Inositol Pyrophosphate Kinase Asp1 Modulates Chromosome Segregation Fidelity and Spindle Function in Schizosaccharomyces pombe

REFERENCES

• Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, Kumar R, Jenkins RB, de Groen PC, Roche P, van Deursen JM. 2004. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36:744–749. http://dx.doi.org/10.1038/ng1382.
   PubMed Web of Science ®Google Scholar
• Lott IT, Head E. 2005. Alzheimer disease and Down syndrome: factors in pathogenesis. Neurobiol Aging 26:383–389. http://dx.doi.org/10.1016/j.neurobiolaging.2004.08.005.
   PubMed Web of Science ®Google Scholar
• Harrison BD, Hashemi J, Bibi M, Pulver R, Bavli D, Nahmias Y, Wellington M, Sapiro G, Berman J. 2014. A tetraploid intermediate precedes aneuploid formation in yeasts exposed to fluconazole. PLoS Biol 12:e1001815. http://dx.doi.org/10.1371/journal.pbio.1001815.
   PubMed Web of Science ®Google Scholar
• Santaguida S, Amon A. 2015. Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat Rev Mol Cell Biol 16:473–485. http://dx.doi.org/10.1038/nrm4025.
   PubMed Web of Science ®Google Scholar
• Carmena M, Wheelock M, Funabiki H, Earnshaw WC. 2012. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 13:789–803. http://dx.doi.org/10.1038/nrm3474.
   PubMed Web of Science ®Google Scholar
• Sacristan C, Kops GJ. 2015. Joined at the hip: kinetochores, microtubules, and spindle assembly checkpoint signaling. Trends Cell Biol 25:21–28. http://dx.doi.org/10.1016/j.tcb.2014.08.006.
   PubMed Web of Science ®Google Scholar
• Akera T, Goto Y, Sato M, Yamamoto M, Watanabe Y. 2015. Mad1 promotes chromosome congression by anchoring a kinesin motor to the kinetochore. Nat Cell Biol 17:1124–1133. http://dx.doi.org/10.1038/ncb3219.
   PubMed Web of Science ®Google Scholar
• Nabeshima K, Nakagawa T, Straight AF, Murray A, Chikashige Y, Yamashita YM, Hiraoka Y, Yanagida M. 1998. Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol Biol Cell 9:3211–3225. http://dx.doi.org/10.1091/mbc.9.11.3211.
   PubMed Web of Science ®Google Scholar
• Mallavarapu A, Sawin K, Mitchison T. 1999. A switch in microtubule dynamics at the onset of anaphase B in the mitotic spindle of Schizosaccharomyces pombe. Curr Biol 9:1423–1426. http://dx.doi.org/10.1016/S0960-9822(00)80090-1.
   PubMedGoogle Scholar
• Mulugu S, Bai W, Fridy PC, Bastidas RJ, Otto JC, Dollins DE, Haystead TA, Ribeiro AA, York JD. 2007. A conserved family of enzymes that phosphorylate inositol hexakisphosphate. Science 316:106–109. http://dx.doi.org/10.1126/science.1139099.
   PubMed Web of Science ®Google Scholar
• Choi JH, Williams J, Cho J, Falck JR, Shears SB. 2007. Purification, sequencing, and molecular identification of a mammalian PP-InsP5 kinase that is activated when cells are exposed to hyperosmotic stress. J Biol Chem 282:30763–30775. http://dx.doi.org/10.1074/jbc.M704655200.
   PubMed Web of Science ®Google Scholar
• Fridy PC, Otto JC, Dollins DE, York JD. 2007. Cloning and characterization of two human VIP1-like inositol hexakisphosphate and diphosphoinositol pentakisphosphate kinases. J Biol Chem 282:30754–30762. http://dx.doi.org/10.1074/jbc.M704656200.
   PubMed Web of Science ®Google Scholar
• Gokhale NA, Zaremba A, Shears SB. 2011. Receptor-dependent compartmentalization of PPIP5K1, a kinase with a cryptic polyphosphoinositide binding domain. Biochem J 434:415–426. http://dx.doi.org/10.1042/BJ20101437.
