Insights into dynamic mitotic chromatin organization through the NIMA kinase suppressor SonC, a chromatin-associated protein involved in the DNA damage response

Genetics

Volumn 196, Issue 1, 2014, Pages 177-195

  Larson, Jennifer R ^a   Facemyer, Eric M ^a   Shen, Kuo Fang ^a   Ukil, Leena ^a   Osmani, Stephen A ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H1; NIMA1 PROTEIN; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; ZINC;

ALLELE; ARTICLE; CELL NUCLEUS MEMBRANE; CHROMATIN; CHROMOSOME; CHROMOSOME NOR; CONTROLLED STUDY; DNA DAMAGE; DNA ISOLATION; EMERICELLA NIDULANS; ESSENTIAL GENE; GENE LOCATION; GENE MUTATION; GENETIC SCREENING; MITOSIS; MUTANT; NONHUMAN; NUCLEAR PORE COMPLEX; NUCLEOLUS; PRIORITY JOURNAL; SONA GENE; SONB GENE; SONC GENE; TEMPERATURE SENSITIVITY;

DNA DAMAGE; MAG1; NIMA; NUCLEOLAR ORGANIZER REGION (NOR); ZN2CYS6 DOMAIN;

ALLELES; AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMATIN; CHROMOSOMES; DNA DAMAGE; DNA REPAIR; FUNGAL PROTEINS; HISTONES; MITOSIS; MOLECULAR SEQUENCE DATA; NUCLEAR ENVELOPE; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEOLUS ORGANIZER REGION; NUCLEOPROTEINS; PROTEIN-SERINE-THREONINE KINASES;

EID: 84901319698     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.113.156745     Document Type: Article

References (157)

1. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts et al., 2002 Molecular Biology of the Cell, Ed. 4. Garland Science, New York.
2. Alseth, I., F. Osman, H. Korvald, I. Tsaneva, M. C. Whitby et al., 2005 Biochemical characterization and DNA repair pathway interactions of Mag1-mediated base excision repair in Schizosaccharomyces pombe. Nucleic Acids Res. 33: 1123-1131.
3. Arnaud, M. B., G. C. Cerqueira, D. O. Inglis, M. S. Skrzypek, J. Binkley et al., 2012 The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources. Nucleic Acids Res. 40: D653-D659.
4. Babu, J. R., K. B. Jeganathan, D. J. Baker, X. Wu, N. Kang-Decker et al., 2003 Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160: 341-353.
5. Bailer, S. M., S. Siniossoglou, A. Podtelejnikov, A. Hellwig, M. Mann et al., 1998 Nup116p and nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor gle2p. EMBO J. 17: 1107-1119.
6. Ben-Hur, E., M. M. Elkind, and B. V. Bronk, 1974 Thermally enhanced radioresponse of cultured Chinese hamster cells: inhibition of repair of sublethal damage and enhancement of lethal damage. Radiat. Res. 58: 38-51.
7. Bhalla, N., S. Biggins, and A. W. Murray, 2002 Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior. Mol. Biol. Cell 13: 632-645.
8. Blower, M. D., M. Nachury, R. Heald, and K. Weis, 2005 A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121: 223-234.
9. Boisvert, F. M., S. Van Koningsbruggen, J. Navascues, and A. I. Lamond, 2007 The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8: 574-585.
10. Borrow, J., A. M. Shearman, V. P. Stanton, Jr., R. Becher, T. Collins et al., 1996 The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat. Genet. 12: 159-167.
11. Brody, H., and J. Carbon, 1989 Electrophoretic karyotype of Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 86: 6260-6263.
12. Brody, H., J. Griffith, A. J. Cuticchia, J. Arnold, and W. E. Timberlake, 1991 Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res. 19: 3105-3109.
13. Brown, J. A., A. Bharathi, A. Ghosh, W. Whalen, E. Fitzgerald et al., 1995 A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J. Biol. Chem. 270: 7411-7419.
14. Chen, J., B. Derfler, A. Maskati, and L. Samson, 1989 Cloning a eukaryotic DNA glycosylase repair gene by the suppression of a DNA repair defect in Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 7961-7965.
