5.9
CiteScore
5.9
Impact Factor
Volume 46 Issue 12
Dec.  2019
Turn off MathJax
Article Contents

Glycolysis regulates gene expression by promoting the crosstalk between H3K4 trimethylation and H3K14 acetylation in Saccharomyces cerevisiae

doi: 10.1016/j.jgg.2019.11.007
More Information
  • Corresponding author: E-mail address: xhzhang0072@hubu.edu.cn (Xianhua Zhang); E-mail address: yuxilan@hubu.edu.cn (Xilan Yu); E-mail address: shl@hubu.edu.cn (Shanshan Li)
  • Received Date: 2019-08-17
  • Accepted Date: 2019-11-25
  • Rev Recd Date: 2019-11-18
  • Available Online: 2019-12-11
  • Publish Date: 2019-12-20
  • Cells need to coordinate gene expression with their metabolic states to maintain cell homeostasis and growth. However, how cells transduce nutrient availability to appropriate gene expression response via histone modifications remains largely unknown. Here, we report that glucose specifically induces histone H3K4 trimethylation (H3K4me3), an evolutionarily conserved histone covalent modification associated with active gene transcription, and that glycolytic enzymes and metabolites are required for this induction. Although glycolysis supplies S-adenosylmethionine for histone methyltransferase Set1 to catalyze H3K4me3, glucose induces H3K4me3 primarily by inhibiting histone demethylase Jhd2-catalyzed H3K4 demethylation. Glycolysis provides acetyl-CoA to stimulate histone acetyltransferase Gcn5 to acetylate H3K14, which then inhibits the binding of Jhd2 to chromatin to increase H3K4me3. By repressing Jhd2-mediated H3K4 demethylation, glycolytic enzymes regulate gene expression and cell survival during chronological aging. Thus, our results elucidate how cells reprogram their gene expression programs in response to glucose availability via histone modifications.
  • These authors contribute equally to this work.
  • loading
  • [1]
    Albers, E., Laize, V., Blomberg, A., Hohmann, S., Gustafsson, L., 2003. Ser3p (Yer081wp) and Ser33p (Yil074cp) are phosphoglycerate dehydrogenases in Saccharomyces cerevisiae. J. Biol. Chem. 278, 10264-10272.
    [2]
    Andersson, A.K., Ma, J., Wang, J., Chen, X., Gedman, A.L., Dang, J., Nakitandwe, J., Holmfeldt, L., Parker, M., Easton, J., Huether, R., Kriwacki, R., Rusch, M., Wu, G., Li, Y., Mulder, H., Raimondi, S., Pounds, S., Kang, G., Shi, L., Becksfort, J., Gupta, P., Payne-Turner, D., Vadodaria, B., Boggs, K., Yergeau, D., Manne, J., Song, G., Edmonson, M., Nagahawatte, P., Wei, L., Cheng, C., Pei, D., Sutton, R., Venn, N.C., Chetcuti, A., Rush, A., Catchpoole, D., Heldrup, J., Fioretos, T., Lu, C., Ding, L., Pui, C.H., Shurtleff, S., Mullighan, C.G., Mardis, E.R., Wilson, R.K., Gruber, T.A., Zhang, J., Downing, J.R., St. Jude Children's Research Hospital-Washington University Pediatric Cancer Genome, P., 2015. The landscape of somatic mutations in infant MLL-rearranged acute lymphoblastic leukemias. Nat. Genet. 47, 330-337.
    [3]
    Boukouris, A.E., Zervopoulos, S.D., Michelakis, E.D., 2016. Metabolic enzymes moonlighting in the nucleus: Metabolic regulation of gene transcription. Trends. Biochem. Sci. 41, 712.
    [4]
    Carey, B.W., Finley, L.W., Cross, J.R., Allis, C.D., Thompson, C.B., 2015. Intracellular alpha-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518, 413-416.
    [5]
    Christofk, H.R., Vander Heiden, M.G., Harris, M.H., Ramanathan, A., Gerszten, R.E., Wei, R., Fleming, M.D., Schreiber, S.L., Cantley, L.C., 2008. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233.
    [6]
    Conaway, R.C., 2018. Metabolic regulation of transcription and chromatin. Annu. Rev. Biochem. 87, 23-25.
    [7]
    Dong, L., Xu, C.W., 2004. Carbohydrates induce mono-ubiquitination of H2B in yeast. J. Biol. Chem. 279, 1577-1580.
    [8]
    Falcon, A.A., Chen, S., Wood, M.S., Aris, J.P., 2010. Acetyl-coenzyme A synthetase 2 is a nuclear protein required for replicative longevity in Saccharomyces cerevisiae. Mol. Cell. Biochem. 333, 99-108.
