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Outer kinetochore protein Dam1 promotes centromere clustering in parallel with Slk19 in budding yeast

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Abstract

A higher order organization of the centromeres in the form of clustering of these DNA loci has been observed in many organisms. While centromere clustering is biologically significant to achieve faithful chromosome segregation, the underlying molecular mechanism is yet to be fully understood. In budding yeast, a kinetochore-associated protein Slk19 is shown to have a role in clustering in association with the microtubules whereas removal of either Slk19 or microtubules alone does not have any effect on the centromere clustering. Furthermore, Slk19 is non-essential for growth and becomes cleaved during anaphase whereas clustering being an essential event occurs throughout the cell cycle. Hence, we searched for an additional factor involved in the clustering and since the integrity of the kinetochore complex is shown to be crucial for centromere clustering, we restricted our search within the complex. We observed that the outermost kinetochore protein Dam1 promotes centromere clustering through stabilization of the kinetochore integrity. While in the absence of Dam1 we failed to detect Slk19 at the centromere, on the other hand, we found almost no Dam1 at the centromere in the absence of Slk19 and microtubules suggesting interdependency between these two pathways. Strikingly, we observed that overexpression of Dam1 or Slk19 could restore the centromere clustering largely in the cells devoid of Slk19 and microtubules or Dam1, respectively. Thus, we propose that in budding yeast, centromere clustering is achieved at least by two parallel pathways, through Dam1 and another via Slk19, in concert with the microtubules suggesting that having a dual mechanism may be crucial for ensuring microtubule capture by the point centromeres where each attaches to only one microtubule.

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Abbreviations

kMT:

Kinetochore microtubule

Aux:

Auxin

NOC:

Nocodazole

References

  • Agarwal M, Mehta G, Ghosh SK (2015) Role of Ctf3 and COMA subcomplexes in meiosis: implication in maintaining Cse4 at the centromere and numeric spindle poles. Biochim Biophys Acta 1853:671–684

    Article  CAS  PubMed  Google Scholar 

  • Akhmanova A, Hoogenraad CC (2005) Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol 17:47–54

    Article  CAS  PubMed  Google Scholar 

  • Anderson M, Haase J, Yeh E, Bloom K (2009) Function and assembly of DNA looping, clustering, and microtubule attachment complexes within a eukaryotic kinetochore. Mol Biol Cell 20:4131–4139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartholdi MF (1991) Nuclear distribution of centromeres during the cell cycle of human diploid fibroblasts. J Cell Sci 99(Pt 2):255–263

    PubMed  Google Scholar 

  • Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13:532–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom KS, Fitzgerald-Hayes M, Carbon J (1983) Structural analysis and sequence organization of yeast centromeres. Cold Spring Harb Symp Quant Biol 47(Pt 2):1175–1185

    Article  PubMed  Google Scholar 

  • Camahort R, Li B, Florens L, Swanson SK, Washburn MP, Gerton JL (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 26:853–865

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman IM, Brew C, Wolyniak M, Desai A, Anderson S, Muster N, Yates JR, Huffaker TC, Drubin DG, Barnes G (2001a) Implication of a novel multiprotein Dam1p complex in outer kinetochore function. J Cell Biol 155:1137–1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeseman IM, Enquist-Newman M, Muller-Reichert T, Drubin DG, Barnes G (2001b) Mitotic spindle integrity and kinetochore function linked by the Duo1p/Dam1p complex. J Cell Biol 152:197–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeseman IM, Anderson S, Jwa M, Green EM, Kang J, Yates JR 3rd, Chan CS, Drubin DG, Barnes G (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111:163–172

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127:983–997

    Article  CAS  PubMed  Google Scholar 

  • Collins KA, Castillo AR, Tatsutani SY, Biggins S (2005) De novo kinetochore assembly requires the centromeric histone H3 variant. Mol Biol Cell 16:5649–5660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui H, Ghosh SK, Jayaram M (2009) The selfish yeast plasmid uses the nuclear motor Kip1p but not Cin8p for its localization and equal segregation. J Cell Biol 185:251–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Rop V, Padeganeh A, Maddox PS (2012) CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121:527–538

  • De Wulf P, McAinsh AD, Sorger PK (2003) Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev 17:2902–2921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhatchinamoorthy K, Shivaraju M, Lange JJ, Rubinstein B, Unruh JR, Slaughter BD, Gerton JL (2017) Structural plasticity of the living kinetochore. J Cell Biol 216(11):3551–3570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunleavy EM, Almouzni G, Karpen GH (2011) H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G(1) phase. Nucleus 2:146–157