15. Chen, J., B. Derfler, and L. Samson, 1990 Saccharomyces cerevisiae 3-methyladenine DNA glycosylase has homology to the AlkA glycosylase of E. coli and is induced in response to DNA alkylation damage. EMBO J. 9: 4569-4575.
16. Chen, Y., P. L. Chen, C. F. Chen, X. Jiang, and D. J. Riley, 2008 Never-in-mitosis related kinase 1 functions in DNA damage response and checkpoint control. Cell Cycle 7: 3194-3201.
17. Clutterbuck, A. J., and M. Farman, 2008 Aspergillus nidulans linkage map and genome sequence: closing gaps and adding telomeres in The Aspergilli Genomics: Medical Aspects, Biotechnology, and Research Methods, edited by G. H. Goldman and S. A. Osmani. Taylor and Francis Group, Boca Raton, FL.
18. Cole, C., J. D. Barber, and G. J. Barton, 2008 The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36: W197-W201.
19. Croteau, D. L., and V. A. Bohr, 1997 Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J. Biol. Chem. 272: 25409-25412.
20. David, H., I. S. Ozcelik, G. Hofmann, and J. Nielsen, 2008 Analysis of Aspergillus nidulans metabolism at the genome-scale. BMC Genomics 9: 163.
21. De Souza, C. P., and S. A. Osmani, 2007 Mitosis, not just open or closed. Eukaryot. Cell 6: 1521-1527.
22. De Souza, C. P., and S. A. Osmani, 2009 Double duty for nuclear proteins: the price of more open forms of mitosis. Trends Genet. 25: 545-554.
23. De Souza, C. P., A. H. Osmani, L. P. Wu, J. L. Spotts, and S. A. Osmani, 2000 Mitotic histone H3 phosphorylation by the NIMA kinase in Aspergillus nidulans. Cell 102: 293-302.
24. De Souza, C. P., K. P. Horn, K. Masker, and S. A. Osmani, 2003 The SONB(NUP98) nucleoporin interacts with the NIMA kinase in Aspergillus nidulans. Genetics 165: 1071-1081.
25. De Souza, C. P., A. H. Osmani, S. B. Hashmi, and S. A. Osmani, 2004 Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr. Biol. 14: 1973-1984.
26. De Souza, C. P., S. B. Hashmi, K. P. Horn, and S. A. Osmani, 2006 A point mutation in the Aspergillus nidulans sonBNup98 nuclear pore complex gene causes conditional DNA damage sensitivity. Genetics 174: 1881-1893.
27. De Souza, C. P., S. B. Hashmi, T. Nayak, B. Oakley, and S. A. Osmani, 2009 Mlp1 acts as a mitotic scaffold to spatially regulate spindle assembly checkpoint proteins in Aspergillus nidulans. Mol. Biol. Cell 20: 2146-2159.
28. De Souza, C. P., S. B. Hashmi, X. Yang, and S. A. Osmani, 2011 Regulated inactivation of the spindle assembly checkpoint without functional mitotic spindles. EMBO J. 30: 2648-2661.
29. Dewey, W. C., L. E. Hopwood, S. A. Sapareto, and L. E. Gerweck, 1977 Cellular responses to combinations of hyperthermia and radiation. Radiology 123: 463-474.
30. Dimario, P. J., 2004 Cell and molecular biology of nucleolar assembly and disassembly. Int. Rev. Cytol. 239: 99-178.
31. Freeman, L., L. Aragon-Alcaide, and A. Strunnikov, 2000 The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol. 149: 811-824.
32. Fry, A. M., L. O'Regan, S. R. Sabir, and R. Bayliss, 2012 Cell cycle regulation by the NEK family of protein kinases. J. Cell Sci. 125: 4423-4433.
33. Funasaka, T., H. Nakano, Y. Wu, C. Hashizume, L. Gu et al., 2011 RNA export factor RAE1 contributes to NUP98-HOXA9-mediated leukemogenesis. Cell Cycle 10: 1456-1467.
34. Galagan, J. E., S. E. Calvo, C. Cuomo, L. J. Ma, J. R. Wortman et al., 2005 Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
35. Gough, S. M., C. I. Slape, and P. D. Aplan, 2011 NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood 118: 6247-6257.
