Genetics, Vol. 149, 1265-1275, July 1998, Copyright © 1998

Isolation and Characterization of New Fission Yeast Cytokinesis Mutants

Mohan K. Balasubramaniana,b, Dannel McColluma,c, Louise Changa, Kelvin C. Y. Wongb, Naweed I. Naqvia,b, Xiangwei Hed, Shelley Sazerd, and Kathleen L. Goulda
a Howard Hughes Medical Institute and Department of Cell Biology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232,
b Institute of Molecular Agrobiology, Singapore 118240,
c Worcester Foundation for Biomedical Research, Shrewsbury, Massachusetts 01545
d Department of Biochemistry, Baylor College of Medicine, Houston, Texas 77030

Corresponding author: Kathleen L. Gould, Howard Hughes Medical Institute and Department of Cell Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, kathy.gould{at}mcmail.vanderbilt.edu (E-mail).

Communicating editor: M. D. ROSE

Schizosaccharomyces pombe is an excellent organism in which to study cytokinesis as it divides by medial fission using an F-actin contractile ring. To enhance our understanding of the cell division process, a large genetic screen was carried out in which 17 genetic loci essential for cytokinesis were identified, 5 of which are novel. Mutants identifying three genes, rng3+, rng4+, and rng5+, were defective in organizing an actin contractile ring. Four mutants defective in septum deposition, septum initiation defective (sid)1, sid2, sid3, and sid4, were also identified and characterized. Genetic analyses revealed that the sid mutants display strong negative interactions with the previously described septation mutants cdc7-24, cdc11-123, and cdc14-118. The rng5+, sid2+, and sid3+ genes were cloned and shown to encode Myo2p (a myosin heavy chain), a protein kinase related to budding yeast Dbf2p, and Spg1p, a GTP binding protein that is a member of the ras superfamily of GTPases, respectively. The ability of Spg1p to promote septum formation from any point in the cell cycle depends on the activity of Sid4p. In addition, we have characterized a phenotype that has not been described previously in cytokinesis mutants, namely the failure to reorganize actin patches to the medial region of the cell in preparation for septum formation.





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J. Cell Sci.Home page
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J. Cell Sci., March 14, 2002; 114(24): 4521 - 4532.
[Abstract] [Full Text] [PDF]


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[Abstract] [Full Text] [PDF]


Home page
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J. Cell Sci., January 11, 2002; 115(21): 3983 - 3990.
[Abstract] [Full Text] [PDF]


Home page
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J. Cell Sci., January 11, 2002; 115(21): 4013 - 4023.
[Abstract] [Full Text] [PDF]


Home page
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J. Cell Sci., January 11, 2002; 115(21): 4081 - 4096.
[Abstract] [Full Text] [PDF]


Home page
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J. Cell Sci., January 3, 2002; 115(5): 887 - 898.
[Abstract] [Full Text] [PDF]


Home page
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[Abstract] [Full Text] [PDF]


Home page
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Mol. Biol. Cell, November 1, 2001; 12(11): 3515 - 3526.
[Abstract] [Full Text] [PDF]


Home page
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Saccharomyces cerevisiae Mob1p Is Required for Cytokinesis and Mitotic Exit
Mol. Cell. Biol., October 15, 2001; 21(20): 6972 - 6983.
[Abstract] [Full Text] [PDF]


Home page
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[Abstract] [Full Text] [PDF]


Home page
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W. Jiang and R. L. Hallberg
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Genetics, August 1, 2001; 158(4): 1413 - 1429.
[Abstract] [Full Text] [PDF]


Home page
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Mol. Biol. Cell, May 1, 2001; 12(5): 1367 - 1380.
[Abstract] [Full Text]


Home page
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[Abstract] [Full Text]


Home page
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Genetics, August 1, 2000; 155(4): 1521 - 1534.
[Abstract] [Full Text]


Home page
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Sid4p is required to localize components of the septation initiation pathway to the spindle pole body in fission yeast
PNAS, May 9, 2000; 97(10): 5249 - 5254.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
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J. Biol. Chem., May 5, 2000; 275(19): 14381 - 14387.
[Abstract] [Full Text] [PDF]