   PubMedGoogle Scholar
• Lin H, Fridy PC, Ribeiro AA, Choi JH, Barma DK, Vogel G, Falck JR, Shears SB, York JD, Mayr GW. 2009. Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases. J Biol Chem 284:1863–1872. http://dx.doi.org/10.1074/jbc.M805686200.
   PubMed Web of Science ®Google Scholar
• Wang H, Falck JR, Hall TM, Shears SB. 2011. Structural basis for an inositol pyrophosphate kinase surmounting phosphate crowding. Nat Chem Biol 8:111–116. http://dx.doi.org/10.1038/nchembio.733.
   PubMed Web of Science ®Google Scholar
• Pöhlmann J, Risse C, Seidel C, Pohlmann T, Jakopec V, Walla E, Ramrath P, Takeshita N, Baumann S, Feldbrugge M, Fischer R, Fleig U. 2014. The Vip1 inositol polyphosphate kinase family regulates polarized growth and modulates the microtubule cytoskeleton in fungi. PLoS Genet 10:e1004586. http://dx.doi.org/10.1371/journal.pgen.1004586.
   PubMedGoogle Scholar
• Wang H, Nair VS, Holland AA, Capolicchio S, Jessen HJ, Johnson MK, Shears SB. 2015. Asp1 from Schizosaccharomyces pombe binds a [2Fe-2S](2+) cluster which inhibits inositol pyrophosphate 1-phosphatase activity. Biochemistry 54:6462–6474. http://dx.doi.org/10.1021/acs.biochem.5b00532.
   PubMed Web of Science ®Google Scholar
• Pulloor NK, Nair S, Kostic AD, Bist P, Weaver JD, Riley AM, Tyagi R, Uchil PD, York JD, Snyder SH, Garcia-Sastre A, Potter BV, Lin R, Shears SB, Xavier RJ, Krishnan MN. 2014. Human genome-wide RNAi screen identifies an essential role for inositol pyrophosphates in type-I interferon response. PLoS Pathog 10:e1003981. http://dx.doi.org/10.1371/journal.ppat.1003981.
   PubMed Web of Science ®Google Scholar
• Laha D, Johnen P, Azevedo C, Dynowski M, Weiss M, Capolicchio S, Mao H, Iven T, Steenbergen M, Freyer M, Gaugler P, de Campos MK, Zheng N, Feussner I, Jessen HJ, Van Wees SC, Saiardi A, Schaaf G. 2015. VIH2 regulates the synthesis of inositol pyrophosphate InsP8 and jasmonate-dependent defenses in Arabidopsis. Plant Cell 27:1082–1097. http://dx.doi.org/10.1105/tpc.114.135160.
   PubMed Web of Science ®Google Scholar
• Feoktistova A, McCollum D, Ohi R, Gould KL. 1999. Identification and characterization of Schizosaccharomyces pombe asp1(+), a gene that interacts with mutations in the Arp2/3 complex and actin. Genetics 152:895–908.
   PubMed Web of Science ®Google Scholar
• Pöhlmann J, Fleig U. 2010. Asp1, a conserved 1/3 inositol polyphosphate kinase, regulates the dimorphic switch in Schizosaccharomyces pombe. Mol Cell Biol 30:4535–4547. http://dx.doi.org/10.1128/MCB.00472-10.
   PubMed Web of Science ®Google Scholar
• Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795–823. http://dx.doi.org/10.1016/0076-6879(91)94059-L.
   PubMed Web of Science ®Google Scholar
• Tran PT, Paoletti A, Chang F. 2004. Imaging green fluorescent protein fusions in living fission yeast cells. Methods 33:220–225. http://dx.doi.org/10.1016/j.ymeth.2003.11.017.
   PubMed Web of Science ®Google Scholar
• Bratman SV, Chang F. 2007. Stabilization of overlapping microtubules by fission yeast CLASP. Dev Cell 13:812–827. http://dx.doi.org/10.1016/j.devcel.2007.10.015.