36. Govindaraghavan, M., A. A. Lad, and S. A. Osmani, 2013 The NIMA kinase is required to execute stage specific mitotic functions after initiation of mitosis. Available at: http://www.ncbi. nlm.nih.gov/pubmed/24186954.
37. Grill, B., L. Chen, E. D. Tulgren, S. T. Baker, W. Bienvenut et al., 2012 RAE-1, a novel PHR binding protein, is required for axon termination and synapse formation in Caenorhabditis elegans. J. Neurosci. 32: 2628-2636.
38. Gutiyama, L. M., J. P. Da Cunha, and S. Schenkman, 2008 Histone H1 of Trypanosoma cruzi is concentrated in the nucleolus region and disperses upon phosphorylation during progression to mitosis. Eukaryot. Cell 7: 560-568.
39. Habash, R. W., D. Krewski, R. Bansal, and H. T. Alhafid, 2011 Principles, applications, risks and benefits of therapeutic hyperthermia. Front. Biosci. (Elite Ed.) 3: 1169-1181.
40. Hernandez-Verdun, D., 2011 Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2: 189-194.
41. Jeganathan, K. B., L. Malureanu, and J. M. Van Deursen, 2005 The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438: 1036-1039.
42. Kalashnikova, A. A., D. D. Winkler, S. J. Mcbryant, R. K. Henderson, J. A. Herman et al., 2013 Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus. Nucleic Acids Res. 41: 4026-4035.
43. Krawczyk, P. M., B. Eppink, J. Essers, J. Stap, H. Rodermond et al., 2011 Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc. Natl. Acad. Sci. USA 108: 9851-9856.
44. Kroon, E., U. Thorsteinsdottir, N. Mayotte, T. Nakamura, and G. Sauvageau, 2001 NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 20: 350-361.
45. Kunkel, T. A., 1984 Mutational specificity of depurination. Proc. Natl. Acad. Sci. USA 81: 1494-1498.
46. Laurell, E., K. Beck, K. Krupina, G. Theerthagiri, B. Bodenmiller et al., 2011 Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144: 539-550.
47. Lavoie, B. D., E. Hogan, and D. Koshland, 2002 In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J. Cell Biol. 156: 805-815.
48. Blower, M. D., M. Nachury, R. Heald, and K. Weis, 2005 A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121: 223-234.
49. Boisvert, F. M., S. Van Koningsbruggen, J. Navascues, and A. I. Lamond, 2007 The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8: 574-585.
50. Borrow, J., A. M. Shearman, V. P. Stanton, Jr., R. Becher, T. Collins et al., 1996 The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat. Genet. 12: 159-167.
51. Brody, H., and J. Carbon, 1989 Electrophoretic karyotype of Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 86: 6260-6263.
52. Brody, H., J. Griffith, A. J. Cuticchia, J. Arnold, and W. E. Timberlake, 1991 Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res. 19: 3105-3109.
53. Brown, J. A., A. Bharathi, A. Ghosh, W. Whalen, E. Fitzgerald et al., 1995 A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J. Biol. Chem. 270: 7411-7419.
54. Chen, J., B. Derfler, A. Maskati, and L. Samson, 1989 Cloning a eukaryotic DNA glycosylase repair gene by the suppression of a DNA repair defect in Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 7961-7965.
55. Chen, J., B. Derfler, and L. Samson, 1990 Saccharomyces cerevisiae 3-methyladenine DNA glycosylase has homology to the AlkA glycosylase of E. coli and is induced in response to DNA alkylation damage. EMBO J. 9: 4569-4575.
56. Chen, Y., P. L. Chen, C. F. Chen, X. Jiang, and D. J. Riley, 2008 Never-in-mitosis related kinase 1 functions in DNA damage response and checkpoint control. Cell Cycle 7: 3194-3201.
57. Clutterbuck, A. J., and M. Farman, 2008 Aspergillus nidulans linkage map and genome sequence: closing gaps and adding telomeres in The Aspergilli Genomics: Medical Aspects, Biotechnology, and Research Methods, edited by G. H. Goldman and S. A. Osmani. Taylor and Francis Group, Boca Raton, FL.