Home page
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Mol. Biol. Cell, February 1, 2000; 11(2): 593 - 611.
[Abstract] [Full Text]


Home page
J. Cell Sci.Home page
L. Frenz, S. Lee, D Fesquet, and L. Johnston
The budding yeast Dbf2 protein kinase localises to the centrosome and moves to the bud neck in late mitosis
J. Cell Sci., January 10, 2000; 113(19): 3399 - 3408.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
K. Wong, N. Naqvi, Y Iino, M Yamamoto, and M. Balasubramanian
Fission yeast Rng3p: an UCS-domain protein that mediates myosin II assembly during cytokinesis
J. Cell Sci., January 7, 2000; 113(13): 2421 - 2432.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
M. Balasubramanian, D McCollum, and U Surana
Tying the knot: linking cytokinesis to the nuclear cycle
J. Cell Sci., January 5, 2000; 113(9): 1503 - 1513.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
E Salimova, M Sohrmann, N Fournier, and V Simanis
The S. pombe orthologue of the S. cerevisiae mob1 gene is essential and functions in signalling the onset of septum formation
J. Cell Sci., January 5, 2000; 113(10): 1695 - 1704.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
F Motegi, K Nakano, and I Mabuchi
Molecular mechanism of myosin-II assembly at the division site in Schizosaccharomyces pombe
J. Cell Sci., January 5, 2000; 113(10): 1813 - 1825.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
J Liu, H Wang, and M. Balasubramanian
A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe
J. Cell Sci., January 4, 2000; 113(7): 1223 - 1230.
[Abstract] [PDF]


Home page
Mol. Biol. CellHome page
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Myosin-II Tails Confer Unique Functions in Schizosaccharomyces pombe: Characterization of a Novel Myosin-II Tail
Mol. Biol. Cell, January 1, 2000; 11(1): 79 - 91.
[Abstract] [Full Text]


Home page
Mol. Biol. CellHome page
J. L. Morrell, M. Morphew, and K. L. Gould
A Mutant of Arp2p Causes Partial Disassembly of the Arp2/3 Complex and Loss of Cortical Actin Function in Fission Yeast
Mol. Biol. Cell, December 1, 1999; 10(12): 4201 - 4215.
[Abstract] [Full Text]


Home page
GeneticsHome page
J. Liu, H. Wang, D. McCollum, and M. K. Balasubramanian
Drc1p/Cps1p, a 1,3-{beta}-Glucan Synthase Subunit, Is Essential for Division Septum Assembly in Schizosaccharomyces pombe
Genetics, November 1, 1999; 153(3): 1193 - 1203.
[Abstract] [Full Text]


Home page
JCBHome page
C. A. Sparks, M. Morphew, and D. McCollum
Sid2p, a Spindle Pole Body Kinase that Regulates the Onset of Cytokinesis
J. Cell Biol., August 23, 1999; 146(4): 777 - 790.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
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Fission Yeast Pob1p, Which Is Homologous to Budding Yeast Boi Proteins and Exhibits Subcellular Localization Close to Actin Patches, Is Essential for Cell Elongation and Separation
Mol. Biol. Cell, August 1, 1999; 10(8): 2745 - 2757.
[Abstract] [Full Text]


Home page
J. Biol. Chem.Home page
D. McCollum, A. Feoktistova, and K. L. Gould
Phosphorylation of the Myosin-II Light Chain Does Not Regulate the Timing of Cytokinesis in Fission Yeast
J. Biol. Chem., June 18, 1999; 274(25): 17691 - 17695.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
K. A. Furge, Q.-c. Cheng, M. Jwa, S. Shin, K. Song, and C. F. Albright
Regions of Byr4, a Regulator of Septation in Fission Yeast, That Bind Spg1 or Cdc16 and Form a Two-component GTPase-activating Protein with Cdc16
J. Biol. Chem., April 16, 1999; 274(16): 11339 - 11343.
[Abstract] [Full Text] [PDF]


Home page
J. Cell Sci.Home page
N Beltraminelli, M Murone, and V Simanis
The S. pombe zfs1 gene is required to prevent septation if mitotic progression is inhibited
J. Cell Sci., January 9, 1999; 112(18): 3103 - 3114.