    Article  PubMed  PubMed Central  Google Scholar 

  • Enquist-Newman M, Cheeseman IM, Van Goor D, Drubin DG, Meluh PB, Barnes G (2001) Dad1p, third component of the Duo1p/Dam1p complex involved in kinetochore function and mitotic spindle integrity. Mol Biol Cell 12:2601–2613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Euskirchen GM (2002) Nnf1p, Dsn1p, Mtw1p, and Nsl1p: a new group of proteins important for chromosome segregation in Saccharomyces cerevisiae. Eukaryot Cell 1:229–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faust AME, Wong CCL, Yates Iii JR, Drubin DG, Barnes G (2013) The FEAR protein Slk19 restricts Cdc14 phosphatase to the nucleus until the end of anaphase, regulating its participation in mitotic exit in Saccharomyces cerevisiae. PLoS One 8:e73194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernius J, Marston AL (2009) Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLoS Genet 5:e1000629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469

    Article  CAS  PubMed  Google Scholar 

  • Funabiki H, Hagan I, Uzawa S, Yanagida M (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J Cell Biol 121:961–976

    Article  CAS  PubMed  Google Scholar 

  • Gardner MK, Bouck DC, Paliulis LV, Meehl JB, O’Toole ET, Haase J, Soubry A, Joglekar AP, Winey M, Salmon ED, Bloom K, Odde DJ (2008) Chromosome congression by kinesin-5 motor-mediated disassembly of longer kinetochore microtubules. Cell 135:894–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gassmann R, Carvalho A, Henzing AJ, Ruchaud S, Hudson DF, Honda R, Nigg EA, Gerloff DL, Earnshaw WC (2004) Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J Cell Biol 166:179–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geil C, Schwab M, Seufert W (2008) A nucleolus-localized activator of Cdc14 phosphatase supports rDNA segregation in yeast mitosis. Curr Biol 18:1001–1005

    Article  CAS  PubMed  Google Scholar 

  • Ghosh SK, Poddar A, Hajra S, Sanyal K, Sinha P (2001) The IML3/MCM19 gene of Saccharomyces cerevisiae is required for a kinetochore-related process during chromosome segregation. Mol Gen Genomics 265:249–257

    Article  CAS  Google Scholar 

  • Gillespie PJ, Blow JJ (2010) Clusters, factories and domains: the complex structure of S phase comes into focus. Cell Cycle 9:3218–3226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goh PY, Kilmartin JV (1993) NDC10: a gene involved in chromosome segregation in Saccharomyces cerevisiae. J Cell Biol 121:503–512

    Article  CAS  PubMed  Google Scholar 

  • Goshima G, Yanagida M (2000) Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell 100:619–633

    Article  CAS  PubMed  Google Scholar 

  • Haase J, Mishra PK, Stephens A, Haggerty R, Quammen C, Taylor RM 2nd, Yeh E, Basrai MA, Bloom K (2013) A 3D map of the yeast kinetochore reveals the presence of core and accessory centromere-specific histone. Curr Biol 23:1939–1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havens KA, Gardner MK, Kamieniecki RJ, Dresser ME, Dawson DS (2010) Slk19p of Saccharomyces cerevisiae regulates anaphase spindle dynamics through two independent mechanisms. Genetics 186:1247–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ho KH, Tsuchiya D, Oliger AC, Lacefield S (2014) Localization and function of budding yeast CENP-A depends upon kinetochore protein interactions and is independent of canonical centromere sequence. Cell Rep 9:2027–2033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofmann C, Cheeseman IM, Goode BL, McDonald KL, Barnes G, Drubin DG (1998) Saccharomyces cerevisiae Duo1p and Dam1p, novel proteins involved in mitotic spindle function. J Cell Biol 143:1029–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt SV, Vergnolle MA, Hussein D, Wozniak MJ, Allan VJ, Taylor SS (2005) Silencing Cenp-F weakens centromeric cohesion, prevents chromosome alignment and activates the spindle checkpoint. J Cell Sci 118:4889–4900

  • Honda R, Körner R, Nigg EA (2003) Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14:3325–3341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoyt MA, He L, Loo KK, Saunders WS (1992) Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol 118:109–120