58. Cole, C., J. D. Barber, and G. J. Barton, 2008 The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36: W197-W201.
59. Croteau, D. L., and V. A. Bohr, 1997 Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J. Biol. Chem. 272: 25409-25412.
60. David, H., I. S. Ozcelik, G. Hofmann, and J. Nielsen, 2008 Analysis of Aspergillus nidulans metabolism at the genome-scale. BMC Genomics 9: 163.
61. De Souza, C. P., and S. A. Osmani, 2007 Mitosis, not just open or closed. Eukaryot. Cell 6: 1521-1527.
62. De Souza, C. P., and S. A. Osmani, 2009 Double duty for nuclear proteins: the price of more open forms of mitosis. Trends Genet. 25: 545-554.
63. De Souza, C. P., A. H. Osmani, L. P. Wu, J. L. Spotts, and S. A. Osmani, 2000 Mitotic histone H3 phosphorylation by the NIMA kinase in Aspergillus nidulans. Cell 102: 293-302.
64. De Souza, C. P., K. P. Horn, K. Masker, and S. A. Osmani, 2003 The SONB(NUP98) nucleoporin interacts with the NIMA kinase in Aspergillus nidulans. Genetics 165: 1071-1081.
65. De Souza, C. P., A. H. Osmani, S. B. Hashmi, and S. A. Osmani, 2004 Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr. Biol. 14: 1973-1984.
66. De Souza, C. P., S. B. Hashmi, K. P. Horn, and S. A. Osmani, 2006 A point mutation in the Aspergillus nidulans sonBNup98 nuclear pore complex gene causes conditional DNA damage sensitivity. Genetics 174: 1881-1893.
67. De Souza, C. P., S. B. Hashmi, T. Nayak, B. Oakley, and S. A. Osmani, 2009 Mlp1 acts as a mitotic scaffold to spatially regulate spindle assembly checkpoint proteins in Aspergillus nidulans. Mol. Biol. Cell 20: 2146-2159.
68. De Souza, C. P., S. B. Hashmi, X. Yang, and S. A. Osmani, 2011 Regulated inactivation of the spindle assembly checkpoint without functional mitotic spindles. EMBO J. 30: 2648-2661.
69. Dewey, W. C., L. E. Hopwood, S. A. Sapareto, and L. E. Gerweck, 1977 Cellular responses to combinations of hyperthermia and radiation. Radiology 123: 463-474.
70. Dimario, P. J., 2004 Cell and molecular biology of nucleolar assembly and disassembly. Int. Rev. Cytol. 239: 99-178.
71. Freeman, L., L. Aragon-Alcaide, and A. Strunnikov, 2000 The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol. 149: 811-824.
72. Fry, A. M., L. O'Regan, S. R. Sabir, and R. Bayliss, 2012 Cell cycle regulation by the NEK family of protein kinases. J. Cell Sci. 125: 4423-4433.
73. Funasaka, T., H. Nakano, Y. Wu, C. Hashizume, L. Gu et al., 2011 RNA export factor RAE1 contributes to NUP98-HOXA9-mediated leukemogenesis. Cell Cycle 10: 1456-1467.
74. Galagan, J. E., S. E. Calvo, C. Cuomo, L. J. Ma, J. R. Wortman et al., 2005 Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
75. Gough, S. M., C. I. Slape, and P. D. Aplan, 2011 NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood 118: 6247-6257.
76. Govindaraghavan, M., A. A. Lad, and S. A. Osmani, 2013 The NIMA kinase is required to execute stage specific mitotic functions after initiation of mitosis. Available at: http://www.ncbi. nlm.nih.gov/pubmed/24186954.
77. Grill, B., L. Chen, E. D. Tulgren, S. T. Baker, W. Bienvenut et al., 2012 RAE-1, a novel PHR binding protein, is required for axon termination and synapse formation in Caenorhabditis elegans. J. Neurosci. 32: 2628-2636.
78. Gutiyama, L. M., J. P. Da Cunha, and S. Schenkman, 2008 Histone H1 of Trypanosoma cruzi is concentrated in the nucleolus region and disperses upon phosphorylation during progression to mitosis. Eukaryot. Cell 7: 560-568.
