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extended data figures source data nature portfolio journals permissions reprints nature portfolio privacy policy personal data data analysis data protection ser857ala-mutated gst–src-3-cid protein data author information authors advertising mcf7-mar-luc cells transduced ser857ala-mutated src-3-cid protein social media mda-mb-231 cells transduced pelp1/src-3-dependent regulation rat liver 6-phosphofructo-2-kinase/fructose-2 metabolic enzyme 6-phosphofructo-2-kinase/fructose-2 src-3-mediated transcriptional output mda-mb-231 cells treated mda-mb-231 cells cultured rnai-kinome library 24 kinome-library plates er-negative/recurrent tumours subscribe nature oncogenic coactivator src-3/aib1 gst–src-3-cid fragment lc-ms/ms-srm charcoal-stripped medium supplemented mda-mb-231 cells nature+ nature 548 nature 510 nature 556 nature estrogen receptor-α gst-fused src-3 fragments pser/thr antibody shows identify potential kinases oestrogen receptor-positive tumours transcription factor atf4 mammalian 6-phosphofructo-2-kinase/fructose-2 er+ breast cancer regulates transcriptional reprogramming ming-jer tsai & bert shrnas targeting pfkfb4 p-src-3-ser857 antibody src-3-dependent growth

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         description:Alterations in both cell metabolism and transcriptional programs are hallmarks of cancer that sustain rapid proliferation and metastasis 1 . However, the mechanisms that control the interaction between metabolic reprogramming and transcriptional regulation remain unclear. Here we show that the metabolic enzyme 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 4 (PFKFB4) regulates transcriptional reprogramming by activating the oncogenic steroid receptor coactivator-3 (SRC-3). We used a kinome-wide RNA interference-based screening method to identify potential kinases that modulate the intrinsic SRC-3 transcriptional response. PFKFB4, a regulatory enzyme that synthesizes a potent stimulator of glycolysis 2 , is found to be a robust stimulator of SRC-3 that coregulates oestrogen receptor. PFKFB4 phosphorylates SRC-3 at serine 857 and enhances its transcriptional activity, whereas either suppression of PFKFB4 or ectopic expression of a phosphorylation-deficient Ser857Ala mutant SRC-3 abolishes the SRC-3-mediated transcriptional output. Functionally, PFKFB4-driven SRC-3 activation drives glucose flux towards the pentose phosphate pathway and enables purine synthesis by transcriptionally upregulating the expression of the enzyme transketolase. In addition, the two enzymes adenosine monophosphate deaminase-1 (AMPD1) and xanthine dehydrogenase (XDH), which are involved in purine metabolism, were identified as SRC-3 targets that may or may not be directly involved in purine synthesis. Mechanistically, phosphorylation of SRC-3 at Ser857 increases its interaction with the transcription factor ATF4 by stabilizing the recruitment of SRC-3 and ATF4 to target gene promoters. Ablation of SRC-3 or PFKFB4 suppresses breast tumour growth in mice and prevents metastasis to the lung from an orthotopic setting, as does Ser857Ala-mutant SRC-3. PFKFB4 and phosphorylated SRC-3 levels are increased and correlate in oestrogen receptor-positive tumours, whereas, in patients with the basal subtype, PFKFB4 and SRC-3 drive a common protein signature that correlates with the poor survival of patients with breast cancer. These findings suggest that the Warburg pathway enzyme PFKFB4 acts as a molecular fulcrum that couples sugar metabolism to transcriptional activation by stimulating SRC-3 to promote aggressive metastatic tumours. The glycolytic enzyme PFKFB4 directly phosphorylates and regulates binding of the coactivator SRC-3 to ATF4 and thereby increases the transcriptional activity of this complex, leading to increased expression of metabolic genes, and enhancing tumour growth and metastasis.
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      name:Xiang H.-F. Zhang
      affiliation:
            name:Baylor College of Medicine
            address:
               name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
      name:Charles E. Foulds
      affiliation:
            name:Baylor College of Medicine
            address:
               name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
            name:Baylor College of Medicine
            address:
               name:Center for Precision Environmental Health, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
      name:Sophia Y. Tsai
      affiliation:
            name:Baylor College of Medicine
            address:
               name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
      name:Ming-Jer Tsai
      affiliation:
            name:Baylor College of Medicine
            address:
               name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
      name:Bert W. O’Malley
      affiliation:
            name:Baylor College of Medicine
            address:
               name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
               type:PostalAddress
            type:Organization
      email:[email protected]
PostalAddress:
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Cell Stress Biology, Roswell Park Comprehensive Cancer Center, Buffalo, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Verna & Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Verna & Marrs McLean Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Center for Precision Environmental Health, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
      name:Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, USA
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