Home LiteratureArticle Details
PMID: 10085293 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p.

The Journal of cell biology ·Vol. 144 ·No. 5 ·1999-03-08 ·Pages 947-61

Lee L, Klee SK, Evangelista M, Boone C, Pellman D

Abstract

Alignment of the mitotic spindle with the axis of cell division is an essential process in Saccharomyces cerevisiae that is mediated by interactions between cytoplasmic microtubules and the cell cortex. We found that a cortical protein, the yeast formin Bni1p, was required for spindle orientation. Two striking abnormalities were observed in bni1Delta cells. First, the initial movement of the spindle pole body (SPB) toward the emerging bud was defective. This phenotype is similar to that previously observed in cells lacking the kinesin Kip3p and, in fact, BNI1 and KIP3 were found to be in the same genetic pathway. Second, abnormal pulling interactions between microtubules and the cortex appeared to cause preanaphase spindles in bni1Delta cells to transit back and forth between the mother and the bud. We therefore propose that Bni1p may localize or alter the function of cortical microtubule-binding sites in the bud. Additionally, we present evidence that other bipolar bud site determinants together with cortical actin are also required for spindle orientation.

MeSH Terms
Actins/metabolism Base Sequence Binding Sites DNA Primers Fungal Proteins/metabolism,physiology Microfilament Proteins/metabolism,physiology Microscopy, Fluorescence Microtubules Molecular Sequence Data Saccharomyces cerevisiae/cytology,genetics,physiology Saccharomyces cerevisiae Proteins Spindle Apparatus/physiology
Chemicals
Actins BUD6 protein, S cerevisiae Bni1 protein, S cerevisiae DNA Primers Fungal Proteins Microfilament Proteins Saccharomyces cerevisiae Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lee L
Department of Pediatric Oncology, The Dana-Farber Cancer Institute and Department of Pediatric Hematology, The Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA.
Klee S K
Evangelista M
Boone C
Pellman D
References (71)
71 references, click to expand
  1. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity.
    Mol Biol Cell. 1993 Dec;4(12):1307-16 PMID: 8167411
  2. The role of Saccharomyces cerevisiae coronin in the actin and microtubule cytoskeletons.
    Curr Biol. 1998 Nov 19;8(23):1281-4 PMID: 9822583
  3. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast.
    J Cell Biol. 1998 Jan 26;140(2):377-90 PMID: 9442113
  4. Kinesin-related KIP3 of Saccharomyces cerevisiae is required for a distinct step in nuclear migration.
    J Cell Biol. 1997 Sep 8;138(5):1023-40 PMID: 9281581
  5. Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Mar;11(3):1295-305 PMID: 1996092
  6. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast.
    J Cell Biol. 1999 Jan 11;144(1):83-98 PMID: 9885246
  7. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1995 May;129(3):751-65 PMID: 7730409
  8. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene.
    Development. 1994 Dec;120(12):3367-77 PMID: 7821209
  9. The plant cytoskeleton.
    Curr Opin Cell Biol. 1991 Feb;3(1):33-42 PMID: 1854481
  10. Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae.
    J Cell Biol. 1991 Aug;114(3):515-32 PMID: 1860883
  11. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae.
    J Cell Biol. 1992 Nov;119(3):583-93 PMID: 1400594
  12. Origins of cell polarity.
    Cell. 1996 Feb 9;84(3):335-44 PMID: 8608587
  13. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  14. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site.
    Mol Biol Cell. 1993 Dec;4(12):1277-94 PMID: 8167410
  15. Identification of a tRNA(Gln) ochre suppressor in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1992 Sep 11;20(17):4661 PMID: 1408770
  16. Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins.
    J Cell Biol. 1997 Sep 8;138(5):1041-53 PMID: 9281582
  17. Pea2 protein of yeast is localized to sites of polarized growth and is required for efficient mating and bipolar budding.
    J Cell Biol. 1996 Nov;135(3):725-39 PMID: 8909546
  18. Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis.
    Genes Dev. 1998 Feb 1;12(3):396-410 PMID: 9450933
  19. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  20. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans.
    J Cell Biol. 1987 Nov;105(5):2123-35 PMID: 3680373
  21. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis.
    Cell. 1995 Aug 25;82(4):631-41 PMID: 7664342
  22. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis.
    Mol Cell Biol. 1998 Jul;18(7):4053-69 PMID: 9632790
  23. Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae.
    J Cell Biol. 1995 Aug;130(3):687-700 PMID: 7622568
  24. Nuclear and spindle dynamics in budding yeast.
    Mol Biol Cell. 1998 Jul;9(7):1627-31 PMID: 9658159
  25. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites.
    Mol Biol Cell. 1997 Apr;8(4):729-53 PMID: 9247651
  26. A role for the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection.
    J Cell Biol. 1997 Jan 13;136(1):111-23 PMID: 9008707
  27. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position.
    J Cell Biol. 1989 Sep;109(3):1185-93 PMID: 2768338
  28. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast.
    Genes Dev. 1995 Aug 1;9(15):1817-30 PMID: 7649470
  29. 'Formins': proteins deduced from the alternative transcripts of the limb deformity gene.
