Role of the spindle-pole-body protein ApsB and the cortex protein ApsA in microtubule organization and nuclear migration in Aspergillus nidulans

Journal of Cell Science

Volumn 118, Issue 16, 2005, Pages 3705-3716

  Veith, Daniel ^a,b   Scherr, Nicole ^a,b   Efimov, Vladimir P ^c   Fischer, Reinhard ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Dynein; Kinesin; Microtubules; MTOC; Nuclear movement; Spindle pole body

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; FUNGAL PROTEIN; KINESIN; MUTANT PROTEIN; PROTEIN APSA; PROTEIN APSB; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; CELL INTERACTION; CELL MIGRATION; CELL NUCLEUS; CELL ORGANELLE; CENTROSOME; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE MICROSCOPY; FUNGUS HYPHAE; GENE MUTATION; IN VIVO STUDY; LETHALITY; MICROTUBULE; MITOSIS SPINDLE; MOLECULAR MODEL; NONHUMAN; NULL ALLELE; OSCILLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINDLE POLE BODY; WILD TYPE;

ASPERGILLUS NIDULANS; CELL MOVEMENT; CELL NUCLEUS; CYTOPLASM; CYTOPLASMIC STREAMING; CYTOSKELETON; DYNEIN ATPASE; FEEDBACK, BIOCHEMICAL; FLUORESCENT DYES; FUNGAL PROTEINS; MEMBRANE PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MOLECULAR MOTOR PROTEINS; MUTATION; NUCLEAR PROTEINS;

EMERICELLA NIDULANS; FUNGI;

EID: 24944501411     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02501     Document Type: Article

References (68)