    Article  CAS  PubMed  Google Scholar 

  • Hyland KM, Kingsbury J, Koshland D, Hieter P (1999) Ctf19p: a novel kinetochore protein in Saccharomyces cerevisiae and a potential link between the kinetochore and mitotic spindle. J Cell Biol 145:15–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JO, Zelter A, Umbreit NT, Bollozos A, Riffle M, Johnson R, MacCoss MJ, Asbury CL, Davis TN (2017) The Ndc80 complex bridges two Dam1 complex rings. eLife. https://doi.org/10.7554/eLife.21069

  • Janke C, Ortiz J, Lechner J, Shevchenko A, Shevchenko A, Magiera MM, Schramm C, Schiebel E (2001) The budding yeast proteins Spc24p and Spc25p interact with Ndc80p and Nuf2p at the kinetochore and are important for kinetochore clustering and checkpoint control. EMBO J 20:777–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janke C, Ortiz J, Tanaka TU, Lechner J, Schiebel E (2002) Four new subunits of the Dam1-Duo1 complex reveal novel functions in sister kinetochore biorientation. EMBO J 21:181–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21:947–962

    Article  CAS  PubMed  Google Scholar 

  • Jenni S, Harrison SC (2018) Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface. Science 360:552–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Q, Trelles-Sticken E, Scherthan H, Loidl J (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141:21–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin QW, Fuchs J, Loidl J (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113(Pt 11):1903–1912

    CAS  PubMed  Google Scholar 

  • Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181:587–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones MH, He X, Giddings TH, Winey M (2001) Yeast Dam1p has a role at the kinetochore in assembly of the mitotic spindle. Proc Natl Acad Sci U S A 98:13675–13680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitagawa K, Hieter P (2001) Evolutionary conservation between budding yeast and human kinetochores. Nat Rev Mol Cell Biol 2:678–687

    Article  CAS  PubMed  Google Scholar 

  • Kitamura E, Blow JJ, Tanaka TU (2006) Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 125:1297–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamura E, Tanaka K, Kitamura Y, Tanaka TU (2007) Kinetochore–microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21:3319–3330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Heck DJ, Nomura M, Horiuchi T (1998) Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev 12:3821–3830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolenda C, Ortiz J, Pelzl M, Norell S, Schmeiser V, Lechner J (2018) Unattached kinetochores drive their own capturing by sequestering a CLASP. Nat Commun 9:886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosco KA, Pearson CG, Maddox PS, Wang PJ, Adams IR, Salmon ED, Bloom K, Huffaker TC (2001) Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol Biol Cell 12:2870–2880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lahiri S, Mehta GD, Ghosh SK (2013) Iml3p, a component of the Ctf19 complex of the budding yeast kinetochore is required to maintain kinetochore integrity under conditions of spindle stress. FEMS Yeast Res 13:375–385

    Article  CAS  PubMed  Google Scholar 

  • Legal T, Zou J, Sochaj A, Rappsilber J, Welburn JPI (2016) Molecular architecture of the Dam1 complex –microtubule interaction. Open Biol. 6:150237

  • Li Y, Bachant J, Alcasabas AA, Wang Y, Qin J, Elledge SJ (2002) The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev 16:183–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lisby M, Mortensen UH, Rothstein R (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5:572–577

    Article  CAS  PubMed  Google Scholar 

  • McCleland ML, Gardner RD, Kallio MJ, Daum JR, Gorbsky GJ, Burke DJ, Stukenberg PT (2003) The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome congression, and spindle checkpoint activity. Genes Dev 17:101–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKinley KL, Cheeseman IM (2016) The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol 17:16–29

    Article  CAS  PubMed  Google Scholar 

  • Measday V, Hailey DW, Pot I, Givan SA, Hyland KM, Cagney G, Fields S, Davis TN, Hieter P (2002) Ctf3p, the Mis6 budding yeast homolog, interacts with Mcm22p and Mcm16p at the yeast outer kinetochore. Genes Dev 16:101–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehta GD, Agarwal M, Ghosh SK (2014) Functional characterization of kinetochore protein, Ctf19 in meiosis I: an implication of differential impact of Ctf19 on the assembly of mitotic and meiotic kinetochores in Saccharomyces cerevisiae. Mol Microbiol 91:1179–1199

    Article  CAS  PubMed  Google Scholar 

  • Meluh PB, Koshland D (1995) Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell 6:793–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meluh PB, Yang P, Glowczewski L, Koshland D, Smith MM (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94:607–613

    Article  CAS  PubMed  Google Scholar 

  • Miranda JJ, De Wulf P, Sorger PK, Harrison SC (2005) The yeast DASH complex forms closed rings on microtubules. Nat Struct Mol Biol 12:138–143