   PubMedGoogle Scholar
• Winey M, Bloom K. 2012. Mitotic spindle form and function. Genetics 190:1197–1224. http://dx.doi.org/10.1534/genetics.111.128710.
   PubMed Web of Science ®Google Scholar
• Snaith HA, Anders A, Samejima I, Sawin KE. 2010. New and old reagents for fluorescent protein tagging of microtubules in fission yeast; experimental and critical evaluation. Methods Cell Biol 97:147–172. http://dx.doi.org/10.1016/S0091-679X(10)97009-X.
   PubMedGoogle Scholar
• Kerres A, Jakopec V, Fleig U. 2007. The conserved Spc7 protein is required for spindle integrity and links kinetochore complexes in fission yeast. Mol Biol Cell 18:2441–2454. http://dx.doi.org/10.1091/mbc.E06-08-0738.
   PubMed Web of Science ®Google Scholar
• Garcia MA, Vardy L, Koonrugsa N, Toda T. 2001. Fission yeast ch-TOG/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint. EMBO J 20:3389–3401. http://dx.doi.org/10.1093/emboj/20.13.3389.
   PubMedGoogle Scholar
• Jakopec V, Topolski B, Fleig U. 2012. Sos7, an essential component of the conserved S. pombe Ndc80-MIND-Spc7 complex, identifies a new family of fungal kinetochore proteins. Mol Cell Biol 32:3308–3312. http://dx.doi.org/10.1128/MCB.00212-12.
   PubMedGoogle Scholar
• Goshima G, Scholey JM. 2010. Control of mitotic spindle length. Annu Rev Cell Dev Biol 26:21–57. http://dx.doi.org/10.1146/annurev-cellbio-100109-104006.
   PubMed Web of Science ®Google Scholar
• Costa J, Fu C, Khare VM, Tran PT. 2014. csi2p modulates microtubule dynamics and organizes the bipolar spindle for chromosome segregation. Mol Biol Cell 25:3900–3908. http://dx.doi.org/10.1091/mbc.E14-09-1370.
   PubMedGoogle Scholar
• Hagan I, Yanagida M. 1995. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J Cell Biol 129:1033–1047. http://dx.doi.org/10.1083/jcb.129.4.1033.
   PubMed Web of Science ®Google Scholar
• Nakazawa N, Nakamura T, Kokubu A, Ebe M, Nagao K, Yanagida M. 2008. Dissection of the essential steps for condensin accumulation at kinetochores and rDNAs during fission yeast mitosis. J Cell Biol 180:1115–1131. http://dx.doi.org/10.1083/jcb.200708170.
   PubMedGoogle Scholar
• Petersen J, Paris J, Willer M, Philippe M, Hagan IM. 2001. The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation. J Cell Sci 114:4371–4384.
   PubMed Web of Science ®Google Scholar
• Kawashima SA, Tsukahara T, Langegger M, Hauf S, Kitajima TS, Watanabe Y. 2007. Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev 21:420–435. http://dx.doi.org/10.1101/gad.1497307.
   PubMedGoogle Scholar
• Heinrich S, Windecker H, Hustedt N, Hauf S. 2012. Mph1 kinetochore localization is crucial and upstream in the hierarchy of spindle assembly checkpoint protein recruitment to kinetochores. J Cell Sci 125:4720–4727. http://dx.doi.org/10.1242/jcs.110387.
   PubMedGoogle Scholar
• Overlack K, Krenn V, Musacchio A. 2014. When Mad met Bub. EMBO Rep 15:326–328. http://dx.doi.org/10.1002/embr.201438574.
   PubMedGoogle Scholar
• Millband DN, Hardwick KG. 2002. Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol Cell Biol 22:2728–2742. http://dx.doi.org/10.1128/MCB.22.8.2728-2742.2002.
