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PMID: 19920251 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth.

Science signaling ·Vol. 2 ·No. 97 ·2009-11-17 ·Pages ra73

Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, Dong S, Lonial S, Wang X, Chen GZ, Xie J, Gu TL, Polakiewicz RD, Roesel JL, Boggon TJ, Khuri FR, Gilliland DG, Cantley LC, Kaufman J, Chen J

Abstract

The Warburg effect describes a pro-oncogenic metabolism switch such that cancer cells take up more glucose than normal tissue and favor incomplete oxidation of glucose even in the presence of oxygen. To better understand how tyrosine kinase signaling, which is commonly increased in tumors, regulates the Warburg effect, we performed phosphoproteomic studies. We found that oncogenic forms of fibroblast growth factor receptor type 1 inhibit the pyruvate kinase M2 (PKM2) isoform by direct phosphorylation of PKM2 tyrosine residue 105 (Y(105)). This inhibits the formation of active, tetrameric PKM2 by disrupting binding of the PKM2 cofactor fructose-1,6-bisphosphate. Furthermore, we found that phosphorylation of PKM2 Y(105) is common in human cancers. The presence of a PKM2 mutant in which phenylalanine is substituted for Y(105) (Y105F) in cancer cells leads to decreased cell proliferation under hypoxic conditions, increased oxidative phosphorylation with reduced lactate production, and reduced tumor growth in xenografts in nude mice. Our findings suggest that tyrosine phosphorylation regulates PKM2 to provide a metabolic advantage to tumor cells, thereby promoting tumor growth.

