5.9
CiteScore
5.9
Impact Factor
Volume 46 Issue 9
Sep.  2019
Turn off MathJax
Article Contents

Temperature-sensitive cytoophidium assembly in Schizosaccharomyces pombe

doi: 10.1016/j.jgg.2019.09.002
More Information
  • Corresponding author: E-mail address: jilong.liu@dpag.ox.ac.uk (Ji-Long Liu)
  • Received Date: 2019-04-19
  • Accepted Date: 2019-09-09
  • Rev Recd Date: 2019-08-29
  • Available Online: 2019-09-24
  • Publish Date: 2019-09-20
  • The metabolic enzyme CTP synthase (CTPS) is able to compartmentalize into filaments, termed cytoophidia, in a variety of organisms including bacteria, budding yeast, fission yeast, fruit flies and mammals. A previous study in budding yeast shows that the filament-forming process of CTPS is not sensitive to temperature shift. Here we study CTPS filamentation in the fission yeast Schizosaccharomyces pombe. To our surprise, we find that both the length and the occurrence of cytoophidia in S. pombe decrease upon cold shock or heat shock. The temperature-dependent changes of cytoophidia are fast and reversible. Taking advantage of yeast genetics, we demonstrate that heat-shock proteins are required for cytoophidium assembly in S. pombe. Temperature sensitivity of cytoophidia makes S. pombe an attractive model system for future investigations of this novel membraneless organelle.
  • loading
  • [1]
    Aughey, G.N., Grice, S.J., Shen, Q.J., Xu, Y., Chang, C.C., Azzam, G., Wang, P.Y., Freeman-Mills, L., Pai, L.M., Sung, L.Y., Yan, J., Liu, J.L., 2014. Nucleotide synthesis is regulated by cytoophidium formation during neurodevelopment and adaptive metabolism. Biol. Open 3, 1045-1056.
    [2]
    Aughey, G.N., Liu, J.L., 2015. Metabolic regulation via enzyme filamentation. Crit. Rev. Biochem. Mol. Biol. 51, 282-293.
    [3]
    Azzam, G., Liu, J.L., 2013. Only one isoform of Drosophila melanogaster CTP synthase forms the cytoophidium. PLoS Genet. 9, e1003256.
    [4]
    Barry, R.M., Bitbol, A.F., Lorestani, A., Charles, E.J., Habrian, C.H., Hansen, J.M., Li, H.J., Baldwin, E.P., Wingreen, N.S., Kollman, J.M., Gitai, Z., 2014. Large-scale filament formation inhibits the activity of CTP synthetase. eLife 3, e03638.
    [5]
    Carcamo, W.C., Satoh, M., Kasahara, H., Terada, N., Hamazaki, T., Chan, J.Y., Yao, B., Tamayo, S., Covini, G., von Muhlen, C.A., Chan, E.K., 2011. Induction of cytoplasmic rods and rings structures by inhibition of the CTP and GTP synthetic pathway in mammalian cells. PLoS One 6, e29690.
    [6]
    Chang, C.C., Keppeke, G.D., Sung, L.Y., Liu, J.L., 2018. Interfilament interaction between IMPDH and CTPS cytoophidia. FEBS J. 285, 3753-3768.
    [7]
    Chang, C.C., Lin, W.C., Pai, L.M., Lee, H.S., Wu, S.C., Ding, S.T., Liu, J.L., Sung, L.Y., 2015. Cytoophidium assembly reflects upregulation of IMPDH activity. J. Cell Sci. 128, 3550-3555.
    [8]
    Chen, K., Zhang, J., Tastan, O.Y., Deussen, Z.A., Siswick, M.Y., Liu, J.L., 2011. Glutamine analogs promote cytoophidium assembly in human and Drosophila cells. J. Genet. Genomics 38, 391-402.
    [9]
    Gou, K.M., Chang, C.C., Shen, Q.J., Sung, L.Y., Liu, J.L., 2014. CTP synthase forms cytoophidia in the cytoplasm and nucleus. Exp. Cell Res. 323, 242-253.
    [10]
    Hayles, J., Wood, V., Jeffery, L., Hoe, K.L., Kim, D.U., Park, H.O., Salas-Pino, S., Heichinger, C., Nurse, P., 2013. A genome-wide resource of cell cycle and cell shape genes of fission yeast. Open Biol. 3, 130053.
    [11]
    Ingerson-Mahar, M., Briegel, A., Werner, J.N., Jensen, G.J., Gitai, Z., 2010. The metabolic enzyme CTP synthase forms cytoskeletal filaments. Nat. Cell Biol. 12, 739-746.