   PubMedGoogle Scholar
• Windecker H, Langegger M, Heinrich S, Hauf S. 2009. Bub1 and Bub3 promote the conversion from monopolar to bipolar chromosome attachment independently of shugoshin. EMBO Rep 10:1022–1028. http://dx.doi.org/10.1038/embor.2009.183.
   PubMedGoogle Scholar
• Ito D, Saito Y, Matsumoto T. 2012. Centromere-tethered Mps1 pombe homolog (Mph1) kinase is a sufficient marker for recruitment of the spindle checkpoint protein Bub1, but not Mad1. Proc Natl Acad Sci U S A 109:209–214. http://dx.doi.org/10.1073/pnas.1114647109.
   PubMedGoogle Scholar
• Yamagishi Y, Yang CH, Tanno Y, Watanabe Y. 2012. MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat Cell Biol 14:746–752. http://dx.doi.org/10.1038/ncb2515.
   PubMed Web of Science ®Google Scholar
• Lara-Gonzalez P, Westhorpe FG, Taylor SS. 2012. The spindle assembly checkpoint. Curr Biol 22:R966–980. http://dx.doi.org/10.1016/j.cub.2012.10.006.
   PubMed Web of Science ®Google Scholar
• Saitoh S, Ishii K, Kobayashi Y, Takahashi K. 2005. Spindle checkpoint signaling requires the mis6 kinetochore subcomplex, which interacts with mad2 and mitotic spindles. Mol Biol Cell 16:3666–3677. http://dx.doi.org/10.1091/mbc.E05-01-0014.
   PubMedGoogle Scholar
• Heinrich S, Geissen EM, Kamenz J, Trautmann S, Widmer C, Drewe P, Knop M, Radde N, Hasenauer J, Hauf S. 2013. Determinants of robustness in spindle assembly checkpoint signalling. Nat Cell Biol 15:1328–1339. http://dx.doi.org/10.1038/ncb2864.
   PubMedGoogle Scholar
• Niwa O, Matsumoto T, Yanagida M. 1986. Construction of a mini-chromosome by deletion and itsmitotic and meiotic behaviour in fission yeast. Mol Gen Genet 203:397–405. http://dx.doi.org/10.1007/BF00422063.
   Google Scholar
• Fleig U, Sen-Gupta M, Hegemann JH. 1996. Fission yeast mal2+ is required for chromosome segregation. Mol Cell Biol 16:6169–6177. http://dx.doi.org/10.1128/MCB.16.11.6169.
   PubMedGoogle Scholar
• Maundrell K. 1993. Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123:127–130. http://dx.doi.org/10.1016/0378-1119(93)90551-D.
   PubMed Web of Science ®Google Scholar
• Hagan I, Yanagida M. 1992. Kinesin-related cut7 protein associates with mitotic and meiotic spindles in fission yeast. Nature 356:74–76. http://dx.doi.org/10.1038/356074a0.
   PubMedGoogle Scholar
• Garcia MA, Koonrugsa N, Toda T. 2002. Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast. EMBO J 21:6015–6024. http://dx.doi.org/10.1093/emboj/cdf611.
   PubMed Web of Science ®Google Scholar
• Garcia MA, Koonrugsa N, Toda T. 2002. Two kinesin-like Kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A. Curr Biol 12:610–621. http://dx.doi.org/10.1016/S0960-9822(02)00761-3.
   PubMed Web of Science ®Google Scholar
• Erent M, Drummond DR, Cross RA. 2012. S. pombe kinesins-8 promote both nucleation and catastrophe of microtubules. PLoS One 7:e30738. http://dx.doi.org/10.1371/journal.pone.0030738.
   PubMedGoogle Scholar
• Grissom PM, Fiedler T, Grishchuk EL, Nicastro D, West RR, McIntosh JR. 2009. Kinesin-8 from fission yeast: a heterodimeric, plus-end-directed motor that can couple microtubule depolymerization to cargo movement. Mol Biol Cell 20:963–972.
