368
Views
5
CrossRef citations to date
0
Altmetric
Biochemistry & Molecular Biology

Glucose limitation and pka1 deletion rescue aberrant mitotic spindle formation induced by Mal3 overexpression in Schizosaccharomyces pombe

, ORCID Icon & ORCID Icon
Pages 1667-1680 | Received 24 Mar 2020, Accepted 27 Apr 2020, Published online: 22 May 2020

References

  • Akhmanova A, Steinmetz MO. Microtubule +TIPs at a glance. J Cell Sci. 2010;123(20):3415–3419.
  • Lansbergen G, Akhmanova A. Microtubule plus end: a hub of cellular activities. Traffic. 2006;7(5):499–507.
  • Beinhauer JD, Hagan IM, Hegemann JH, et al. Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form. J Cell Biol. 1997;139(3):717–728.
  • Chang F, Martin SG. Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol. 2009;1(1):a001347.
  • Busch KE, Hayles J, Nurse P, et al. Tea2p kinesin is involved in spatial microtubule organization by transporting tip1p on microtubules. Dev Cell. 2004;6(6):831–843.
  • Kerres A, Vietmeier-Decker C, Ortiz J, et al. The fission yeast kinetochore component Spc7 associates with the EB1 family member Mal3 and is required for kinetochore-spindle association. Mol Biol Cell. 2004;15(12):5255–5267.
  • Matsuo Y, Maurer SP, Yukawa M, et al. An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation. J Cell Sci. 2016;129(24):4592–4606.
  • Gimona M, Djinovic-Carugo K, Kranewitter WJ, et al. Functional plasticity of CH domains. FEBS Lett. 2002;513(1):98–106.
  • Hayashi I, Ikura M. Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J Biol Chem. 2003;278(38):36430–36434.
  • Des Georges A, Katsuki M, DR D, et al. Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice. Nat Struct Mol Biol. 2008;15(10):1102–1108.
  • Maurer SP, Fourniol FJ, Bohner G, et al. EBs recognize a nucleotide-dependent structural cap at growing microtubule ends. Cell. 2012;149(2):371–382.
  • Iimori M, Ozaki K, Chikashige Y, et al. A mutation of the fission yeast EB1 overcomes negative regulation by phosphorylation and stabilizes microtubules. Exp Cell Res. 2012;318(3):262–275.
  • Blangy A, Lane HA, d’Herin P, et al. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell. 1995;83(7):1159–1169.
  • Enos AP, Morris NR. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell. 1990;60(6):1019–1027.
  • Goshima G, Vale RD. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J Cell Biol. 2003;162(6):1003–1016.
  • Hagan I, Yanagida M. Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature. 1990;347(6293):563–566.
  • Hoyt MA, He L, Loo KK, et al. Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol. 1992;118(1):109–120.
  • Mann BJ, Wadsworth P. Kinesin-5 regulation and function in mitosis. Trends Cell Biol. 2019;29(1):66–79.
  • Akera T, Goto Y, Sato M, et al. Mad1 promotes chromosome congression by anchoring a kinesin motor to the kinetochore. Nat Cell Biol. 2015;17(9):1124–1133.
  • Hirano T, Funahashi S, Uemura T, et al. Isolation and characterization of Schizosaccharomyces pombe cut mutants that block nuclear division but not cytokinesis. Embo J. 1986;5(11):2973–2979.
  • Yukawa M, Yamada Y, Toda T. Suppressor analysis uncovers that maps and microtubule dynamics balance with the Cut7/Kinesin-5 motor for mitotic spindle assembly in Schizosaccharomyces pombe. G3. 2019;9(1):269–280.
  • Hoffman CS. Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans. 2005;33(1):257–260.
  • Kim JH, Roy A, Jouandot D, et al. The glucose signaling network in yeast. Biochim Biophys Acta. 2013;1830(11):5204–5210.
  • Santangelo GM. Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2006;70(1):253–282.
  • Van Ende M, Wijnants S, Van Dijck P. Sugar sensing and signaling in Candida albicans and Candida glabrata. Front Microbiol. 2019;10:99.
  • DeVoti J, Seydoux G, Beach D, et al. Interaction between ran1+ protein kinase and cAMP dependent protein kinase as negative regulators of fission yeast meiosis. Embo J. 1991;10(12):3759–3768.
  • Gupta DR, Paul SK, Oowatari Y, et al. Multistep regulation of protein kinase A in its localization, phosphorylation and binding with a regulatory subunit in fission yeast. Curr Genet. 2011;57(5):353–365.
  • Kawamukai M, Ferguson K, Wigler M, et al. Genetic and biochemical analysis of the adenylyl cyclase of Schizosaccharomyces pombe. Cell Regul. 1991;2(2):155–164.
  • Maeda T, Watanabe Y, Kunitomo H, et al. Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J Biol Chem. 1994;269(13):9632–9637.
  • Matsuo Y, Kawamukai M. cAMP-dependent protein kinase involves calcium tolerance through the regulation of Prz1 in Schizosaccharomyces pombe. Biosci Biotechnol Biochem. 2017;81(2):231–241.
  • Matsuo Y, McInnis B, Marcus S. Regulation of the subcellular localization of cyclic AMP-dependent protein kinase in response to physiological stresses and sexual differentiation in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell. 2008;7(9):1450–1459.