79. Habash, R. W., D. Krewski, R. Bansal, and H. T. Alhafid, 2011 Principles, applications, risks and benefits of therapeutic hyperthermia. Front. Biosci. (Elite Ed.) 3: 1169-1181.
80. Hernandez-Verdun, D., 2011 Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2: 189-194.
81. Jeganathan, K. B., L. Malureanu, and J. M. Van Deursen, 2005 The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438: 1036-1039.
82. Kalashnikova, A. A., D. D. Winkler, S. J. Mcbryant, R. K. Henderson, J. A. Herman et al., 2013 Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus. Nucleic Acids Res. 41: 4026-4035.
83. Krawczyk, P. M., B. Eppink, J. Essers, J. Stap, H. Rodermond et al., 2011 Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc. Natl. Acad. Sci. USA 108: 9851-9856.
84. Kroon, E., U. Thorsteinsdottir, N. Mayotte, T. Nakamura, and G. Sauvageau, 2001 NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 20: 350-361.
85. Kunkel, T. A., 1984 Mutational specificity of depurination. Proc. Natl. Acad. Sci. USA 81: 1494-1498.
86. Laurell, E., K. Beck, K. Krupina, G. Theerthagiri, B. Bodenmiller et al., 2011 Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144: 539-550.
87. Lavoie, B. D., E. Hogan, and D. Koshland, 2002 In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J. Cell Biol. 156: 805-815.
88. Lavoie, B. D., E. Hogan, and D. Koshland, 2004 In vivo requirements for rDNA chromosome condensation reveal two cell-cycleregulated pathways for mitotic chromosome folding. Genes Dev. 18: 76-87.
89. Lavoie, B. D., K. M. Tuffo, S. Oh, D. Koshland, and C. Holm, 2000 Mitotic chromosome condensation requires Brn1p, the yeast homologue of Barren. Mol. Biol. Cell 11: 1293-1304.
90. Lechner, J., 1994 A zinc finger protein, essential for chromosome segregation, constitutes a putative DNA binding subunit of the Saccharomyces cerevisiae kinetochore complex, Cbf3. EMBO J. 13: 5203-5211.
91. Leung, A. K., D. Gerlich, G. Miller, C. Lyon, Y. W. Lam et al., 2004 Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. J. Cell Biol. 166: 787-800.
92. Liu, H. L., C. P. De Souza, A. H. Osmani, and S. A. Osmani, 2009 The three fungal transmembrane nuclear pore complex proteins of Aspergillus nidulans are dispensable in the presence of an intact An-Nup84-120 complex. Mol. Biol. Cell 20: 616-630.
93. Liu, H. L., A. H. Osmani, L. Ukil, S. Son, S. Markossian et al., 2010 Single-step affinity purification for fungal proteomics. Eukaryot. Cell 9: 831-833.
94. Liu, S., C. K. Ho, J. Ouyang, and L. Zou, 2013 Nek1 kinase associates with ATR-ATRIP and primes ATR for efficient DNA damage signaling. Proc. Natl. Acad. Sci. USA 110: 2175-2180.
95. Lu, K. P., and T. Hunter, 1995 Evidence for a NIMA-like mitotic pathway in vertebrate cells. Cell 81: 413-424.
96. Lu, K. P., and A. R. Means, 1994 Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. EMBO J. 13: 2103-2113.
97. Malumbres, M., 2011 Physiological relevance of cell cycle kinases. Physiol. Rev. 91: 973-1007.
98. Maniatis, T., J. Sambrook, and E. F. Fritsch, 1989 Molecular Cloning: A Laboratory Manual. Cold Srping Harbor Laboratory Press, Cold Spring Harbor, NY.
99. Melixetian, M., D. K. Klein, C. S. Sorensen, and K. Helin, 2009 NEK11 regulates CDC25A degradation and the IR-induced G2/M checkpoint. Nat. Cell Biol. 11: 1247-1253.
100. Mi, J., C. Guo, D. L. Brautigan, and J. M. Larner, 2007 Protein phosphatase-1alpha regulates centrosome splitting through Nek2. Cancer Res. 67: 1082-1089.
