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Bcl-6 directly represses the gene program of the glycolysis pathway

Nature Immunology volume 15, pages 957–964 (2014)Cite this article

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Abstract

Despite the increasing knowledge of the molecular events that induce the glycolysis pathway in effector T cells, very little is known about the transcriptional mechanisms that dampen the glycolysis program in quiescent cell populations such as memory T cells. Here we found that the transcription factor Bcl-6 directly repressed genes encoding molecules involved in the glycolysis pathway, including Slc2a1, Slc2a3, Pkm and Hk2, in type 1 helper T cells (TH1 cells) exposed to low concentrations of interleukin 2 (IL-2). Thus, Bcl-6 had a role opposing the IL-2-sensitive glycolytic transcriptional program that the transcription factors c-Myc and HIF-1α promote in effector T cells. Additionally, the TH1 lineage–specifying factor T-bet functionally antagonized the Bcl-6-dependent repression of genes encoding molecules in the glycolysis pathway, which links the molecular balance of these two factors to regulation of the metabolic gene program.

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Figure 1: IL-2 signaling regulates the expression of genes encoding molecules in the glycolysis pathway in CD8+ TC1 cells.
Figure 2: Environmental IL-2 conditions regulate genes encoding molecules in the glycolysis pathway in CD4+ TH1 cells.
Figure 3: Bcl-6 directly represses genes encoding molecules in the glycolytic pathway.
Figure 4: Genomic distribution of Bcl-6, HIF-1α and c-Myc throughout the loci of genes encoding molecules in the glycolysis pathway.
Figure 5: The association of c-Myc and HIF-1α inversely correlates with binding of Bcl-6 at the promoters of genes encoding molecules involved in glycolysis.
Figure 6: The relative balance of T-bet and Bcl-6 regulates the expression of genes encoding molecules involved in the glycolysis pathway.
Figure 7: The carboxy-terminal domain of T-bet inhibits the Bcl-6-dependent repression of a subset of genes encoding molecules in the glycolysis pathway.

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Acknowledgements

We thank D. Rawlings (University of Washington) for human Ramos B cells; the preclinical repository of the National Cancer Institute for IL-2 and anti-IL-4; M. Wijaranakula for technical assistance; D. Chisolm for critical reading of the manuscript; and A. Ballesteros-Tato, B. Leon and T. Dadali-Abel for advice and assistance. Supported by the National Institute of Allergy and Infectious Diseases (AI061061 to A.S.W.) and the American Cancer Society (RSG-09-045-01-DDC to A.S.W.).

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Authors and Affiliations

  1. Department of Immunology, University of Washington, Seattle, Washington, USA

    Kenneth J Oestreich, Sarah E Gilbertson & Amy S Weinmann

  2. Virginia Tech Carilion Research Institute, Roanoke, Virginia, USA

    Kenneth J Oestreich, Kaitlin A Read & Paul W McDonald

  3. Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA

    Kenneth J Oestreich

  4. Department of Microbiology, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Kenneth P Hough, Veena Krishnamoorthy & Amy S Weinmann

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Contributions

K.J.O. and A.S.W. conceived of and designed the study, performed experiments, analyzed data and wrote the manuscript; and K.A.R., S.E.G., K.P.H., P.W.M. and V.K. performed experiments and analyzed data sets.

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Integrated supplementary information

Supplementary Figure 1 IL-2 signaling regulates the expression of genes encoding molecules in the glycolysis pathway in CD8+ TC1 cells.

Primary CD8+ T cells were cultured in TC1 polarizing conditions (IL-12 and anti-IL-4) with either high (white bars) or low (black bars) IL-2 conditions. Transcript abundance for the indicated genes was determined by quantitative RT-PCR using the BioRad PrimePCR system with primers specific to the indicated genes. Relative expression was normalized to the Rps18 control followed by comparison relative to the high IL-2 condition (set to 1). Three independent experiments were performed and the error bars represent the standard error of the mean (SEM). *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 2 IL-2 signaling regulates the expression of genes encoding molecules in the glycolysis pathway in CD8+ TC1 cells and CD4+ TH1 cells.

(a) Primary CD8+ or (b) CD4+ T cells were cultured in TC1/TH1 (IL-12 and anti-IL-4) conditions, with either high (white bars) or low (black bars) IL-2. Transcript amounts were determined as described in Supplementary Fig. 1. (a, b) Three independent experiments were performed and the error bars represent SEM. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 3 IL-2 signaling regulates the expression of genes encoding molecules in the glycolysis pathway in CD4+ TH1 cells.

Primary CD4+ T cells were cultured in TH1 polarizing conditions with either high (white bars) or low (black bars) IL-2. Transcript abundance was determined as indicated in Supplementary Fig. 1. Three independent experiments were performed and the error bars represent SEM. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 4 Bcl-6 and c-Myc–HIF-1α have inverse roles in regulating genes encoding molecules involved in glycolysis.