  • Welton RM, Hoffman CS. Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics. 2000;156(2):513–521.
  • Byrne SM, Hoffman CS. Six git genes encode a glucose-induced adenylate cyclase activation pathway in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1993;105(4):1095-1100.
  • Roux AE, Quissac A, Chartrand P, et al. Regulation of chronological aging in Schizosaccharomyces pombe by the protein kinases Pka1 and Sck2. Aging Cell. 2006;5(4):345–357.
  • Stiefel J, Wang L, Kelly DA, et al. Suppressors of an adenylate cyclase deletion in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell. 2004;3(3):610–619.
  • Tanabe T, Yamaga M, Kawamukai M, et al. Mal3 is a multi-copy suppressor of the sensitivity to microtubule-depolymerizing drugs and chromosome mis-segregation in a fission yeast pka1 mutant. PLoS One. 2019;14(4):e0214803.
  • Wu SY, McLeod M. The sak1+ gene of Schizosaccharomyces pombe encodes an RFX family DNA-binding protein that positively regulates cyclic AMP-dependent protein kinase-mediated exit from the mitotic cell cycle. Mol Cell Biol. 1995;15(3):1479–1488.
  • Gupta DR, Paul SK, Oowatari Y, et al. Complex formation, phosphorylation, and localization of protein kinase A of Schizosaccharomyces pombe upon glucose starvation. Biosci Biotechnol Biochem. 2011;75(8):1456–1465.
  • Murray JM, Watson AT, Carr AM. Transformation of Schizosaccharomyces pombe: lithium acetate/dimethyl sulfoxide procedure. Cold Spring Harb Protoc. 2016. DOI:10.1101/pdb.prot090969
  • Petersen J, Russell P. Growth and the environment of Schizosaccharomyces pombe. Cold Spring Harb Protoc. 2016. DOI:10.1101/pdb.top079764
  • Ekwall K, Thon G. Spore analysis and tetrad dissection of Schizosaccharomyces pombe. Cold Spring Harb Protoc. 2017. DOI:10.1101/pdb.prot091710
  • Forsburg SL. Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res. 1993;21(12):2955–2956.
  • Matsuo Y, Tanaka K, Nakagawa T, et al. Genetic analysis of chs1+ and chs2+ encoding chitin synthases from Schizosaccharomyces pombe. Biosci Biotechnol Biochem. 2004;68(7):1489–1499.
  • Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48(3):452–458.
  • Matsuzawa T, Fujita Y, Tohda H, et al. Snf1-like protein kinase Ssp2 regulates glucose derepression in Schizosaccharomyces pombe. Eukaryot Cell. 2012;11(2):159–167.
  • Saitoh S, Mori A, Uehara L, et al. Mechanisms of expression and translocation of major fission yeast glucose transporters regulated by CaMKK/phosphatases, nuclear shuttling, and TOR. Mol Biol Cell. 2015;26(2):373–386.
  • Mana-Capelli S, McLean JR, Chen CT, et al. The kinesin-14 Klp2 is negatively regulated by the SIN for proper spindle elongation and telophase nuclear positioning. Mol Biol Cell. 2012;23(23):4592–4600.
  • Nehlig A, Molina A, Rodrigues-Ferreira S, et al. Regulation of end-binding protein EB1 in the control of microtubule dynamics. Cell Mol Life Sci. 2017;74(13):2381–2393.
  • Snaith HA, Thompson J, Yates JR 3rd, et al. Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J Cell Sci. 2011;124(13):2187–2199.
  • Yukawa M, Yamada Y, Yamauchi T, et al. Two spatially distinct kinesin-14 proteins, Pkl1 and Klp2, generate collaborative inward forces against kinesin-5 Cut7 in S. pombe. J Cell Sci. 2018;131(1):jcs210740.
  • Akhmanova A, Steinmetz MO. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol. 2008;9(4):309–322.
  • Wood V, Harris MA, McDowall MD, et al. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res. 2011;40:D695–9.
  • Yukawa M, Kawakami T, Okazaki M, et al. A microtubule polymerase cooperates with the kinesin-6 motor and a microtubule cross-linker to promote bipolar spindle assembly in the absence of kinesin-5 and kinesin-14 in fission yeast. Mol Biol Cell. 2017;28(25):3647–3659.
  • Kawasaki Y, Nagao K, Nakamura T, et al. Fission yeast MAP kinase is required for the increased securin-separase interaction that rescues separase mutants under stresses. Cell Cycle. 2006;5(16):1831–1839.
  • Yamashita YM, Nakaseko Y, Kumada K, et al. Fission yeast APC/cyclosome subunits, Cut20/Apc4 and Cut23/Apc8, in regulating metaphase-anaphase progression and cellular stress responses. Genes Cells. 1999;4(8):445–463.
  • Yamashita YM, Nakaseko Y, Samejima I, et al. 20S cyclosome complex formation and proteolytic activity inhibited by the cAMP/PKA pathway. Nature. 1996;384(6606):276–279.
  • Yanagida M, Yamashita YM, Tatebe H, et al. Control of metaphase-anaphase progression by proteolysis: cyclosome function regulated by the protein kinase A pathway, ubiquitination and localization. Philos Trans R Soc Lond B Biol Sci. 1999;354(1389):1559–1570.
  • Kelkar M, Martin SG. PKA antagonizes CLASP-dependent microtubule stabilization to re-localize Pom1 and buffer cell size upon glucose limitation. Nat Commun. 2015;6(8445):8445.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.