101. Miles, T. D., J. Jakovljevic, E. W. Horsey, P. Harnpicharnchai, L. Tang et al., 2005 Ytm1, Nop7, and Erb1 form a complex necessary for maturation of yeast 66S preribosomes. Mol. Cell. Biol. 25: 10419-10432.
102. Moniz, L. S., and V. Stambolic, 2011 Nek10 mediates G2/M cell cycle arrest and MEK autoactivation in response to UV irradiation. Mol. Cell. Biol. 31: 30-42.
103. Moniz, L., P. Dutt, N. Haider, and V. Stambolic, 2011 Nek family of kinases in cell cycle, checkpoint control and cancer. Cell Div. 6: 18.
104. Moore, M. A., K. Y. Chung, M. Plasilova, J. J. Schuringa, J. H. Shieh et al., 2007 NUP98 dysregulation in myeloid leukemogenesis. Ann. N. Y. Acad. Sci. 1106: 114-142.
105. Morris, N. R., 1975 Mitotic mutants of Aspergillus nidulans. Genet. Res. 26: 237-254.
106. Morris, N. R., S. W. James, and M. J. O'Connell, 1992 Mitotic regulation in Aspergillus nidulans. Ciba Found. Symp. 170: 115-123; discussion 123-129.
107. Moura, D. J., B. Castilhos, B. F. Immich, A. D. Canedo, J. A. Henriques et al., 2010 Kin3 protein, a NIMA-related kinase of Saccharomyces cerevisiae, is involved in DNA adduct damage response. Cell Cycle 9: 2220-2229.
108. Moy, T. I., D. Boettner, J. C. Rhodes, P. A. Silver, and D. S. Askew, 2002 Identification of a role for Saccharomyces cerevisiae Cgr1p in pre-rRNA processing and 60S ribosome subunit synthesis. Microbiology 148: 1081-1090.
109. Nassirpour, R., L. Shao, P. Flanagan, T. Abrams, B. Jallal et al., 2010 Nek6 mediates human cancer cell transformation and is a potential cancer therapeutic target. Mol. Cancer Res. 8: 717-728.
110. Nayak, T., E. Szewczyk, C. E. Oakley, A. Osmani, L. Ukil et al., 2006 A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172: 1557-1566.
111. Nayak, T., H. Edgerton-Morgan, T. Horio, Y. Xiong, C. P. De Souza et al., 2010 Gamma-tubulin regulates the anaphase-promoting complex/cyclosome during interphase. J. Cell Biol. 190: 317-330.
112. Noguchi, K., H. Fukazawa, Y. Murakami, and Y. Uehara, 2002 Nek11, a new member of the NIMA family of kinases, involved in DNA replication and genotoxic stress responses. J. Biol. Chem. 277: 39655-39665.
113. Noguchi, K., H. Fukazawa, Y. Murakami, and Y. Uehara, 2004 Nucleolar Nek11 is a novel target of Nek2A in G1/Sarrested cells. J. Biol. Chem. 279: 32716-32727.
114. Oakley, B. R., and N. R. Morris, 1980 Nuclear movement is beta-tubulin-dependent in Aspergillus nidulans. Cell 19: 255-262.
115. Oakley, B. R., and N. R. Morris, 1983 A mutation in Aspergillus nidulans that blocks the transition from interphase to prophase. J. Cell Biol. 96: 1155-1158.
116. O'Connell, M. J., C. Norbury, and P. Nurse, 1994 Premature chromatin condensation upon accumulation of NIMA. EMBO J. 13: 4926-4937.
117. O'Connell, M. J., M. J. Krien, and T. Hunter, 2003 Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13: 221-228.
118. Ong, T. M., and F. J. Serres, 1975 Mutation induction by difunctional alkylating agents in Neurospora crassa. Genetics 80: 475-482.
119. Osherov, N., and G. May, 2000 Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. Genetics 155: 647-656.
120. Osmani, A. H., S. L. McGuire, K. L. O'Donnell, R. T. Pu, and S. A. Osmani, 1991 Role of the cell-cycle-regulated NIMA protein kinase during G2 and mitosis: evidence for two pathways of mitotic regulation. Cold Spring Harb. Symp. Quant. Biol. 56: 549-555.