    [9]
    Fingerman, I.M., Wu, C.L., Wilson, B.D., Briggs, S.D., 2005. Global loss of Set1-mediated H3 Lys4 trimethylation is associated with silencing defects in Saccharomyces cerevisiae. J. Biol. Chem. 280, 28761-28765.
    [10]
    Friis, R.M., Wu, B.P., Reinke, S.N., Hockman, D.J., Sykes, B.D., Schultz, M.C., 2009. A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res. 37, 3969-3980.
    [11]
    Gillies, R.J., Robey, I., Gatenby, R.A., 2008. Causes and consequences of increased glucose metabolism of cancers. J. Nucl. Med. 49 Suppl 2, 24S-42S.
    [12]
    Grant, P.A., Eberharter, A., John, S., Cook, R.G., Turner, B.M., Workman, J.L., 1999. Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274, 5895-5900.
    [13]
    Herzig, S., Shaw, R.J., 2018. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat. Rev. Mol. Cell Biol. 19, 121-135.
    [14]
    Huang, J., Luo, Z., Ying, W., Cao, Q., Huang, H., Dong, J., Wu, Q., Zhao, Y., Qian, X., Dai, J., 2017. 2-Hydroxyisobutyrylation on histone H4K8 is regulated by glucose homeostasis in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 114, 8782-8787.
    [15]
    Keller, K.E., Doctor, Z.M., Dwyer, Z.W., Lee, Y.S., 2014. SAICAR induces protein kinase activity of PKM2 that is necessary for sustained proliferative signaling of cancer cells. Mol. Cell 53, 700-709.
    [16]
    Li, S., Shogren-Knaak, M.A., 2008. Cross-talk between histone H3 tails produces cooperative nucleosome acetylation. Proc. Natl. Acad. Sci. U. S. A. 105, 18243-18248.
    [17]
    Li, S., Swanson, S.K., Gogol, M., Florens, L., Washburn, M.P., Workman, J.L., Suganuma, T., 2015. Serine and SAM responsive complex SESAME regulates histone modification crosstalk by sensing cellular metabolism. Mol. Cell 60, 408-421.
    [18]
    Liang, G., Klose, R.J., Gardner, K.E., Zhang, Y., 2007. Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat. Struct. Mol. Biol. 14, 243-245.
    [19]
    Liu, X.S., Little, J.B., Yuan, Z.M., 2015. Glycolytic metabolism influences global chromatin structure. Oncotarget 6, 4214-4225.
    [20]
    Ma, R., Wu, Y., Zhai, Y., Hu, B., Ma, W., Yang, W., Yu, Q., Chen, Z., Workman, J.L., Yu, X., Li, S. (2019). Exogenous pyruvate represses histone gene expression and inhibits cancer cell proliferation via the NAMPT-NAD+-SIRT1 pathway. Nucleic Acids Res. 47:11132-11150.
    [21]
    Mei, Q., Xu, C., Gogol, M., Tang, J., Chen, W., Yu, X., Workman, J.L., Li, S., 2019. Set1-catalyzed H3K4 trimethylation antagonizes the HIR/Asf1/Rtt106 repressor complex to promote histone gene expression and chronological life span. Nucleic Acids Res. 47, 3434-3449.
    [22]
    Mnaimneh, S., Davierwala, A.P., Haynes, J., Moffat, J., Peng, W.T., Zhang, W., Yang, X., Pootoolal, J., Chua, G., Lopez, A., Trochesset, M., Morse, D., Krogan, N.J., Hiley, S.L., Li, Z., Morris, Q., Grigull, J., Mitsakakis, N., Roberts, C.J., Greenblatt, J.F., Boone, C., Kaiser, C.A., Andrews, B.J., Hughes, T.R., 2004. Exploration of essential gene functions via titratable promoter alleles. Cell 118, 31-44.
    [23]
    Nacev, B.A., Feng, L., Bagert, J.D., Lemiesz, A.E., Gao, J., Soshnev, A.A., Kundra, R., Schultz, N., Muir, T.W., Allis, C.D., 2019. The expanding landscape of 'oncohistone' mutations in human cancers. Nature 567, 473-478.
    [24]
    Nakanishi, S., Sanderson, B.W., Delventhal, K.M., Bradford, W.D., Staehling-Hampton, K., and Shilatifard, A. (2008). A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat. Struct. Mol. Biol. 15, 881-888.
    [25]
    Neumann, H., Hancock, S.M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen-Hughes, T., van Noort, J., Rhodes, D., Chin, J.W., 2009. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 36, 153-163.
