Kinetochore-associated Stu2 promotes chromosome biorientation in vivo


Autoři: Matthew P. Miller aff001;  Rena K. Evans aff001;  Alex Zelter aff002;  Elisabeth A. Geyer aff003;  Michael J. MacCoss aff004;  Luke M. Rice aff003;  Trisha N. Davis aff002;  Charles L. Asbury aff005;  Sue Biggins aff001
Působiště autorů: Howard Hughes Medical Institute, Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America aff001;  Department of Biochemistry, University of Washington, Seattle, Washington 98195, United States of America aff002;  Departments of Biophysics and Biochemistry, UT Southwestern Medical Center, Dallas, Texas, United States of America aff003;  Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America aff004;  Department of Physiology & Biophysics, University of Washington, Seattle, Washington, United States of America aff005
Vyšlo v časopise: Kinetochore-associated Stu2 promotes chromosome biorientation in vivo. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008423
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008423

Souhrn

Accurate segregation of chromosomes to daughter cells is a critical aspect of cell division. It requires the kinetochores on duplicated chromosomes to biorient, attaching to microtubules from opposite poles of the cell. Bioriented attachments come under tension, while incorrect attachments lack tension and must be released to allow proper attachments to form. A well-studied error correction pathway is mediated by the Aurora B kinase, which destabilizes low tension-bearing attachments. We recently discovered that in vitro, kinetochores display an additional intrinsic tension-sensing pathway that utilizes Stu2. The contribution of kinetochore-associated Stu2 to error correction in cells, however, was unknown. Here, we identify a Stu2 mutant that abolishes its kinetochore function and show that it causes biorientation defects in vivo. We also show that this Stu2-mediated pathway functions together with the Aurora B-mediated pathway. Altogether, our work indicates that cells employ multiple pathways to ensure biorientation and the accuracy of chromosome segregation.

Klíčová slova:

Auxins – Cell cycle and cell division – Immunoprecipitation – Metaphase – Microtubules – Protein domains – Saccharomyces cerevisiae – Aurora


Zdroje

1. Targa A, Rancati G. Cancer: a CINful evolution. Curr Opin Cell Biol. 2018;52: 136–144. doi: 10.1016/j.ceb.2018.03.007 29625384

2. Lampson MA, Grishchuk EL. Mechanisms to Avoid and Correct Erroneous Kinetochore-Microtubule Attachments. Biology. 2017;6. doi: 10.3390/biology6010001 28067761

3. Nicklas RB, Koch CA. Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol. 1969;43: 40–50. doi: 10.1083/jcb.43.1.40 5824068

4. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 1999;13: 532–544. doi: 10.1101/gad.13.5.532 10072382

5. Cheeseman IM, Anderson S, Jwa M, Green EM, seog Kang J, Yates JR 3rd, et al. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell. 2002;111: 163–172. doi: 10.1016/s0092-8674(02)00973-x 12408861

6. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED. Kinetochore Microtubule Dynamics and Attachment Stability Are Regulated by Hec1. Cell. 2006;127: 969–982. doi: 10.1016/j.cell.2006.09.047 17129782

7. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, et al. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol. 2003;161: 281–294. doi: 10.1083/jcb.200208092 12707311

8. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, et al. Evidence that the Ipl1-Sli15 (Aurora Kinase-INCENP) Complex Promotes Chromosome Bi-orientation by Altering Kinetochore-Spindle Pole Connections. Cell. 2002;108: 317–329. doi: 10.1016/s0092-8674(02)00633-5 11853667

9. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, et al. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature. 2010;468: 576–579. doi: 10.1038/nature09594 21107429

10. Miller MP, Asbury CL, Biggins S. A TOG Protein Confers Tension Sensitivity to Kinetochore-Microtubule Attachments. Cell. 2016;165: 1428–1439. doi: 10.1016/j.cell.2016.04.030 27156448

11. Al-Bassam J, Chang F. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 2011;21: 604–614. doi: 10.1016/j.tcb.2011.06.007 21782439

12. Al-Bassam J, van Breugel M, Harrison SC, Hyman A. Stu2p binds tubulin and undergoes an open-to-closed conformational change. J Cell Biol. 2006;172: 1009–1022. doi: 10.1083/jcb.200511010 16567500