    Nature. 1990 Aug 30;346(6287):850-3 PMID: 2392150
  30. Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud.
    J Cell Biol. 1997 Nov 17;139(4):985-94 PMID: 9362516
  31. The Rho-GEF Rom2p localizes to sites of polarized cell growth and participates in cytoskeletal functions in Saccharomyces cerevisiae.
    Mol Biol Cell. 1997 Oct;8(10):1829-44 PMID: 9348527
  32. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells.
    Mol Biol Cell. 1996 Feb;7(2):225-32 PMID: 8688554
  33. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae.
    Genes Dev. 1994 May 1;8(9):1087-105 PMID: 7926789
  34. The SPA2 protein of yeast localizes to sites of cell growth.
    J Cell Biol. 1989 Apr;108(4):1419-29 PMID: 2647769
  35. Targeting, capture, and stabilization of microtubules at early focal adhesions.
    J Cell Biol. 1998 Jul 13;142(1):181-90 PMID: 9660872
  36. The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization.
    J Cell Biol. 1999 Mar 8;144(5):963-75 PMID: 10085294
  37. Assay of yeast mating reaction.
    Methods Enzymol. 1991;194:77-93 PMID: 2005823
  38. Amplification with arbitrary primers.
    Methods Mol Biol. 1996;54:123-9 PMID: 8597783
  39. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex.
    J Cell Biol. 1997 Aug 11;138(3):629-41 PMID: 9245791
  40. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins.
    Cell. 1996 Mar 8;84(5):687-97 PMID: 8625407
  41. APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle.
    Science. 1997 Feb 28;275(5304):1311-4 PMID: 9036857
  42. Yeast Num1p associates with the mother cell cortex during S/G2 phase and affects microtubular functions.
    J Cell Biol. 1995 Nov;131(4):1003-14 PMID: 7490278
  43. Spindle positioning and cell polarity.
    Curr Biol. 1992 Sep;2(9):469-71 PMID: 15335895
  44. Generation of cell polarity in yeast.
    Curr Opin Cell Biol. 1996 Aug;8(4):557-65 PMID: 8791457
  45. Motoring to the finish: kinesin and dynein work together to orient the yeast mitotic spindle.
    J Cell Biol. 1997 Sep 8;138(5):957-60 PMID: 9281575
  46. Actin cytoskeleton: are FH proteins local organizers?
    Curr Biol. 1997 Jul 1;7(7):R414-7 PMID: 9210364
  47. Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae.
    J Cell Biol. 1995 Sep;130(6):1373-85 PMID: 7559759
  48. Characterization of fus1 of Schizosaccharomyces pombe: a developmentally controlled function needed for conjugation.
    Mol Cell Biol. 1995 Jul;15(7):3697-707 PMID: 7791776
  49. ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Oct;16(10):5264-75 PMID: 8816439
  50. Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Oct 23;273(43):28341-5 PMID: 9774458
  51. Review: an overview of the Saccharomyces cerevisiae microtubule and microfilament cytoskeleton.
    Yeast. 1997 Apr;13(5):399-434 PMID: 9153752
  52. The Aspergillus nidulans sepA gene encodes an FH1/2 protein involved in cytokinesis and the maintenance of cellular polarity.
    EMBO J. 1997 Jun 16;16(12):3474-83 PMID: 9218790
  53. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis.
    Science. 1997 Apr 4;276(5309):118-22 PMID: 9082982
  54. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae.
    EMBO J. 1997 May 15;16(10):2745-55 PMID: 9184220
  55. Kinetics of spindle pole body separation in budding yeast.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9707-11 PMID: 7568202
  56. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1857-70 PMID: 8657162
  57. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A.
    J Cell Biol. 1997 Apr 21;137(2):399-416 PMID: 9128251
  58. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae.
    EMBO J. 1996 Nov 15;15(22):6060-8 PMID: 8947028
  59. Bud position in Saccharomyces cerevisiae.
    J Bacteriol. 1960 Oct;80:567-8 PMID: 13701687
  60. Evidence for an involvement of actin in the positioning and motility of centrosomes.
    J Cell Biol. 1985 Jul;101(1):96-103 PMID: 4040137
  61. Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 May;9(5):1221-33 PMID: 9571251
  62. Mitosis in living budding yeast: anaphase A but no metaphase plate.
    Science. 1997 Jul 25;277(5325):574-8 PMID: 9228009
  63. The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast.
    Mol Biol Cell. 1998 Aug;9(8):2051-68 PMID: 9693366
  64. Morphogenetic properties of microtubules and mitotic spindle assembly.
    Cell. 1996 Feb 9;84(3):401-10 PMID: 8608594
  65. The dynamics of chromosome movement in the budding yeast Saccharomyces cerevisiae.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3355-66 PMID: 2689456
  66. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae.
    Genetics. 1997 Mar;145(3):671-84 PMID: 9055077
  67. Fluorescence microscopy methods for yeast.
    Methods Cell Biol. 1989;31:357-435 PMID: 2476649
  68. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin.
    J Cell Biol. 1997 Apr 7;137(1):169-82 PMID: 9105045
  69. Role of inscuteable in orienting asymmetric cell divisions in Drosophila.
    Nature. 1996 Sep 5;383(6595):50-5 PMID: 8779714
  70. Spindle orientation and asymmetric cell fate.
    Cell. 1995 Aug 25;82(4):523-6 PMID: 7664329
  71. Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus.
    Genes Dev. 1995 Oct 15;9(20):2482-94 PMID: 7590229
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1999-03-08
Pages
947-61
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2148193
Subset
IM
Grants
NIGMS NIH HHS · GM55772 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]