Regulation of mitosis by the NIMA kinase involves TINA and its newly discovered partner, An-WDR8, at spindle pole bodies

Molecular Biology of the Cell

Volumn 24, Issue 24, 2013, Pages 3842-3856

  Shen, Kuo Fang ^a   Osmani, Stephen A ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AN WDR8 PROTEIN; AURORA A KINASE; BIMC KINESIN; CYCLIN B; GREEN FLUORESCENT PROTEIN; KINESIN; MEMBRANE PROTEIN; NIMA KINASE; PHOSPHOTRANSFERASE; TINA PROTEIN; UNCLASSIFIED DRUG; AGENTS AFFECTING CELL DIVISION; BIMC PROTEIN, ASPERGILLUS NIDULANS; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE 1; FUNGAL PROTEIN; NIMA PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE;

ARTICLE; BINDING AFFINITY; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NUCLEAR PORE COMPLEX; PLANT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; REGULATORY MECHANISM; SPINDLE POLE BODY; AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; CONFOCAL MICROSCOPY; GENETICS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; AURORA KINASE A; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CYCLIN B; FUNGAL PROTEINS; G2 PHASE; GREEN FLUORESCENT PROTEINS; KINESIN; MICROSCOPY, CONFOCAL; MITOSIS; MITOSIS MODULATORS; MOLECULAR SEQUENCE DATA; PROTEIN-SERINE-THREONINE KINASES; SPINDLE POLE BODIES;

EID: 84890483704     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-07-0422     Document Type: Article

References (71)