    Article  CAS  PubMed  Google Scholar 

  • Nagpal H, Fukagawa T (2016) Kinetochore assembly and function through the cell cycle. Chromosoma 125:645–659

    Article  CAS  PubMed  Google Scholar 

  • Nakajima Y, Tyers RG, Wong CC, Yates JR 3rd, Drubin DG, Barnes G (2009) Nbl1p: a Borealin/Dasra/CSC-1-like protein essential for Aurora/Ipl1 complex function and integrity in Saccharomyces cerevisiae. Mol Biol Cell 20:1772–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M (2009) An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods 6:917–922

    Article  CAS  PubMed  Google Scholar 

  • Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, Yates JR 3rd, Desai A, Fukagawa T (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8:446–457

    Article  CAS  PubMed  Google Scholar 

  • Ortiz J, Stemmann O, Rank S, Lechner J (1999) A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev 13:1140–1155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36:1065–1071

    Article  CAS  PubMed  Google Scholar 

  • Pfiz S, Zimmermann J, Hilt W (2002) The yeast kinetochore protein Slk19 is required to prevent aberrant chromosome segregation in meiosis and mitosis. Genes Cells 7:1033–1042

    Article  CAS  PubMed  Google Scholar 

  • Pinsky BA, Kotwaliwale CV, Tatsutani SY, Breed CA, Biggins S (2006) Glc7/protein phosphatase 1 regulatory subunits can oppose the Ipl1/aurora protein kinase by redistributing Glc7. Mol Cell Biol 26:2648–2660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poddar A, Roy N, Sinha P (1999) MCM21 and MCM22, two novel genes of the yeast Saccharomyces cerevisiae are required for chromosome transmission. Mol Microbiol 31:349–360

    Article  CAS  PubMed  Google Scholar 

  • Pot I, Measday V, Snydsman B, Cagney G, Fields S, Davis TN, Muller EG, Hieter P (2003) Chl4p and iml3p are two new members of the budding yeast outer kinetochore. Mol Biol Cell 14:460–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prajapati HK, Rizvi SM, Rathore I, Ghosh SK (2017) Microtubule-associated proteins, Bik1 and Bim1, are required for faithful partitioning of the endogenous 2 micron plasmids in budding yeast. Mol Microbiol 103:1046–1064

    Article  CAS  PubMed  Google Scholar 

  • Prajapati HK, Agarwal M, Mittal P, Ghosh SK (2018) Evidence of Zip1 promoting sister kinetochore mono-orientation During meiosis in budding yeast. G3 8:3691–3701

    Article  PubMed  PubMed Central  Google Scholar 

  • Rhind N, Gilbert DM (2013) DNA replication timing. Cold Spring Harb Perspect Biol 5:a010132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richmond D, Rizkallah R, Liang F, Hurt MM, Wang Y (2013) Slk19 clusters kinetochores and facilitates chromosome bipolar attachment. Mol Biol Cell 24:566–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roof DM, Meluh PB, Rose MD (1992) Kinesin-related proteins required for assembly of the mitotic spindle. J Cell Biol 118:95–108

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Perez I, Renwick SJ, Crawley K, Karig I, Buck V, Meadows JC, Franco-Sanchez A, Fleig U, Toda T, Millar JB (2005) The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast. EMBO J 24:2931–2943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandall S, Severin F, McLeod IX, Yates JR 3rd, Oegema K, Hyman A, Desai A (2006) A Bir1-Sli15 complex connects centromeres to microtubules and is required to sense kinetochore tension. Cell 127:1179–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanyal K, Ghosh SK, Sinha P (1998) The MCM16 gene of the yeast Saccharomyces cerevisiae is required for chromosome segregation. Mol Gen Genet 260:242–250

    Article  CAS  PubMed  Google Scholar 

  • Sawin KE, LeGuellec K, Philippe M, Mitchison TJ (1992) Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359:540–543

    Article  CAS  PubMed  Google Scholar 

  • Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solovei I, Schermelleh L, During K, Engelhardt A, Stein S, Cremer C, Cremer T (2004) Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112:410–423

    Article  PubMed  Google Scholar 

  • Stults DM, Killen MW, Pierce HH, Pierce AJ (2008) Genomic architecture and inheritance of human ribosomal RNA gene clusters. Genome Res 18:13–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581–592