1. Adams, N. R. and Cooper, J. A. (2000). Microtubule interactions with the cell cortex causing nuclear movements in Saccharomcyces cerevisiae. J. Cell Biol. 149, 863-874.
2. Ahringer, J. (2003). Control of cell polarity and mitotic spindle positioning in animal cells. Curr. Opin. Cell Biol. 15, 73-81.
3. Aramayo, R., Adams, T. H. and Timberlake, W. E. (1989). A large cluster of highly expressed genes is dispensable for growth and development in Aspergillus nidulans. Genetics 122, 65-71.
4. Berns, M. W., Aist, J. R., Wright, W. H. and Liang, H. (1992). Optical trapping in animal and fungal cells using a tunable, near-infrared titanium-sapphire laser. Exp. Cell Res. 198, 375-378.
5. Bloom, K. (2000). It's a kar9ochore to capture microtubules. Nat. Cell Biol. 2, E96-E98.
6. Bloom, K. (2001). Nuclear migration: cortical anchors for cytoplasmic dynein. Curr. Biol. 11, R326-R329.
7. Clutterbuck, A. J. (1969). A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63, 317-327.
8. Clutterbuck, A. J. (1994). Mutants of Aspergillus nidulans deficient in nuclear migration during hyphal growth and conidiation. Microbiology 140, 1169-1174.
9. Cottingham, F. R. and Hoyt, M. A. (1997). Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins. J. Cell Biol. 138, 1041-1053.
10. Cottingham, F. R., Gheber, L., Miller, D. L. and Hoyt, M. A. (1999). Novel roles for Saccharomyces cerevisiae mitotic spindle motors. J. Cell Biol. 147, 335-349.
11. Efimov, V. P. (2003). Roles of NUDE and NUDF protein of Aspergillus nidulans: Insights from intracellular localization and overexpression effects. Mol. Biol. Cell 14, 871-888.
12. Efimov, V. P. and Morris, N. R. (2000). The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J. Cell Biol. 150, 681-688.
13. Farkasovsky, M. and Küntzel, H. (2001). Cortical Num1p interacts with the dynein intermediate chain Pac11p and cytoplasmic microtubules. J. Cell Biol. 152, 251-262.
14. Fernandez-Abalos, J. M., Fox, H., Pitt, C., Wells, B. and Doonan, J. H. (1998). Plant-adapted green fluorescent protein is a versatile vital reporter for gene expression, protein localization and mitosis in the filamentous fungus Aspergillus nidulans. Mol. Microbiol. 27, 121-130.
15. Fischer, R. (1999). Nuclear movement in filamentous fungi. FEMS Microbiol. Rev. 23, 38-69.
16. Fischer, R. and Timberlake, W. E. (1995). Aspergillus nidulans apsA (anucleate primary sterigmata) encodes a coiled-coil protein necessary for nuclear positioning and completion of asexual development. J. Cell Biol. 128, 485-498.
17. PP1 in living hyphae of Aspergillus indicates a novel role in septum formation. Mol. Microbiol. 45, 1219-1230.
18. Gundersen, G. G. and Bretscher, A. (2003). Microtubule asymmetry. Science 300, 2040-2041.
19. Han, G., Liu, B., Zhang, J., Zuo, W., Morris, N. R. and Xiang, X. (2001). The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr. Biol. 11, 19-24.
20. Harris, S. D., Morrell, J. L. and Hamer, J. E. (1994). Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136, 517-532.
21. Hill, T. W. and Käfer, E. (2001). Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet. Newsl. 48, 20-21.
22. v. Mol. Biol. Cell 11, 1197-1211.
23. Inoue, S., Turgeon, B. G., Yoder, O. C. and Aist, J. R. (1998). Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration. J. Cell Sci. 111, 1555-1566.
24. Ketelaar, T., Faivre-Moskalenko, C., Esseling, J. J., de Ruijter, N. C., Grierson, C. S., Dogterom, M. and Emons, A. M. (2002). Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14, 2941-2955.
25. Konzack, S., Rischitor, P., Enke, C. and Fischer, R. (2005). The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans. Mol. Biol. Cell 16, 497-506.
26. Lee, W. L., Oberle, J. R. and Cooper, J. A. (2003). The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J. Cell Biol. 160, 355-364.
27. Maekawa, H., Usui, T., Knop, M. and Schiebel, E. (2003). Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate but cortex interactions. EMBO J. 22, 438-449.
28. Miller, R. K. and Rose, M. D. (1998). Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J. Cell Biol. 140, 377-390.
29. Miller, R. K., Heller, K. K., Frisèn, L., Wallack, D. L., Loayza, D., Gammie, A. E. and Rose, M. D. (1998). The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast. Mol. Biol. Cell 9, 2051-2068.
30. Miller, R. K., Matheos, D. and Rose, M. D. (1999). The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J. Cell Biol. 144, 963-975.
31. Minke, P. F., Lee, I. H. and Plamann, M. (1999). Microscopic analysis of Neurospora ropy mutants defective in nuclear distribution. Fungal Genet. Biol. 28, 55-67.
32. Morris, N. R. (1976). Mitotic mutants of Aspergillus nidulans. Genet. Res. 26, 237-254.
33. Morris, N. R. (2003). Nuclear positioning: the means is at the ends. Curr. Opin. Cell Biol. 15, 54-59.
34. Morris, N. R., Xiang, X. and Beckwith, S. M. (1995). Nuclear migration advances in fungi. Trends Cell Biol. 5, 278-282.
35. Morris, N. R., Efimov, V. P. and Xiang, X. (1998a). Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol. 8, 467-470.
36. Morris, S. M., Albrecht, U., Reiner, O., Eichele, G. and Yu-Lee, L.-y. (1998b). The lissencephaly gene product Lis1, a protein involved in neuronal migration, interacts with a nuclear movement protein, NudC. Curr. Biol. 8, 603-609.
37. Osmani, A. H., Osmani, S. A. and Morris, N. R. (1990). The molecular cloning and identification of a gene product specifically required for nuclear movement in Aspergillus nidulans. J. Cell Biol. 111, 543-551.
38. Osmani, A. H., Davies, J., Oakley, C. E., Oakley, B. R. and Osmani, S. A. (2003). TINA interacts with the NIMA kinase in Aspergillus nidulans and negatively regulates astral microtubules during metaphase arrest. Mol. Biol. Cell 14, 3169-3179.
39. Plamann, M., Minke, P. F., Tinsley, J. H. and Bruno, K. S. (1994). Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127, 139-149.