13. Kosco KA, Pearson CG, Maddox PS, Wang PJ, Adams IR, Salmon ED, et al. Control of microtubule dynamics by Stu2p is essential for spindle orientation and metaphase chromosome alignment in yeast. Mol Biol Cell. 2001;12: 2870–2880. doi: 10.1091/mbc.12.9.2870 11553724

14. Pearson CG, Maddox PS, Zarzar TR, Salmon ED, Bloom K. Yeast kinetochores do not stabilize Stu2p-dependent spindle microtubule dynamics. Mol Biol Cell. 2003;14: 4181–4195. doi: 10.1091/mbc.E03-03-0180 14517328

15. Ayaz P, Ye X, Huddleston P, Brautigam CA, Rice LM. A TOG:αβ-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science. 2012;337: 857–860. doi: 10.1126/science.1221698 22904013

16. Ayaz P, Munyoki S, Geyer EA, Piedra F-A, Vu ES, Bromberg R, et al. A tethered delivery mechanism explains the catalytic action of a microtubule polymerase. eLife. 2014;3: e03069. doi: 10.7554/eLife.03069 25097237

17. Fox JC, Howard AE, Currie JD, Rogers SL, Slep KC. The XMAP215 family drives microtubule polymerization using a structurally diverse TOG array. Mol Biol Cell. 2014;25: 2375–2392. doi: 10.1091/mbc.E13-08-0501 24966168

18. Geyer EA, Miller MP, Brautigam CA, Biggins S, Rice LM. Design principles of a microtubule polymerase. eLife. 2018;7: e34574. doi: 10.7554/eLife.34574 29897335

19. Wang PJ, Huffaker TC. Stu2p: A microtubule-binding protein that is an essential component of the yeast spindle pole body. J Cell Biol. 1997;139: 1271–1280. doi: 10.1083/jcb.139.5.1271 9382872

20. Usui T, Maekawa H, Pereira G, Schiebel E. The XMAP215 homologue Stu2 at yeast spindle pole bodies regulates microtubule dynamics and anchorage. EMBO J. 2003;22: 4779–4793. doi: 10.1093/emboj/cdg459 12970190

21. Wolyniak MJ, Blake-Hodek K, Kosco K, Hwang E, You L, Huffaker TC. The Regulation of Microtubule Dynamics in Saccharomyces cerevisiae by Three Interacting Plus-End Tracking Proteins. Mol Biol Cell. 2006;17: 2789–2798. doi: 10.1091/mbc.E05-09-0892 16571681

22. Humphrey L, Felzer-Kim I, Joglekar AP. Stu2 acts as a microtubule destabilizer in metaphase budding yeast spindles. Mol Biol Cell. 2018;29: 247–255. doi: 10.1091/mbc.E17-08-0494 29187578

23. Goshima G, Yanagida M. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell. 2000;100: 619–633. doi: 10.1016/s0092-8674(00)80699-6 10761928

24. He X, Rines DR, Espelin CW, Sorger PK. Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell. 2001;106: 195–206. doi: 10.1016/s0092-8674(01)00438-x 11511347

25. Pearson CG, Maddox PS, Salmon ED, Bloom K. Budding yeast chromosome structure and dynamics during mitosis. J Cell Biol. 2001;152: 1255–1266. doi: 10.1083/jcb.152.6.1255 11257125

26. Hsu K-S, Toda T. Ndc80 internal loop interacts with Dis1/TOG to ensure proper kinetochore-spindle attachment in fission yeast. Curr Biol CB. 2011;21: 214–220. doi: 10.1016/j.cub.2010.12.048 21256022

27. Tang NH, Takada H, Hsu K-S, Toda T. The internal loop of fission yeast Ndc80 binds Alp7/TACC-Alp14/TOG and ensures proper chromosome attachment. Mol Biol Cell. 2013;24: 1122–1133. doi: 10.1091/mbc.E12-11-0817 23427262

28. Kim JO, Zelter A, Umbreit NT, Bollozos A, Riffle M, Johnson R, et al. The Ndc80 complex bridges two Dam1 complex rings. eLife. 2017;6. doi: 10.7554/eLife.21069 28191870