   PubMed Web of Science ®Google Scholar
• Yukawa M, Ikebe C, Toda T. 2015. The Msd1-Wdr8-Pkl1 complex anchors microtubule minus ends to fission yeast spindle pole bodies. J Cell Biol 209:549–562. http://dx.doi.org/10.1083/jcb.201412111.
   PubMedGoogle Scholar
• Syrovatkina V, Tran PT. 2015. Loss of kinesin-14 results in aneuploidy via kinesin-5-dependent microtubule protrusions leading to chromosome cut. Nat Commun 6:7322. http://dx.doi.org/10.1038/ncomms8322.
   PubMedGoogle Scholar
• Daniel JA, Keyes BE, Ng YP, Freeman CO, Burke DJ. 2006. Diverse functions of spindle assembly checkpoint genes in Saccharomyces cerevisiae. Genetics 172:53–65.
   PubMedGoogle Scholar
• Syrovatkina V, Fu C, Tran PT. 2013. Antagonistic spindle motors and MAPs regulate metaphase spindle length and chromosome segregation. Curr Biol 23:2423–2429. http://dx.doi.org/10.1016/j.cub.2013.10.023.
   PubMedGoogle Scholar
• West RR, Malmstrom T, McIntosh JR. 2002. Kinesins klp5(+) and klp6(+) are required for normal chromosome movement in mitosis. J Cell Sci 115:931–940.
   PubMed Web of Science ®Google Scholar
• Lee YS, Mulugu S, York JD, O'Shea EK. 2007. Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 316:109–112. http://dx.doi.org/10.1126/science.1139080.
   PubMed Web of Science ®Google Scholar
• Saiardi A, Bhandari R, Resnick AC, Snowman AM, Snyder SH. 2004. Phosphorylation of proteins by inositol pyrophosphates. Science 306:2101–2105. http://dx.doi.org/10.1126/science.1103344.
   PubMed Web of Science ®Google Scholar
• Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, Kobayashi Y, Hashimoto A, Hamamoto M, Hiraoka Y, Horinouchi S, Yoshida M. 2006. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24:841–847. http://dx.doi.org/10.1038/nbt1222.
   PubMed Web of Science ®Google Scholar
• Beinhauer JD, Hagan IM, Hegemann JH, Fleig U. 1997. 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 139:717–728. http://dx.doi.org/10.1083/jcb.139.3.717.
   PubMed Web of Science ®Google Scholar
• Loiodice I, Staub J, Setty TG, Nguyen NP, Paoletti A, Tran PT. 2005. Ase1p organizes antiparallel microtubule arrays during interphase and mitosis in fission yeast. Mol Biol Cell 16:1756–1768. http://dx.doi.org/10.1091/mbc.E04-10-0899.
   PubMed Web of Science ®Google Scholar
• Yamashita A, Sato M, Fujita A, Yamamoto M, Toda T. 2005. The roles of fission yeast ase1 in mitotic cell division, meiotic nuclear oscillation, and cytokinesis checkpoint signaling. Mol Biol Cell 16:1378–1395. http://dx.doi.org/10.1091/mbc.E04-10-0859.
   PubMedGoogle Scholar
• Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. 2001. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 153:517–527. http://dx.doi.org/10.1083/jcb.153.3.517.
   PubMed Web of Science ®Google Scholar
• Janssen A, van der Burg M, Szuhai K, Kops GJ, Medema RH. 2011. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 333:1895–1898. http://dx.doi.org/10.1126/science.1210214.
   PubMed Web of Science ®Google Scholar
• Ruchaud S, Carmena M, Earnshaw WC. 2007. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8:798–812. http://dx.doi.org/10.1038/nrm2257.
   PubMed Web of Science ®Google Scholar
• Bakhoum SF, Thompson SL, Manning AL, Compton DA. 2009. Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat Cell Biol 11:27–35. http://dx.doi.org/10.1038/ncb1809.
   PubMed Web of Science ®Google Scholar
• Banerjee B, Kestner CA, Stukenberg PT. 2014. EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B. J Cell Biol 204:947–963. http://dx.doi.org/10.1083/jcb.201307119.
   PubMedGoogle Scholar