121. Osmani, A. H., J. Davies, H. L. Liu, A. Nile, and S. A. Osmani, 2006a Systematic deletion and mitotic localization of the nuclear pore complex proteins of Aspergillus nidulans. Mol. Biol. Cell 17: 4946-4961.
122. Osmani, A. H., B. R. Oakley, and S. A. Osmani, 2006b Identification and analysis of essential Aspergillus nidulans genes using the heterokaryon rescue technique. Nat. Protoc. 1: 2517-2526.
123. Osmani, S. A., G. S. May, and N. R. Morris, 1987 Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J. Cell Biol. 104: 1495-1504.
124. Osmani, S. A., R. T. Pu, and N. R. Morris, 1988 Mitotic induction and maintenance by overexpression of a G2-specific gene that encodes a potential protein kinase. Cell 53: 237-244.
125. Park, H. S., and J. H. Yu, 2012 Multi-copy genetic screen in Aspergillus nidulans. Methods Mol. Biol. 944: 183-190.
126. Pel, H. J., J. H. De Winde, D. B. Archer, P. S. Dyer, G. Hofmann et al., 2007 Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 25: 221-231.
127. Pelegrini, A. L., D. J. Moura, B. L. Brenner, P. F. Ledur, G. P. Maques et al., 2010 Nek1 silencing slows down DNA repair and blocks DNA damage-induced cell cycle arrest. Mutagenesis 25: 447-454.
128. Pestov, D. G., M. G. Stockelman, Z. Strezoska, and L. F. Lau, 2001 ERB1, the yeast homolog of mammalian Bop1, is an essential gene required for maturation of the 25S and 5.8S ribosomal RNAs. Nucleic Acids Res. 29: 3621-3630.
129. Petes, T. D., 1979 Yeast ribosomal DNA genes are located on chromosome XII. Proc. Natl. Acad. Sci. USA 76: 410-414.
130. Polci, R., A. Peng, P. L. Chen, D. J. Riley, and Y. Chen, 2004 NIMArelated protein kinase 1 is involved early in the ionizing radiationinduced DNA damage response. Cancer Res. 64: 8800-8803.
131. Pontecorvo, G., J. A. Roper, L. M. Hemmons, K. D. Macdonald, and A. W. Bufton, 1953 The genetics of Aspergillus nidulans. Adv. Genet. 5: 141-238.
132. Prakash, L., and S. Prakash, 1977 Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 86: 33-55.
133. Pritchard, C. E., M. Fornerod, L. H. Kasper, and J. M. Van Deursen, 1999 RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J. Cell Biol. 145: 237-254.
134. Pu, R. T., and S. A. Osmani, 1995 Mitotic destruction of the cell cycle regulated NIMA protein kinase of Aspergillus nidulans is required for mitotic exit. EMBO J. 14: 995-1003.
135. Pu, R. T., G. Xu, L. Wu, J. Vierula, K. O'Donnell et al., 1995 Isolation of a functional homolog of the cell cycle-specific NIMA protein kinase of Aspergillus nidulans and functional analysis of conserved residues. J. Biol. Chem. 270: 18110-18116.
136. Quarmby, L. M., and M. R. Mahjoub, 2005 Caught Nek-ing: cilia and centrioles. J. Cell Sci. 118: 5161-5169.
137. Rajani, K. R., E. L. Pettit Kneller, M. O. McKenzie, D. A. Horita, J. W. Chou et al., 2012 Complexes of vesicular stomatitis virus matrix protein with host Rae1 and Nup98 involved in inhibition of host transcription. PLoS Pathog. 8: e1002929.
138. Ren, Y., H. S. Seo, G. Blobel, and A. Hoelz, 2010 Structural and functional analysis of the interaction between the nucleoporin Nup98 and the mRNA export factor Rae1. Proc. Natl. Acad. Sci. USA 107: 10406-10411.
139. Shen, K. F., and S. A. Osmani, 2013 Regulation of mitosis by the NIMA kinase involves TINA and its newly discovered partner An-WDR8 at spindle pole bodies. Available at: http://www. ncbi.nlm.nih.gov/pubmed/24152731.