29. Tien JF, Umbreit NT, Zelter A, Riffle M, Hoopmann MR, Johnson RS, et al. Kinetochore biorientation in Saccharomyces cerevisiae requires a tightly folded conformation of the Ndc80 complex. Genetics. 2014;198: 1483–1493. doi: 10.1534/genetics.114.167775 25230952

30. Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell. 1992;71: 1223–1237. doi: 10.1016/s0092-8674(05)80070-4 1473154

31. van Breugel M, Drechsel D, Hyman A. Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-associated proteins is a plus end-binding microtubule destabilizer. J Cell Biol. 2003;161: 359–369. doi: 10.1083/jcb.200211097 12719475

32. Stangier MM, Kumar A, Chen X, Farcas A-M, Barral Y, Steinmetz MO. Structure-Function Relationship of the Bik1-Bim1 Complex. Structure. 2018;26: 607–618.e4. doi: 10.1016/j.str.2018.03.003 29576319

33. Franck AD, Powers AF, Gestaut DR, Davis TN, Asbury CL. Direct physical study of kinetochore-microtubule interactions by reconstitution and interrogation with an optical force clamp. Methods San Diego Calif. 2010;51: 242–250. doi: 10.1016/j.ymeth.2010.01.020 20096784

34. Powers AF, Franck AD, Gestaut DR, Cooper J, Gracyzk B, Wei RR, et al. The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell. 2009;136: 865–875. doi: 10.1016/j.cell.2008.12.045 19269365

35. Marco E, Dorn JF, Hsu P, Jaqaman K, Sorger PK, Danuser G. S. cerevisiae chromosomes biorient via gradual resolution of syntely between S phase and anaphase. Cell. 2013;154: 1127–1139. doi: 10.1016/j.cell.2013.08.008 23993100

36. Severin F, Habermann B, Huffaker T, Hyman T. Stu2 promotes mitotic spindle elongation in anaphase. J Cell Biol. 2001;153: 435–442. doi: 10.1083/jcb.153.2.435 11309422

37. Pinsky BA, Kung C, Shokat KM, Biggins S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol. 2006;8: 78–83. doi: 10.1038/ncb1341 16327780

38. Lischetti T, Nilsson J. Regulation of mitotic progression by the spindle assembly checkpoint. Mol Cell Oncol. 2015;2: e970484. doi: 10.4161/23723548.2014.970484 27308407

39. Straight AF, Belmont AS, Robinett CC, Murray AW. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol CB. 1996;6: 1599–1608. doi: 10.1016/s0960-9822(02)70783-5 8994824

40. Biggins S, Murray AW. The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev. 2001;15: 3118–3129. doi: 10.1101/gad.934801 11731476

41. Haase KP, Fox JC, Byrnes AE, Adikes RC, Speed SK, Haase J, et al. Stu2 uses a 15-nm parallel coiled coil for kinetochore localization and concomitant regulation of the mitotic spindle. Mol Biol Cell. 2018;29: 285–294. doi: 10.1091/mbc.E17-01-0057 29187574

42. Aravamudhan P, Felzer-Kim I, Gurunathan K, Joglekar AP. Assembling the protein architecture of the budding yeast kinetochore-microtubule attachment using FRET. Curr Biol CB. 2014;24: 1437–1446. doi: 10.1016/j.cub.2014.05.014 24930965

43. Dhatchinamoorthy K, Shivaraju M, Lange JJ, Rubinstein B, Unruh JR, Slaughter BD, et al. Structural plasticity of the living kinetochore. J Cell Biol. 2017;216: 3551–3570. doi: 10.1083/jcb.201703152 28939613

44. Dhatchinamoorthy K, Unruh JR, Lange JJ, Levy M, Slaughter BD, Gerton JL. The stoichiometry of the outer kinetochore is modulated by microtubule-proximal regulatory factors. J Cell Biol. 2019; jcb.201810070. doi: 10.1083/jcb.201810070 31118239

45. Charrasse S, Mazel M, Taviaux S, Berta P, Chow T, Larroque C. Characterization of the cDNA and pattern of expression of a new gene over-expressed in human hepatomas and colonic tumors. Eur J Biochem FEBS. 1995;234: 406–413.