    Article  CAS  PubMed  Google Scholar 

  • Sullivan M, Lehane C, Uhlmann F (2001) Orchestrating anaphase and mitotic exit: separase cleavage and localization of Slk19. Nat Cell Biol 3:771–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taddei A, Van Houwe G, Nagai S, Erb I, van Nimwegen E, Gasser SM (2009) The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Res 19:611–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur J, Sanyal K (2012) A coordinated interdependent protein circuitry stabilizes the kinetochore ensemble to protect CENP-A in the human pathogenic yeast Candida albicans. PLoS Genet 8:e1002661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas GE, Renjith MR, Manna TK (2017) Kinetochore-microtubule interactions in chromosome segregation: lessons from yeast and mammalian cells. Biochem J 474:3559–3577

    Article  CAS  PubMed  Google Scholar 

  • Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151:95–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umbreit NT, Miller MP, Tien JF, Ortola JC, Gui L, Lee KK, Biggins S, Asbury CL, Davis TN (2014) Kinetochores require oligomerization of Dam1 complex to maintain microtubule attachments against tension and promote biorientation. Nat Commun 5:4951

    Article  CAS  PubMed  Google Scholar 

  • Varis A, Salmela AL, Kallio MJ (2006) Cenp-F (mitosin) is more than a mitotic marker. Chromosoma 115:288–295

    Article  CAS  PubMed  Google Scholar 

  • Wargacki MM, Tay JC, Muller EG, Asbury CL, Davis TN (2010) Kip3, the yeast kinesin-8, is required for clustering of kinetochores at metaphase. Cell Cycle 9:2581–2588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welburn JP, Cheeseman IM (2008) Toward a molecular structure of the eukaryotic kinetochore. Dev Cell 15:645–655

    Article  CAS  PubMed  Google Scholar 

  • Welburn JP, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR 3rd, Cheeseman IM (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16:374–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westermann S, Avila-Sakar A, Wang HW, Niederstrasser H, Wong J, Drubin DG, Nogales E, Barnes G (2005) Formation of a dynamic kinetochore- microtubule interface through assembly of the Dam1 ring complex. Mol Cell 17:277–290

    Article  CAS  PubMed  Google Scholar 

  • Wigge PA, Kilmartin JV (2001) The Ndc80p complex from Saccharomyces cerevisiae contains conserved centromere components and has a function in chromosome segregation. J Cell Biol 152:349–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng X, Kahana JA, Silver PA, Morphew MK, McIntosh JR, Fitch IT, Carbon J, Saunders WS (1999) Slk19p is a centromere protein that functions to stabilize mitotic spindles. J Cell Biol 146:415–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Zhao J, Bibikova M, Leverson JD, Bossy-Wetzel E, Fan JB, Abraham RT, Jiang W (2005) Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol Biol Cell 16:3187–3199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank Tim C. Huffaker for providing the plasmid pKK1. We would like to acknowledge the central instrumentation facility of IIT Bombay for providing the microscopy facility and Arpita Sarkar for the help to construct the Slk19 overexpression strain. SKG lab is supported by DBT (BT/PR20932/BRB/10/1539/2016) and BRNS (37(1)/14/30/2015/BRNS) grants. PM and DT are funded by UGC (17-06/2012(i) EU-V) and CSIR (09/087(0886)/2017-EMR-I) fellowships, respectively. We acknowledge the central instrumentation facility of IIT Bombay.

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Author notes

  1. Ankita Chavan and Deepika Trakroo contributed equally to this work.

Authors and Affiliations

  1. Department of Biosciences and Bioengineering, Indian Institute of Technology Bombay, Powai, Mumbai, 400076, India

    Priyanka Mittal, Deepika Trakroo & Santanu K. Ghosh

  2. Molecular and Cell Biology Department, University of Connecticut, Storrs, CT, 06269, USA

    Ankita Chavan

  3. Advanced Centre for Treatment, Research and Education in Cancer, Kharghar, Navi Mumbai, 410210, India

    Sanket Shah

Authors
  1. Priyanka Mittal
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  2. Ankita Chavan
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  3. Deepika Trakroo
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  4. Sanket Shah
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  5. Santanu K. Ghosh
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Correspondence to Santanu K. Ghosh.

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Mittal, P., Chavan, A., Trakroo, D. et al. Outer kinetochore protein Dam1 promotes centromere clustering in parallel with Slk19 in budding yeast. Chromosoma 128, 133–148 (2019). https://doi.org/10.1007/s00412-019-00694-9

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  • DOI: https://doi.org/10.1007/s00412-019-00694-9

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