MeSH Terms
Adenosine Triphosphate/metabolism Animals Cell Line Cell Line, Tumor Cell Proliferation Fructosediphosphates/metabolism Glucose/metabolism Glycolysis/physiology Humans Immunoblotting K562 Cells Male Mice Mice, Nude Mutation Neoplasms/genetics,metabolism,pathology Neoplasms, Experimental/genetics,metabolism,pathology Oxygen Consumption Phosphorylation Proteomics/methods Pyruvate Kinase/genetics,metabolism Receptor, Fibroblast Growth Factor, Type 1/genetics,metabolism Transplantation, Heterologous Tumor Burden Tyrosine/metabolism
Chemicals
Fructosediphosphates Tyrosine Adenosine Triphosphate Pyruvate Kinase Receptor, Fibroblast Growth Factor, Type 1 Glucose fructose-1,6-diphosphate
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Hitosugi Taro
Winship Cancer Institute, Emory University School of Medicine, Atlanta, GA 30322, USA.
Kang Sumin
Vander Heiden Matthew G
Chung Tae-Wook
Elf Shannon
Lythgoe Katherine
Dong Shaozhong
Lonial Sagar
Wang Xu
Chen Georgia Z
Xie Jianxin
Gu Ting-Lei
Polakiewicz Roberto D
Roesel Johannes L
Boggon Titus J
Khuri Fadlo R
Gilliland D Gary
Cantley Lewis C
Kaufman Jonathan
Chen Jing
References (25)
25 references, click to expand
  1. Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia.
    Blood. 2006 Dec 15;108(13):4202-4 PMID: 16946300
  2. Tumor-specific pyruvate kinase isoenzyme M2 involved in biochemical strategy of energy generation in neoplastic cells.
    Acta Biochim Pol. 1997;44(4):711-24 PMID: 9584851
  3. FGFR1 emerges as a potential therapeutic target for lobular breast carcinomas.
    Clin Cancer Res. 2006 Nov 15;12(22):6652-62 PMID: 17121884
  4. Pyruvate kinase M2 is a phosphotyrosine-binding protein.
    Nature. 2008 Mar 13;452(7184):181-6 PMID: 18337815
  5. FGFR1 is fused with a novel zinc-finger gene, ZNF198, in the t(8;13) leukaemia/lymphoma syndrome.
    Nat Genet. 1998 Jan;18(1):84-7 PMID: 9425908
  6. PKC412 inhibits the zinc finger 198-fibroblast growth factor receptor 1 fusion tyrosine kinase and is active in treatment of stem cell myeloproliferative disorder.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14479-84 PMID: 15448205
  7. Modulation of M2-type pyruvate kinase activity by the cytoplasmic PML tumor suppressor protein.
    Genes Cells. 2008 Mar;13(3):245-54 PMID: 18298799
  8. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  9. Aberrant expression of type I fibroblast growth factor receptor in human pancreatic adenocarcinomas.
    Cancer Res. 1993 Oct 15;53(20):4741-4 PMID: 8402651
  10. The allosteric regulation of pyruvate kinase.
    FEBS Lett. 1996 Jun 24;389(1):15-9 PMID: 8682196
  11. Fibroblast growth factor receptor gene expression and immunoreactivity are elevated in human glioblastoma multiforme.
    Cancer Res. 1994 May 15;54(10):2794-9 PMID: 8168112
  12. Tumour M2-pyruvate kinase: a gastrointestinal cancer marker.
    Eur J Gastroenterol Hepatol. 2007 Mar;19(3):265-76 PMID: 17301655
  13. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth.
    Nature. 2008 Mar 13;452(7184):230-3 PMID: 18337823
  14. High-resolution analysis of chromosome rearrangements on 8p in breast, colon and pancreatic cancer reveals a complex pattern of loss, gain and translocation.
    Oncogene. 2006 Sep 14;25(41):5693-706 PMID: 16636668
  15. Expression of basic fibroblast growth factor, FGFR1 and FGFR2 in normal and malignant human breast, and comparison with other normal tissues.
    Br J Cancer. 1992 Aug;66(2):273-80 PMID: 1380281
  16. Current status of tumor M2 pyruvate kinase (tumor M2-PK) as a biomarker of gastrointestinal malignancy.
    Ann Surg Oncol. 2007 Oct;14(10):2714-20 PMID: 17602267
  17. Fibroblast growth factor (FGF) and FGF receptor-mediated autocrine signaling in non-small-cell lung cancer cells.
    Mol Pharmacol. 2009 Jan;75(1):196-207 PMID: 18849352
  18. Pyruvate kinase type M2: a crossroad in the tumor metabolome.
    Br J Nutr. 2002 Jan;87 Suppl 1:S23-9 PMID: 11895152
  19. ZNF198-FGFR1 transforming activity depends on a novel proline-rich ZNF198 oligomerization domain.
    Blood. 2000 Jul 15;96(2):699-704 PMID: 10887137
  20. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells.
    Nat Biotechnol. 2005 Jan;23(1):94-101 PMID: 15592455
  21. Pyruvate kinase type M2 and its role in tumor growth and spreading.
    Semin Cancer Biol. 2005 Aug;15(4):300-8 PMID: 15908230
  22. Hypoxia signalling controls metabolic demand.
    Curr Opin Cell Biol. 2007 Apr;19(2):223-9 PMID: 17303407
  23. Tumor cell metabolism: cancer's Achilles' heel.
    Cancer Cell. 2008 Jun;13(6):472-82 PMID: 18538731
  24. New structures of allosteric proteins revealing remarkable conformational changes.
    Curr Opin Struct Biol. 1996 Dec;6(6):824-9 PMID: 8994883
  25. Expression of FGF and FGF receptor genes in human breast cancer.
    Int J Cancer. 1995 Apr 10;61(2):170-6 PMID: 7705943
Article Info
Journal
Science signaling
Abbr.
Sci Signal
ISSN
1937-9145
Published
2009-11-17
Epub
2009-00-17
Pages
ra73
Language
English
Region
United States
NLM ID
101465400
PMCID
PMC2812789
Subset
IM
Grants
NCI NIH HHS · R01 CA120272-04 · United States
NCI NIH HHS · R01 CA120272-01 · United States
NCI NIH HHS · T32 CA009172 · United States
NCI NIH HHS · R01 CA120272-02 · United States
NCI NIH HHS · R01 CA120272-03 · United States
NCI NIH HHS · CA120272 · United States
NCI NIH HHS · R01 CA140515 · United States
NCI NIH HHS · R01 CA120272 · United States
NIGMS NIH HHS · R01 GM056203 · United States
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