46. Charrasse S, Schroeder M, Gauthier-Rouviere C, Ango F, Cassimeris L, Gard DL, et al. The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215. J Cell Sci. 1998;111 (Pt 10): 1371–1383.

47. Sarangapani KK, Akiyoshi B, Duggan NM, Biggins S, Asbury CL. Phosphoregulation promotes release of kinetochores from dynamic microtubules via multiple mechanisms. Proc Natl Acad Sci U S A. 2013;110: 7282–7287. doi: 10.1073/pnas.1220700110 23589891

48. Sherman F, Fink G, Lawrence C. Methods in Yeast Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 1974.

49. Shonn MA, Murray AL, Murray AW. Spindle Checkpoint Component Mad2 Contributes to Biorientation of Homologous Chromosomes. Curr Biol. 2003;13: 1979–1984. doi: 10.1016/j.cub.2003.10.057 14614824

50. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14: 953–961. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U 9717241

51. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods. 2009;6: 917–922. doi: 10.1038/nmeth.1401 19915560

52. Liu H, Naismith JH. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 2008;8: 91. doi: 10.1186/1472-6750-8-91 19055817

53. Tseng W-C, Lin J-W, Wei T-Y, Fang T-Y. A novel megaprimed and ligase-free, PCR-based, site-directed mutagenesis method. Anal Biochem. 2008;375: 376–378. doi: 10.1016/j.ab.2007.12.013 18198125

54. Sarangapani KK, Duro E, Deng Y, Alves F de L, Ye Q, Opoku KN, et al. Sister kinetochores are mechanically fused during meiosis I in yeast. Science. 2014;346: 248–251. doi: 10.1126/science.1256729 25213378

55. Burnette WN. “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate—polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981;112: 195–203. doi: 10.1016/0003-2697(81)90281-5 6266278

56. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnol Read Mass. 1992;24: 145–149.

57. Tien JF, Umbreit NT, Gestaut DR, Franck AD, Cooper J, Wordeman L, et al. Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J Cell Biol. 2010;189: 713–723. doi: 10.1083/jcb.200910142 20479468

58. Wei RR, Sorger PK, Harrison SC. Molecular organization of the Ndc80 complex, an essential kinetochore component. Proc Natl Acad Sci U S A. 2005;102: 5363–5367. doi: 10.1073/pnas.0501168102 15809444

59. Zelter A, Bonomi M, Kim J ook, Umbreit NT, Hoopmann MR, Johnson R, et al. The molecular architecture of the Dam1 kinetochore complex is defined by cross-linking based structural modelling. Nat Commun. 2015;6: 8673. doi: 10.1038/ncomms9673 26560693

60. Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30: 918–920. doi: 10.1038/nbt.2377 23051804

61. Eng JK, Jahan TA, Hoopmann MR. Comet: an open-source MS/MS sequence database search tool. Proteomics. 2013;13: 22–24. doi: 10.1002/pmic.201200439 23148064

62. Hoopmann MR, Zelter A, Johnson RS, Riffle M, MacCoss MJ, Davis TN, et al. Kojak: efficient analysis of chemically cross-linked protein complexes. J Proteome Res. 2015;14: 2190–2198. doi: 10.1021/pr501321h 25812159

63. Käll L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods. 2007;4: 923–925. doi: 10.1038/nmeth1113 17952086

64. Riffle M, Jaschob D, Zelter A, Davis TN. ProXL (Protein Cross-Linking Database): A Platform for Analysis, Visualization, and Sharing of Protein Cross-Linking Mass Spectrometry Data. J Proteome Res. 2016;15: 2863–2870. doi: 10.1021/acs.jproteome.6b00274 27302480

65. Umbreit NT, Gestaut DR, Tien JF, Vollmar BS, Gonen T, Asbury CL, et al. The Ndc80 kinetochore complex directly modulates microtubule dynamics. Proc Natl Acad Sci U S A. 2012;109: 16113–16118. doi: 10.1073/pnas.1209615109 22908300

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