40. Requena, N., Alberti-Segui, C., Winzenburg, E., Horn, C., Schliwa, M., Philippsen, P., Liese, R. and Fischer, R. (2001). Genetic evidence for a microtubule-destabilizing effect of conventional kinesin and analysis of its consequences for the control of nuclear distribution in Aspergillus nidulans. Mol. Microbiol. 42, 121-132.
41. Rischitor, P., Konzack, S. and Fischer, R. (2004). The Kip3-like kinesin KipB moves along microtubules and determines spindle position during synchronized mitoses in Aspergillus nidulans hyphae. Eukaryot. Cell 3, 632-645.
42. Sambrook, J. and Russel, D. W. (1999). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
43. Sawin, K. E., Lourenco, P. C. C. and Snaith, H. A. (2004). Microtubule nucleation at non-spindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr. Biol. 14, 763-775.
44. Segal, M., Bloom, K. and Reed, S. I. (2002). Kar9p-independent microtubule capture at Bud6p cortical sites primes spindle polarity before bud emergence in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 4141-4155.
45. Shaw, S. L., Yeh, E., Maddox, P., Salmon, E. D. and Bloom, K. (1997). Astral microtubule dynamics in yeast: A microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud. J. Cell Biol. 139, 985-994.
46. Shaw, S. L., Maddox, P., Skibbens, R. V., Yeh, E., Salmon, E. D. and Bloom, K. (1998). Nuclear and spindle dynamics in budding yeast. Mol. Biol. Cell 9, 1627-1631.
47. Sheeman, B., Carvalho, P., Sagot, I., Geiser, J., Kho, D., Hoyt, M. A. and Pellman, D. (2003). Determinants of S. cerevisiae dynein localization and activation: Implications for the mechanism of spindle positioning. Curr. Biol. 13, 364-372.
48. Stringer, M. A., Dean, R. A., Sewall, T. C. and Timberlake, W. E. (1991). Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Genes Dev. 5, 1161-1171.
49. Su, W., Li, S., Oakley, B. R. and Xiang, X. (2004). Dual-color imaging of nucelar division and mitotic spindle elongation in live cells of Aspergillus nidulans. Eukaryot. Cell 3, 553-556.
50. Suelmann, R., Sievers, N. and Fischer, R. (1997). Nuclear traffic in fungal hyphae: In vivo study of nuclear migration and positioning in Aspergillus nidulans. Mol. Microbiol. 25, 757-769.
51. Suelmann, R., Sievers, N., Galetzka, D., Robertson, L., Timberlake, W. E. and Fischer, R. (1998). Increased nuclear traffic chaos in hyphae of apsB mutants of Aspergillus nidulans: Molecular characterization of apsB and in vivo observation of nuclear behaviour. Mol. Microbiol. 30, 831-842.
52. Toews, M. W., Warmbold, J., Konzack, S., Rischitor, P. E., Veith, D., Vienken, K., Vinuesa, C., Wei, H. and Fischer, R. (2004). Establishment of mRFP1 as fluorescent marker in Aspergillus nidulans and construction of expression vectors for high-throughput protein tagging using recombination in Escherichia coli (GATEWAY). Curr. Genet. 45, 383-389.
53. Tran, P. T., Marsh, L., Doye, V., Inoue, S. and Chang, F. (2001). A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J. Cell Biol. 153, 397-411.
54. Venkatram, S., Tasto, J. J., Feoktistova, A., Jennings, J. L., Link, A. J. and Gould, K. L. (2004). Identification and characterization of two novel proteins affecting fission yeast γ-tubulin complex function. Mol. Biol. Cell 15, 2287-2301.
55. Venkatram, S., Jennings, J. L., Link, A. and Gould, K. L. (2005). Mto2p, a novel fission yeast protein required for cytoplasmic microtubule organization and anchoring of the cytokinetic actin ring. Mol. Biol. Cell 16, 3052-3063.
56. Waring, R. B., May, G. S. and Morris, N. R. (1989). Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin coding genes. Gene 79, 119-130.
57. Willins, D. A., Xiang, X. and Morris, N. R. (1995). An alpha tubulin mutation suppresses nuclear migration mutations in Aspergillus nidulans. Genetics 141, 1287-1298.
58. Xiang, S., Han, G., Winkelmann, D. A., Zuo, W. and Morris, N. R. (2000). Dynamics of cytoplasmic dynein in living cells and the effect of a mutation in the dynactin complex actin-related protein Arp1. Curr. Biol. 10, 603-606.
59. Xiang, X. and Morris, R. (1999). Hyphal tip growth and nuclear migration. Curr. Opin. Microbiol. 2, 636-640.
60. Xiang, X. and Fischer, R. (2004). Nuclear migration and positioning in filamentous fungi. Fungal Genet. Biol. 41, 411-419.
61. Xiang, X., Beckwith, S. M. and Morris, N. R. (1994). Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 91, 2100-2104.
62. Xiang, X., Osmani, A. H., Osmani, S. A., Xin, M. and Morris, N. R. (1995a). NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6, 297-310.
63. Xiang, X., Roghi, C. and Morris, N. R. (1995b). Characterization and localization of the cytoplasmic dynein heavy chain in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 92, 9890-9894.
64. Yang, L., Ukil, L., Osmani, A., Nahm, F., Davies, J., De Souza, C. P. C., Dou, X., Perez-Balguer, A. and Osmani, S. A. (2004). Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans. Eukaryot. Cell 3, 1359-1362.
65. Yeh, E., Yang, C., Chin, E., Maddox, P., Salmon, E. D., Lew, D. J. and Bloom, K. (2000). Dynamic positioning of mitotic spindles in yeast: Role of microtubule motors and cortical determinants. Mol. Biol. Cell 11, 3949-3961.
66. Yelton, M. M., Hamer, J. E. and Timberlake, W. E. (1984). Transformation of Aspergillus nidulans by using a trpC plasmid. Proc. Natl. Acad. Sci. USA 81, 1470-1474.
67. Zhang, J., Han, G. and Xiang, X. (2002). Cytoplasmic dynein intermediate chain and heavy chain are dependent upon each other for microtubule end localization in Aspergillus nidulans. Mol. Microbiol. 44, 381-392.
68. Zhang, J., Li, S., Fischer, R. and Xiang, X. (2003). The accumulation of cytoplasmic dynein and dynactin at microtubule plus-ends is kinesin dependent in Aspergillus nidulans. Mol. Biol. Cell 14, 1479-1488.