(a, b) EL4 T cells were co-transfected with (a) the P4ha2-promoter-reporter construct or (b) the pGL3-promoter vector in combination with either an empty vector control (white bars) or one expressing Bcl-6 (black bars). Luciferase promoter-reporter values were normalized to a renilla control and expressed relative to the control sample (set to 1). (c, d) ChIP experiments were performed with TH1 polarized cells maintained in either low (black bars) or high (white bars) IL-2 conditions. Chromatin samples were immunoprecipitated with antibodies specific to (c) Bcl-6, (d) c-Myc, HIF-1α, or (c, d) a nonspecific IgG antibody control. The indicated promoter regions were monitored by qPCR and the values for the precipitated samples were determined as described in Fig. 3c. Either (c) at least two, (d) three, (b) four, or (a) five independent experiments were performed with the error bars representing SEM. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 5 Bcl-6 expression represses the endogenous expression of genes encoding molecules in the glycolysis pathway in primary CD4+ TH1 cells maintained in conditions of a high concentration of IL-2.

Primary CD4+ T cells were cultured in TH1 conditions with high IL-2 concentrations. The cells were transfected with either a control (white bars) or Bcl-6 (black bars) expression vector. Cells were placed back in high IL-2 conditions and then RNA was harvested 24 h later. Relative expression was determined by quantitative RT-PCR analysis using the BioRad PrimePCR system customized with primers specific to the indicated genes. Samples were first normalized to the expression of Rps18 and then compared to the control sample (set to 1) in each independent experiment. Three independent experiments were performed and the error bars represent SEM. The P value for Egln3 was 0.0564 and was not quite statistically significant. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 6 Genomic distribution of Bcl-6, HIF-1α and c-Myc surrounding the loci of genes encoding molecules of the glycolysis pathway.

Shown are images derived from the UCSC genome browser displaying ChIP-seq peak tracks for BCOR, SMRT, three independent Bcl-6 experiments, HIF-1α in hypoxic conditions, and ENCODE c-Myc data as described in Fig. 4 and Methods.

Supplementary Figure 7 The relative balance between T-bet and Bcl-6 regulates the expression of genes encoding molecules in the glycolysis pathway.

(a-c) Primary wild-type (white bars) or Tbx21-/- (black bars) CD4+ T cells were cultured in TH1 polarizing conditions. Transcript expression for the indicated genes was determined as described in Fig. 6a. (d) Primary CD4+ T cells isolated from either wild-type (white bars) or Tbx21-/- (black bars) mice were treated as in (a). Chromatin samples were immunoprecipitated with an antibody specific to H3K9Ac or a nonspecific IgG antibody control and quantitated as described in Fig. 3c. (a-d) Three independent experiments were performed and error bars represent SEM. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 8 The C-terminal domain of T-bet inhibits the Bcl-6-dependent repression of genes encoding molecules in the glycolysis pathway.

(a) V5-epitope tagged expression constructs for T-bet(300-530), T-bet(120-331), or an empty vector control were transfected into A20 cells. Note that the T-bet(120-331) construct contains a point mutation in a required DNA-binding amino acid. An immunoblot analysis was performed using a V5 specific antibody to detect construct expression. (b) Untreated A20 cells or A20 cells treated with PMA and ionomycin (P/I) were harvested and lysates were subjected to an immunoblot analysis to assess Bcl-6 expression. Gapdh was monitored as a protein loading control. (c) Transfected samples from Fig. 7b were split into two independent wells and one was treated with P/I. Results are expressed as described in Fig. 7b. (d) A20 cells were co-transfected with the indicated promoter-reporter constructs and either an empty vector control (black bars), T-bet(120-331) (grey bars) or T-bet(300-530) (white bars). Luciferase promoter-reporter values were determined as described in Fig. 7b. (e) Ramos human B cells were transfected with either an empty vector control (black bars) or one expressing T-bet(300-530) (white bars) and stimulated with anti-CD40. Transcript abundance for the indicated endogenous genes were analyzed by quantitative RT-PCR and normalized to the Rps18 control. The graph represents the normalized expression in comparison to the control sample (set to 1). (a-e) Three independent experiments were performed and (c-e) the error bars represent SEM. *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

Supplementary Figure 9 The C-terminal domain of T-bet inhibits the Bcl-6-dependent repression of the endogenous expression of a subset of genes encoding molecules of the glycolysis pathway.

A20 murine B cells were transfected with either an empty vector control (black bars) or T-bet(300-530) (white bars). Transcript amounts for the indicated endogenous genes were analyzed by quantitative RT-PCR using PrimePCR plates and normalized to the Rps18 control. The sample expression was compared relative to the control sample (set to 1). Three independent experiments were performed and the error bars represent SEM. The P values for Slc2a1 and Tpi1 were less than 0.0549, but did not quite reach statistical significance (NS). *P < 0.05, **P < 0.01, ***P < 0.001 (unpaired Student’s t-test).

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Oestreich, K., Read, K., Gilbertson, S. et al. Bcl-6 directly represses the gene program of the glycolysis pathway. Nat Immunol 15, 957–964 (2014). https://doi.org/10.1038/ni.2985

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