1. Arnaud MB 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.
2. Bahe S, Stierhof YD, Wilkinson CJ, Leiss F, Nigg EA (2005). Rootletin forms centriole-Associated filaments and functions in centrosome cohesion. J Cell Biol 171, 27-33.
3. Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH Jr., O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI (2008). beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 22, 91-105.
4. Belham C, Roig J, Caldwell JA, Aoyama Y, Kemp BE, Comb M, Avruch J (2003). A mitotic cascade of NIMA family kinases. Nercc1/Nek9 activates the Nek6 and Nek7 kinases. J Biol Chem 278, 34897-34909.
5. Bertran MT, Sdelci S, Regue L, Avruch J, Caelles C, Roig J (2011). Nek9 is a Plk1-Activated kinase that controls early centrosome separation through Nek6/7 and Eg5. EMBO J 30, 2634-2647.
6. Chen Y, Chen CF, Riley DJ, Chen PL (2011). Nek1 kinase functions in DNA damage response and checkpoint control through a pathway independent of ATM and ATR. Cell Cycle 10, 655-663.
7. Davies JR, Osmani AH, De Souza CP, Bachewich C, Osmani SA (2004). Potential link between the NIMA mitotic kinase and nuclear membrane fission during mitotic exit in Aspergillus nidulans. Eukaryot Cell 3, 1433-1444.
8. Dereeper A et al. 2008 Phylogeny.fr: robust phylogenetic analysis for the non-specialist Nucleic Acids Res 36 W465-W469
9. De Souza CP, Hashmi SB, Nayak T, Oakley B, Osmani SA (2009). Mlp1 acts as a mitotic scaffold to spatially regulate spindle assembly checkpoint proteins in Aspergillus nidulans. Mol Biol Cell 20, 2146-2159.
10. De Souza CP, Hashmi SB, Osmani AH, Andrews P, Ringelberg CS, Dunlap JC, Osmani SA (2013). Functional analysis of the Aspergillus nidulans kinome. PLoS One 8, e58008.
11. De Souza CP, Hashmi SB, Yang X, Osmani SA (2011). Regulated inactivation of the spindle assembly checkpoint without functional mitotic spindles. EMBO J 30, 2648-2661.
12. De Souza CP, Horn KP, Masker K, Osmani SA (2003). The SONB(NUP98) nucleoporin interacts with the NIMA kinase in Aspergillus nidulans. Genetics 165, 1071-1081.
13. De Souza CP, Osmani AH, Hashmi SB, Osmani SA (2004). Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr Biol 14, 1973-1984.
14. De Souza CP, Osmani AH, Wu LP, Spotts JL, Osmani SA (2000). Mitotic histone H3 phosphorylation by the NIMA kinase in Aspergillus nidulans. Cell 102, 293-302.
15. Edgar RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
16. Enos AP, Morris NR (1990). Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60, 1019-1027.
17. Fry AM, Mayor T, Meraldi P, Stierhof YD, Tanaka K, Nigg EA (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J Cell Biol 141, 1563-1574.
18. Fry AM, O'Regan L, Sabir SR, Bayliss R (2012). Cell cycle regulation by the NEK family of protein kinases. J Cell Sci 125, 4423-4433.
19. Fry AM, Schultz SJ, Bartek J, Nigg EA (1995). Substrate specificity and cell cycle regulation of the Nek2 protein kinase, a potential human homolog of the mitotic regulator NIMA of Aspergillus nidulans. J Biol Chem 270, 12899-12905.
20. Grallert A, Hagan IM (2002). Schizosaccharomyces pombe NIMA-related kinase, Fin1, regulates spindle formation and an affinity of Polo for the SPB. EMBO J 21, 3096-3107.
21. Hagan I, Yanagida M (1995). The product of the spindle formation gene sad1 +associates with the fission yeast spindle pole body and is essential for viability. J Cell Biol 129, 1033-1047.
22. Higa LA, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8, 1277-1283.
23. Jakobsen L et al. (2011). Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J 30, 1520-1535.
24. Jeong Y, Lee J, Kim K, Yoo JC, Rhee K (2007). Characterization of NIP2/centrobin, a novel substrate of Nek2, and its potential role in microtubule stabilization. J Cell Sci 120, 2106-2116.
25. Kim S, Lee K, Rhee K (2007). NEK7 is a centrosomal kinase critical for microtubule nucleation. Biochem Biophys Res Commun 360, 56-62.
26. Koshizuka Y, Ikegawa S, Sano M, Nakamura K, Nakamura Y (2001). Isolation, characterization, and mapping of the mouse and human WDR8 genes, members of a novel WD-repeat gene family. Genomics 72, 252-259.
27. Krien MJ, West RR, John UP, Koniaras K, McIntosh JR, O'Connell MJ (2002). The fission yeast NIMA kinase Fin1p is required for spindle function and nuclear envelope integrity. EMBO J 21, 1713-1722.
28. Laurell E, Beck K, Krupina K, Theerthagiri G, Bodenmiller B, Horvath P, Aebersold R, Antonin W, Kutay U (2011). Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144, 539-550.
29. Liu HL, De Souza CP, Osmani AH, Osmani SA (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.
30. Liu HL et al. (2010). Single-step affinity purification for fungal proteomics. Eukaryot Cell 9, 831-833.
31. Liu S, Ho CK, Ouyang J, Zou L (2013). Nek1 kinase associates with ATR-ATRIP and primes ATR for efficient DNA damage signaling. Proc Natl Acad Sci USA 110, 2175-2180.
32. Lu KP, Hunter T (1995). Evidence for a NIMA-like mitotic pathway in vertebrate cells. Cell 81, 413-424.
33. Lu KP, Means AR (1994). Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. EMBO J 13, 2103-2113.
34. Melixetian M, Klein DK, Sorensen CS, Helin K (2009). NEK11 regulates CDC25A degradation and the IR-induced G2/M checkpoint. Nat Cell Biol 11, 1247-1253.
