204
  7. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8164-9 PMID: 12808131
  8. Cancer revoked: oncogenes as therapeutic targets.
    Nat Rev Cancer. 2003 May;3(5):375-80 PMID: 12724735
  9. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  10. Reversible tumorigenesis by MYC in hematopoietic lineages.
    Mol Cell. 1999 Aug;4(2):199-207 PMID: 10488335
  11. Characterization of the c-MYC-regulated transcriptome by SAGE: identification and analysis of c-MYC target genes.
    Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6274-9 PMID: 11983916
  12. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network.
    Genes Dev. 2003 May 1;17(9):1101-14 PMID: 12695332
  13. Myc-binding-site recognition in the human genome is determined by chromatin context.
    Nat Cell Biol. 2006 Jul;8(7):764-70 PMID: 16767079
  14. Sustained loss of a neoplastic phenotype by brief inactivation of MYC.
    Science. 2002 Jul 5;297(5578):102-4 PMID: 12098700
  15. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth.
    Proc Natl Acad Sci U S A. 2006 Nov 28;103(48):18261-6 PMID: 17114293
  16. Reversible lymphomagenesis in conditionally c-MYC expressing mice.
    Int J Cancer. 2004 Jun 20;110(3):336-42 PMID: 15095297
  17. Inhibition of HMGcoA reductase by atorvastatin prevents and reverses MYC-induced lymphomagenesis.
    Blood. 2007 Oct 1;110(7):2674-84 PMID: 17622571
  18. Identification of c-myc responsive genes using rat cDNA microarray.
    Cancer Res. 2000 Nov 1;60(21):5922-8 PMID: 11085504
  19. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development.
    Nat Cell Biol. 2005 Mar;7(3):295-302 PMID: 15723055
  20. Reversible kinetic analysis of Myc targets in vivo provides novel insights into Myc-mediated tumorigenesis.
    Cancer Res. 2006 May 1;66(9):4591-601 PMID: 16651409
  21. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression.
    Cell. 2002 May 3;109(3):321-34 PMID: 12015982
  22. Identifying genes regulated in a Myc-dependent manner.
    J Biol Chem. 2002 Oct 4;277(40):36921-30 PMID: 12145275
  23. c-MYC induces mammary tumorigenesis by means of a preferred pathway involving spontaneous Kras2 mutations.
    Nat Med. 2001 Feb;7(2):235-9 PMID: 11175856
  24. Brief inactivation of c-Myc is not sufficient for sustained regression of c-Myc-induced tumours of pancreatic islets and skin epidermis.
    BMC Biol. 2004 Dec 21;2:26 PMID: 15613240
  25. Extracting binary signals from microarray time-course data.
    Nucleic Acids Res. 2007;35(11):3705-12 PMID: 17517782
  26. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer.
    Nature. 2004 Oct 28;431(7012):1112-7 PMID: 15475948
  27. Transcriptional regulation and transformation by Myc proteins.
    Nat Rev Mol Cell Biol. 2005 Aug;6(8):635-45 PMID: 16064138
  28. Analysis of protein phosphorylation and cellular signaling events by flow cytometry: techniques and clinical applications.
    Clin Immunol. 2004 Mar;110(3):206-21 PMID: 15047199
  29. Analysis of gene expression during myc oncogene-induced lymphomagenesis in the bursa of Fabricius.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6378-83 PMID: 11353853
  30. Flow cytometric analysis of kinase signaling cascades.
    Methods Mol Biol. 2004;263:67-94 PMID: 14976361
  31. Global mapping of c-Myc binding sites and target gene networks in human B cells.
    Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17834-9 PMID: 17093053
  32. Cell cycle regulation of E2F site occupation in vivo.
    Science. 1996 Mar 15;271(5255):1595-7 PMID: 8599118
  33. Involvement of c-myc-regulated genes in hepatocellular carcinoma related to genotype-C hepatitis B virus.
    J Cancer Res Clin Oncol. 2006 Jul;132(7):473-81 PMID: 16703398
  34. Gene expression phenotypic models that predict the activity of oncogenic pathways.
    Nat Genet. 2003 Jun;34(2):226-30 PMID: 12754511
  35. Myc influences global chromatin structure.
    EMBO J. 2006 Jun 21;25(12):2723-34 PMID: 16724113
  36. The c-Myc target gene network.
    Semin Cancer Biol. 2006 Aug;16(4):253-64 PMID: 16904903
  37. Myc-driven murine prostate cancer shares molecular features with human prostate tumors.
    Cancer Cell. 2003 Sep;4(3):223-38 PMID: 14522256
  38. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I.
    Nat Cell Biol. 2005 Mar;7(3):311-8 PMID: 15723054
  39. Genomic targets of the human c-Myc protein.
    Genes Dev. 2003 May 1;17(9):1115-29 PMID: 12695333
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2008-07-01
Pages
5132-42
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC4191850
Subset
IM
Grants
NCI NIH HHS · 3R01 CA89305-0351 · United States
NCI NIH HHS · 2P01 CA034233-22A1 · United States
NCI NIH HHS · R01 CA089305 · United States
NHLBI NIH HHS · N01-HV-28183 · United States
NCRR NIH HHS · 1U54RR022241 · United States
NIAID NIH HHS · R01 AI065824 · United States
NCI NIH HHS · R01 CA105102 · United States
NCI NIH HHS · 1R01 CA89305-01A1 · United States
NCI NIH HHS · 1R01 CA105102 · United States
NCI NIH HHS · 3U56 CA112973-03S1 · United States
NHLBI NIH HHS · N01HV28183 · United States
NCI NIH HHS · U56 CA112973 · United States
NCRR NIH HHS · U54 RR022241 · United States
NCI NIH HHS · P01 CA034233 · United States
NIAID NIH HHS · R01-AI065824 · United States
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