140. Sorensen, C. S., M. Melixetian, D. K. Klein, and K. Helin, 2010 NEK11: linking CHK1 and CDC25A in DNA damage checkpoint signaling. Cell Cycle 9: 450-455.
141. Strezoska, Z., D. G. Pestov, and L. F. Lau, 2000 Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5.8S RRNA processing and 60S ribosome biogenesis. Mol. Cell. Biol. 20: 5516-5528.
142. Sun, J., D. Boettner, N. Huebner, F. Xu, J. C. Rhodes et al., 2001 Molecular cloning of cgrA, the gene encoding the Aspergillus nidulans ortholog of Saccharomyces cerevisiae CGR1. Curr. Microbiol. 42: 403-407.
143. Szewczyk, E., T. Nayak, C. E. Oakley, H. Edgerton, Y. Xiong et al., 2006 Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 1: 3111-3120.
144. Tollervey, D., H. Lehtonen, M. Carmo-Fonseca, and E. C. Hurt, 1991 The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10: 573-583.
145. Torres-Rosell, J., F. Machin, A. Jarmuz, and L. Aragon, 2004 Nucleolar segregation lags behind the rest of the genome and requires Cdc14p activation by the FEAR network. Cell Cycle 3: 496-502.
146. Tsunoda, N., T. Kokuryo, K. Oda, T. Senga, Y. Yokoyama et al., 2009 Nek2 as a novel molecular target for the treatment of breast carcinoma. Cancer Sci. 100: 111-116.
147. Ukil, L., A. Varadaraj, M. Govindaraghavan, H. L. Liu, and S. A. Osmani, 2008 Copy number suppressors of the Aspergillus nidulans nimA1 mitotic kinase display distinctive and highly dynamic cell cycle-regulated locations. Eukaryot. Cell 7: 2087-2099.
148. Ukil, L., C. P. De Souza, H. L. Liu, and S. A. Osmani, 2009 Nucleolar separation from chromosomes during Aspergillus nidulans mitosis can occur without spindle forces. Mol. Biol. Cell 20: 2132-2145.
149. Velichko, A. K., N. V. Petrova, O. L. Kantidze, and S. V. Razin, 2012 Dual effect of heat shock on DNA replication and genome integrity. Mol. Biol. Cell 23: 3450-3460.
150. Wong, R. W., G. Blobel, and E. Coutavas, 2006 Rae1 interaction with NuMA is required for bipolar spindle formation. Proc. Natl. Acad. Sci. USA 103: 19783-19787.
151. Wortman, J. R., J. M. Gilsenan, V. Joardar, J. Deegan, J. Clutterbuck et al., 2009 The 2008 update of the Aspergillus nidulans genome annotation: a community effort. Fungal Genet. Biol. 46 (Suppl. 1): S2-S13.
152. Wu, L., S. A. Osmani, and P. M. Mirabito, 1998 A role for NIMA in the nuclear localization of cyclin B in Aspergillus nidulans. J. Cell Biol. 141: 1575-1587.
153. Yang, L., L. Ukil, A. Osmani, F. Nahm, J. Davies et al., 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.
154. Ye, X. S., G. Xu, R. T. Pu, R. R. Fincher, S. L. McGuire et al., 1995 The NIMA protein kinase is hyperphosphorylated and activated downstream of p34cdc2/cyclin B: coordination of two mitosis promoting kinases. EMBO J. 14: 986-994.
155. Ye, X. S., R. R. Fincher, A. Tang, K. O'Donnell, and S. A. Osmani, 1996 Two S-phase checkpoint systems, one involving the function of both BIME and Tyr15 phosphorylation of p34cdc2, inhibit NIMA and prevent premature mitosis. EMBO J. 15: 3599-3610.
156. Ye, X. S., R. R. Fincher, A. Tang, A. H. Osmani, and S. A. Osmani, 1998 Regulation of the anaphase-promoting complex/cyclosome by bimAAPC3 and proteolysis of NIMA. Mol. Biol. Cell 9: 3019-3030.
157. Zhang, B., H. W. Chen, R. L. Mu, W. K. Zhang, M. Y. Zhao et al., 2011 NIMA-related kinase NEK6 affects plant growth and stress response in Arabidopsis. Plant J. 68: 830-843.