    [26]
    Ng, H.H., Robert, F., Young, R.A., Struhl, K., 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709-719.
    [27]
    Orlandi, I., Coppola, D.P., Vai, M., 2014. Rewiring yeast acetate metabolism through MPC1 loss of function leads to mitochondrial damage and decreases chronological lifespan. Microb. Cell 1, 393-405.
    [28]
    Ramakrishnan, S., Pokhrel, S., Palani, S., Pflueger, C., Parnell, T.J., Cairns, B.R., Bhaskara, S., Chandrasekharan, M.B., 2016. Counteracting H3K4 methylation modulators Set1 and Jhd2 co-regulate chromatin dynamics and gene transcription. Nat. Commun. 7, 11949.
    [29]
    Ringel, A.E., Ryznar, R., Picariello, H., Huang, K.L., Lazarus, A.G., Holmes, S.G., 2013. Yeast Tdh3 (glyceraldehyde 3-phosphate dehydrogenase) is a Sir2-interacting factor that regulates transcriptional silencing and rDNA recombination. PLoS Genet. 9, e1003871.
    [30]
    Rusche, L.N., Kirchmaier, A.L., Rine, J., 2003. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu. Rev. Biochem. 72, 481-516.
    [31]
    Sadhu, M.J., Guan, Q., Li, F., Sales-Lee, J., Iavarone, A.T., Hammond, M.C., Cande, W.Z., Rine, J., 2013. Nutritional control of epigenetic processes in yeast and human cells. Genetics 195, 831-844.
    [32]
    Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J., Kouzarides, T., 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419, 407-411.
    [33]
    Shilatifard, A., 2012. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95.
    [34]
    Smolle, M., Workman, J.L., 2013. Transcription-associated histone modifications and cryptic transcription. Biochim. Biophys. Acta. 1829, 84-97.
    [35]
    Takahashi, H., McCaffery, J.M., Irizarry, R.A., Boeke, J.D., 2006. Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol. Cell 23, 207-217.
    [36]
    Thomas, D., Rothstein, R., Rosenberg, N., Surdin-Kerjan, Y., 1988. SAM2 encodes the second methionine S-adenosyl transferase in Saccharomyces cerevisiae: physiology and regulation of both enzymes. Mol. Cell. Biol. 8, 5132-5139.
    [37]
    van der Knaap, J.A., Verrijzer, C.P., 2016. Undercover: gene control by metabolites and metabolic enzymes. Genes Dev. 30, 2345-2369.
    [38]
    Vander Heiden, M.G., Cantley, L.C., Thompson, C.B., 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033.
    [39]
    Walter, D., Matter, A., Fahrenkrog, B., 2014. Loss of histone H3 methylation at lysine 4 triggers apoptosis in Saccharomyces cerevisiae. PLoS Genet. 10, e1004095.
    [40]
    Xu, H.H., Su, T., Xue, Y., 2016a. Histone H3 N-terminal acetylation sites especially K14 are important for rDNA silencing and aging. Sci. Rep. 6, 21900.
    [41]
    Xu, W., Wang, F., Yu, Z., Xin, F., 2016b. Epigenetics and cellular metabolism. Genet. Epigenet. 8, 43-51.
    [42]
    Yang, W., Xia, Y., Hawke, D., Li, X., Liang, J., Xing, D., Aldape, K., Hunter, T., Alfred Yung, W.K., Lu, Z., 2012. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 150, 685-696.
    [43]
    Yu, Q., Tong, C., Luo, M., Xue, X., Mei, Q., Ma, L., Yu, X., Mao, W., Kong, L., Yu, X., Li, S., 2017. Regulation of SESAME-mediated H3T11 phosphorylation by glycolytic enzymes and metabolites. PLoS One 12, e0175576.
    [44]
    Yu, X., Li, S., 2017. Non-metabolic functions of glycolytic enzymes in tumorigenesis. Oncogene 36, 2629-2636.
    [45]
    Yu, X., Ma, R., Wu, Y., Zhai, Y., Li, S., 2018. Reciprocal regulation of metabolic reprogramming and epigenetic modifications in cancer. Front. Genet. 9, 394.
    [46]
    Zhang, C.S., Hawley, S.A., Zong, Y., Li, M., Wang, Z., Gray, A., Ma, T., Cui, J., Feng, J.W., Zhu, M., Wu, Y.Q., Li, T.Y., Ye, Z., Lin, S.Y., Yin, H., Piao, H.L., Hardie, D.G., Lin, S.C., 2017. Fructose-1,6-bisphosphate and aldolase mediate glucose sensing by AMPK. Nature 548, 112-116.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (122) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return