35. Moniz L, Dutt P, Haider N, Stambolic V (2011). Nek family of kinases in cell cycle, checkpoint control and cancer. Cell Div 6, 18.
36. Moniz LS, Stambolic V (2011). Nek10 mediates G2/M cell cycle arrest and MEK autoactivation in response to UV irradiation. Mol Cell Biol 31, 30-42.
37. Nayak T, Szewczyk E, Oakley CE, Osmani A, Ukil L, Murray SL, Hynes MJ, Osmani SA, Oakley BR (2006). A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172, 1557-1566.
38. Oakley BR, Morris NR (1981). A beta-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly. Cell 24, 837-845.
39. Oakley BR, Morris NR (1983). A mutation in Aspergillus nidulans that blocks the transition from interphase to prophase. J Cell Biol 96, 1155-1158.
40. O'Connell MJ, Krien MJ, Hunter T (2003). Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol 13, 221-228.
41. O'Connell MJ, Norbury C, Nurse P (1994). Premature chromatin condensation upon accumulation of NIMA. EMBO J 13, 4926-4937.
42. O'Connell MJ, Osmani AH, Morris NR, Osmani SA (1992). An extra copy of nimEcyclinB elevates pre-MPF levels and partially suppresses mutation of nimTcdc25 in Aspergillus nidulans. EMBO J 11, 2139-2149.
43. O'Regan L, Blot J, Fry AM (2007). Mitotic regulation by NIMA-related kinases. Cell Div 2, 25.
44. O'Regan L, Fry AM (2009). The Nek6 and Nek7 protein kinases are required for robust mitotic spindle formation and cytokinesis. Mol Cell Biol 29, 3975-3990.
45. Osmani AH, Davies J, Liu HL, Nile A, Osmani SA (2006). Systematic deletion and mitotic localization of the nuclear pore complex proteins of Aspergillus nidulans. Mol Biol Cell 17, 4946-4961.
46. Osmani AH, Davies J, Oakley CE, Oakley BR, Osmani SA (2003). TINA interacts with the NIMA kinase in Aspergillus nidulans and negatively regulates astral microtubules during metaphase arrest. Mol Biol Cell 14, 3169-3179.
47. Osmani AH, McGuire SL, Osmani SA (1991). Parallel activation of the NIMA and p34cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A. nidulans. Cell 67, 283-291.
48. Osmani SA, May GS, Morris NR (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.
49. Osmani SA, Pu RT, Morris NR (1988). Mitotic induction and maintenance by overexpression of a G2-specific gene that encodes a potential protein kinase. Cell 53, 237-244.
50. Osmani SA, Ye XS (1996). Cell cycle regulation in Aspergillus by two protein kinases. Biochem J 317(Pt 3), 633-641.
51. Pemberton LF, Rout MP, Blobel G (1995). Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc Natl Acad Sci USA 92, 1187-1191.
52. Petroski MD, Deshaies RJ (2005). Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6, 9-20.
53. Pontecorvo G, Roper JA, Hemmons LM, Macdonald KD, Bufton AW (1953). The genetics of Aspergillus nidulans. Adv Genet 5, 141-238.
54. Pu RT, Osmani SA (1995). Mitotic destruction of the cell cycle regulated NIMA protein kinase of Aspergillus nidulans is required for mitotic exit. EMBO J 14, 995-1003.
55. Rapley J, Nicolas M, Groen A, Regue L, Bertran MT, Caelles C, Avruch J, Roig J (2008). The NIMA-family kinase Nek6 phosphorylates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J Cell Sci 121, 3912-3921.
56. Sdelci S, Bertran MT, Roig J (2011). Nek9, Nek6, Nek7 and the separation of centrosomes. Cell Cycle 10, 3816-3817.
57. Sorensen CS, Melixetian M, Klein DK, Helin K (2010). NEK11: linking CHK1 and CDC25A in DNA damage checkpoint signaling. Cell Cycle 9, 450-455.
58. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR (2006). Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1, 3111-3120.
59. Todd RB, Davis MA, Hynes MJ (2007a). Genetic manipulation of Aspergillus nidulans: heterokaryons and diploids for dominance, complementation and haploidization analyses. Nat Protoc 2, 822-830.
60. Todd RB, Davis MA, Hynes MJ (2007b). Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2, 811-821.
61. Toya M, Sato M, Haselmann U, Asakawa K, Brunner D, Antony C, Toda T (2007). Gamma-tubulin complex-mediated anchoring of spindle microtubules to spindle-pole bodies requires Msd1 in fission yeast. Nat Cell Biol 9, 646-653.
62. Ukil L, Varadaraj A, Govindaraghavan M, Liu HL, Osmani SA (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.
63. van Hemert MJ, Lamers GE, Klein DC, Oosterkamp TH, Steensma HY, van Heusden GP (2002). The Saccharomyces cerevisiae Fin1 protein forms cell cycle-specific filaments between spindle pole bodies. Proc Natl Acad Sci USA 99, 5390-5393.
64. von Zeska Kress MR, Harting R, Bayram O, Christmann M, Irmer H, Valerius O, Schinke J, Goldman GH, Braus GH (2012). The COP9 signalosome counteracts the accumulation of cullin SCF ubiquitin E3 RING ligases during fungal development. Mol Microbiol 83, 1162-1177.
65. Wu L, Osmani SA, Mirabito PM (1998). A role for NIMA in the nuclear localization of cyclin B in Aspergillus nidulans. J Cell Biol 141, 1575-1587.
66. Xiong Y, Oakley BR (2009). In vivo analysis of the functions of gamma-tubulin-complex proteins. J Cell Sci 122, 4218-4227.
67. Yang J, Adamian M, Li T (2006). Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol Biol Cell 17, 1033-1040.
68. Yang L, Ukil L, Osmani A, Nahm F, Davies J, De Souza CP, Dou X, Perez-Balaguer A, Osmani SA (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.
69. Ye XS, