The fission yeast spindle orientation checkpoint: A model that generates tension?

Yeast

Volumn 23, Issue 13, 2006, Pages 1015-1029

  Gachet, Yannick ^a   Reyes, Céline ^a   Goldstone, Sherilyn ^a   Tournier, Sylvie ^a  

^a Université de Toulouse Paul Sabatier   (France)

Author keywords

Actin; Astral microtubule; Fission yeast; Mitosis; Spindle orientation

Indexed keywords

ACTIN;

ANAPHASE; BIOLOGICAL MODEL; CELL DIVISION; CELL FATE; CELL POLARITY; CHROMOSOME SEGREGATION; CYTOSKELETON; EUKARYOTE; INVERTEBRATE; METAPHASE; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

CELL DIVISION; CELL POLARITY; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; SCHIZOSACCHAROMYCES;

EUKARYOTA; INVERTEBRATA; SCHIZOSACCHAROMYCES POMBE;

EID: 33751263849     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1410     Document Type: Review

References (82)

1. Asakawa K, Toda T. 2006. Cooperation of EB1-Mal3 and the Bub1 spindle checkpoint. Cell Cycle 5: 27-30.
2. Asakawa K, Toya M, Sato M, et al. 2005. Mal3, the fission yeast EB1 homologue, cooperates with Bub1 spindle checkpoint to prevent monopolar attachment. EMBO Rep 6: 1194-1200.
3. Bahler J, Steever AB, Wheatley S, et al. 1998. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J Cell Biol 143: 1603-1616.
4. Bai SW, Rouquette J, Umeda M, et al. 2004. The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Mol Cell Biol 24: 6379-6392.
5. Banuett F, Herskowitz I. 2002. Bud morphogenesis and the actin and microtubule cytoskeletons during budding in the corn smut fungus, Ustilago maydis. Fung Genet Biol 37: 149-170.
6. Beach DL, Thibodeaux J, Maddox P, Yeh E, Bloom K. 2000. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr Biol 10: 1497-1506.
7. Bernard P, Hardwick K, Javerzat JP. 1998. Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J Cell Biol 143: 1775-1787.
8. Burgess DR, Chang F. 2005. Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol 15: 156-162.
9. Chang F, Woollard A, Nurse P. 1996. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J Cell Sci 109(1): 131-142.
10. Cleveland DW, Mao Y, Sullivan KF. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421.
11. Ding R, McDonald KL, McIntosh JR. 1993. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe. J Cell Biol 120: 141-151.
12. Ding R, West RR, Morphew DM, Oakley BR, McIntosh JR. 1997. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds. Mol Biol Cell 8: 1461-1479.
13. Fankhauser C, Reymond A, Cerutti L, et al. 1995. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 82: 435-444.
14. Farr KA, Hoyt MA. 1998. Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint. Mol Cell Biol 18: 2738-2747.
15. Feierbach B, Chang F. 2001. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr Biol 11: 1656-1665.
16. Gachet Y, Tournier S, Millar JB, Hyams JS. 2001. A MAP kinase-dependent actin checkpoint ensures proper spindle orientation in fission yeast. Nature 412: 352-355.
17. Gachet Y, Tournier S, Millar JB, Hyams JS. 2004. Mechanism controlling perpendicular alignment of the spindle to the axis of cell division in fission yeast. EMBO J 23: 1289-1300.
18. Giansanti MG, Gatti M, Bonaccorsi S. 2001. The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 128: 1137-1145.
19. Gillett ES, Espelin CW, Sorger PK. 2004. Spindle checkpoint proteins and chromosome- microtubule attachment in budding yeast. J Cell Biol 164: 535-546.
20. Hagan I, Yanagida M. 1997. Evidence for cell cycle-specific, spindle pole body-mediated, nuclear positioning in the fission yeast Schizosaccharomyces pombe. J Cell Sci 110(16): 1851-1866.
21. Hagan IM, Hyams JS. 1996. Forces acting on the fission yeast anaphase spindle. Cell Motil Cytoskel 34: 69-75.
22. Hardwick KG, Weiss E, Luca FC, Winey M, Murray AW. 1996. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273: 953-956.
23. He X, Patterson TE, Sazer S. 1997. The Schizosaccharomyces pombe spindle checkpoint protein mad2p blocks anaphase and genetically interacts with the anaphase-promoting complex. Proc Natl Acad Sci USA 94: 7965-7970.
24. Huisman SM, Segal M. 2005. Cortical capture of microtubules and spindle polarity in budding yeast - where's the catch? J Cell Sci 118: 463-471.
25. Ikui AE, Furuya K, Yanagida M, Matsumoto T. 2002. Control of localization of a spindle checkpoint protein, Mad2, in fission yeast. J Cell Sci 115: 1603-1610.
26. Ishiguro J, Kobayashi W. 1996. An actin point-mutation neighboring the 'hydrophobic plug' causes defects in the maintenance of cell polarity and septum organization in the fission yeast Schizosaccharomyces pombe. FEBS Lett 392: 237-241.
27. King JM, Nicklas RB. 2000. Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J Cell Sci 113(21): 3815-3823.
28. Krapp A, Schmidt S, Cano E, Simanis V. 2001. S. pombe cdc11p, together with sid4p, provides an anchor for septation initiation network proteins on the spindle pole body. Curr Biol 11: 1559-1568.
29. Kusch J, Liakopoulos D, Barral Y. 2003. Spindle asymmetry: a compass for the cell. Trends Cell Biol 13: 562-569.
30. Labbe JC, Maddox PS, Salmon ED, Goldstein B. 2003. PAR proteins regulate microtubule dynamics at the cell cortex in C. elegans. Curr Biol 13: 707-714.
31. Lenart P, Bacher CP, Daigle N, et al. 2005. A contractile nuclear actin network drives chromosome congression in oocytes. Nature 436: 812-818.
32. Li R, Murray AW. 1991. Feedback control of mitosis in budding yeast. Cell 66: 519-531.
33. Li X, Nicklas RB. 1995. Mitotic forces control a cell-cycle checkpoint. Nature 373: 630-632.
34. Louvet-Vallee S, Vinot S, Maro B. 2005. Mitotic spindles and cleavage planes are oriented randomly in the two-cell mouse embryo. Curr Biol 15: 464-469.
35. Marks J, Hagan IM, Hyams JS. 1986. Growth polarity and cytokinesis in fission yeast: the role of the cytoskeleton. J Cell Sci (suppl 5): 229-241.
36. McCully EK, Robinow CF. 1971. Mitosis in the fission yeast Schizosaccharomyces pombe: a comparative study with light and electron microscopy. J Cell Sci 9: 475-507.
37. Motegi F, Arai R, Mabuchi I. 2001. Identification of two type V myosins in fission yeast, one of which functions in polarized cell growth and moves rapidly in the cell. Mol Biol Cell 12: 1367-1380.
38. Motegi F, Velarde NV, Piano F, Sugimoto A. 2006. Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev Cell 10: 509-520.
39. Nabeshima K, Nakagawa T, Straight AF, et al. 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.
40. O'Connell CB, Wang YL. 2000. Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. Mol Biol Cell 11: 1765-1774.
41. Oliferenko S, Balasubramanian MK. 2002. Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4: 816-820.
42. Paoletti A, Chang F. 2000. Analysis of midlp, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast. Mol Biol Cell 11: 2757-2773.
43. Petersen J, Hagan IM. 2005. Polo kinase links the stress pathway to cell cycle control and tip growth in fission yeast. Nature 435: 507-512.
44. Pines J. 2006. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol 16: 55-63.
45. Rajagopalan S, Bimbo A, Balasubramanian MK, Oliferenko S. 2004. A potential tension-sensing mechanism that ensures timely anaphase onset upon metaphase spindle orientation. Curr Biol 14: 69-74.
46. Rhyu MS, Knoblich JA. 1995. Spindle orientation and asymmetric cell fate. Cell 82: 523-526.
47. Rieder CL, Cole RW, Khodjakov A, Sluder G. 1995. The checkpoint delaying anaphase in response to chromosome moncorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130: 941-948.
48. Sagolla MJ, Uzawa S, Cande WZ. 2003. Individual microtubule dynamics contribute to the function of mitotic and cytoplasmic arrays in fission yeast. J Cell Sci 116: 4891-4903.
49. Samejima I, Lourenco PC, Snaith HA, Sawin KE. 2005. Fission yeast mto2p regulates microtubule nucleation by the centrosomin-related protein mto1p. Mol Biol Cell 16: 3040-3051.
50. Sato M, Koonrugsa N, Toda T, et al. 2003. Deletion of Mia1/Alp7 activates Mad2-dependent spindle assembly checkpoint in fission yeast. Nat Cell Biol 5: 764-766; author reply 766.
51. Sato M, Vardy L, Angel Garcia M, Koonrugsa N, Toda T. 2004. Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol Biol Cell 15: 1609-1622.
52. Sawin KE, Lourenco PC, Snaith HA. 2004. Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr Biol 14: 763-775.
53. Shannon KB, Canman JC, Salmon ED. 2002. Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol Biol Cell 13: 3706-3719.
54. Shiozaki K, Russell P. 1996. Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev 10: 2276-2288.