    [12]
    Keppeke, G.D., Chang, C.C., Peng, M., Chen, L.Y., Lin, W.C., Pai, L.M., Andrade, L.E.C., Sung, L.Y., Liu, J.L., 2018. IMP/GTP balance modulates cytoophidium assembly and IMPDH activity. Cell Div. 13, 5.
    [13]
    Kim, D.U., Hayles, J., Kim, D., Wood, V., Park, H.O., Won, M., Yoo, H.S., Duhig, T., Nam, M., Palmer, G., Han, S., Jeffery, L., Baek, S.T., Lee, H., Shim, Y.S., Lee, M., Kim, L., Heo, K.S., Noh, E.J., Lee, A.R., Jang, Y.J., Chung, K.S., Choi, S.J., Park, J.Y., Park, Y., Kim, H.M., Park, S.K., Park, H.J., Kang, E.J., Kim, H.B., Kang, H.S., Park, H.M., Kim, K., Song, K., Song, K.B., Nurse, P., Hoe, K.L., 2010. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 28, 617-623.
    [14]
    Li, H., Ye, F., Ren, J.Y., Wang, P.Y., Du, L.L., Liu, J.L., 2018. Active transport of cytoophidia in Schizosaccharomyces pombe. FASEB J. 32, 5891-5898.
    [15]
    Li, Z., Srivastava, P., 2004. Heat-shock proteins. Curr Protoc Immunol Appendix 1, Appendix 1T.
    [16]
    Liu, J.L., 2010. Intracellular compartmentation of CTP synthase in Drosophila. J. Genet. Genomics 37, 281-296.
    [17]
    Liu, J.L., 2016. The cytoophidium and its kind: Filamentation and compartmentation of metabolic enzymes. Annu. Rev. Cell Dev. Biol. 32, 349-372.
    [18]
    Lynch, E.M., Hicks, D.R., Shepherd, M., Endrizzi, J.A., Maker, A., Hansen, J.M., Barry, R.M., Gitai, Z., Baldwin, E.P., Kollman, J.M., 2017. Human CTP synthase filament structure reveals the active enzyme conformation. Nat. Struct. Mol. Biol. 24, 507-514.
    [19]
    Narayanaswamy, R., Levy, M., Tsechansky, M., Stovall, G.M., O’Connell, J.D., Mirrielees, J., Ellington, A.D., Marcotte, E.M., 2009. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc. Natl. Acad. Sci. U. S. A. 106, 10147-10152.
    [20]
    Noree, C., Monfort, E., Shiau, A.K., Wilhelm, J.E., 2014. Common regulatory control of CTP synthase enzyme activity and filament formation. Mol. Biol. Cell 25, 2282-2290.
    [21]
    Noree, C., Sato, B.K., Broyer, R.M., Wilhelm, J.E., 2010. Identification of novel filament-forming proteins in Saccharomyces cerevisiae and Drosophila melanogaster. J. Cell Biol. 190, 541-551.
    [22]
    Petrovska, I., Nuske, E., Munder, M.C., Kulasegaran, G., Malinovska, L., Kroschwald, S., Richter, D., Fahmy, K., Gibson, K., Verbavatz, J.M., Alberti, S., 2014. Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation. eLife doi: 10.7554/eLife.02409.
    [23]
    Shen, Q.J., Kassim, H., Huang, Y., Li, H., Zhang, J., Li, G., Wang, P.Y., Yan, J., Ye, F., Liu, J.L., 2016. Filamentation of metabolic enzymes in Saccharomyces cerevisiae. J. Genet. Genomics 43, 393-404.
    [24]
    Strochlic, T.I., Stavrides, K.P., Thomas, S.V., Nicolas, E., O’Reilly, A.M., Peterson, J.R., 2014. Ack kinase regulates CTP synthase filaments during Drosophila oogenesis. EMBO Rep. 15, 1184-1191.
    [25]
    Sun, Z., Liu, J.L., 2019. Forming cytoophidia prolongs the half-life of CTP synthase. Cell Discov. 5, 32.
    [26]
    Tastan, O.Y., Liu, J.L., 2015. CTP synthase is required for optic lobe homeostasis in Drosophila. J. Genet. Genomics 42, 261-274.
    [27]
    Wu, C., 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11, 441-469.
    [28]
    Wu, Z., Liu, J.L., 2019. Cytoophidia respond to nutrient stress in Drosophila. Exp. Cell Res. 376, 159-167.
    [29]
    Zhang, J., Hulme, L., Liu, J.L., 2014. Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe. Biol. Open 3, 1092-1097.
    [30]
    Zhang, S., Ding, K., Shen, Q.J., Zhao, S., Liu, J.L., 2018. Filamentation of asparagine synthetase in Saccharomyces cerevisiae. PLoS Genet. 14, e1007737.
  • 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 (117) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return