55. Skoufias DA, Andreassen PR, Lacroix FB, Wilson L, Margolis RL. 2001. Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc Natl Acad Sci USA 98: 4492-4497.
56. Sohrmann M, Fankhauser C, Brodbeck C, Simanis V. 1996. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev 10: 2707-2719.
57. Stern BM, Murray AW. 2001. Lack of tension at kinetochores activates the spindle checkpoint in budding yeast. Curr Biol 11: 1462-1467.
58. Tanaka K, Kanbe T. 1986. Mitosis in the fission yeast Schizosaccharomyces pombe as revealed by freeze-substitution electron microscopy. J Cell Sci 80: 253-268.
59. Tatebe H, Goshima G, Takeda K, et al. 2001. Fission yeast living mitosis visualized by GFP-tagged gene products. Micron 32: 67-74.
60. Tatebe H, Shimada K, Uzawa S, Morigasaki S, Shiozaki K. 2005. Wsh3/Tea4 is a novel cell-end factor essential for bipolar distribution of Tea1 and protects cell polarity under environmental stress in S. pombe. Curr Biol 15: 1006-1015.
61. Taylor SS, Ha E, McKeon F. 1998. The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J Cell Biol 142: 1-11.
62. Thery M, Pepin A, Dressaire E, Chen Y, Bornens M. 2006. Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil Cytoskel 63: 341-355.
63. Tolic-Norrelykke IM, Sacconi L, Thou G, Pavone FS. 2004. Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr Biol 14: 1181-1186.
64. Tomonaga T, Nagao K, Kawasaki Y, et al. 2000. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14: 2757-2770.
65. Tournier S, Gachet Y, Buck V, Hyams JS, Millar JB. 2004. Disruption of astral microtubule contact with the cell cortex activates a Bub1, Bub3, and Mad3-dependent checkpoint in fission yeast. Mol Biol Cell 15: 3345-3356.
66. Uhlmann F, Lottspeich F, Nasmyth K. 1999. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Sccl. Nature 400: 37-42.
67. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K. 2000. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103: 375-386.
68. Vanoosthuyse V, Valsdottir R, Javerzat JP, Hardwick KG. 2004. Kinetochore targeting of fission yeast Mad and Bub proteins is essential for spindle checkpoint function but not for all chromosome segregation roles of Bub1p. Mol Cell Biol 24: 9786-9801.
69. Venkatram S, Tasto JJ, Feoktistova A, et al. 2004. Identification and characterization of two novel proteins affecting fission yeast γ-tubulin complex function. Mol Biol Cell 15: 2287-2301.
70. Warren CD, Brady DM, Johnston RC, et al. 2002. Distinct chromosome segregation roles for spindle checkpoint proteins. Mol Biol Cell 13: 3029-3041.
71. Waters JC, Chen RH, Murray AW, Salmon ED. 1998. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 141: 1181-1191.
72. Weiss E, Winey M. 1996. The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132: 111-123.
73. Wilkinson MG, Millar JB. 2000. Control of the eukaryotic cell cycle by MAP kinase signaling pathways. FASEB J 14: 2147-2157.
74. Wilkinson MG, Samuels M, Takeda T, et al. 1996. The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev 10: 2289-2301.
75. Win TZ, Gachet Y, Mulvihill DP, May KM, Hyams JS. 2001. Two type V myosins with non-overlapping functions in the fission yeast Schizosaccharomyces pombe: Myo52 is concerned with growth polarity and cytokinesis, Myo51 is a component of the cytokinetic actin ring. J Cell Sci 114: 69-79.
76. Yamamoto A, West RR, McIntosh JR, Hiraoka Y. 1999. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast. J Cell Biol 145: 1233-1249.
77. Yeh E, Yang C, Chin E, et al. 2000. Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants. Mol Biol Cell 11: 3949-3961.
78. Yin H, Pruyne D, Huffaker TC, Bretscher A. 2000. Myosin V orientates the mitotic spindle in yeast. Nature 406: 1013-1016.
79. Yu H. 2002. Regulation of APC-Cdc20 by the spindle checkpoint. Curr Opin Cell Biol 14: 706-714.
80. Zhou J, Panda D, Landen JW, Wilson L, Joshi HC. 2002. Minor alteration of microtubule dynamics causes loss of tension across kinetochore pairs and activates the spindle checkpoint. J Biol Chem 277: 17200-17208.
81. Zimmerman S, Chang F. 2005. Effects of γ-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Mol Biol Cell 16: 2719-2733.
82. Zimmerman S, Daga RR, Chang F. 2004. Intra-nuclear microtubules and a mitotic spindle orientation checkpoint. Nat Cell Biol 6: 1245-1246.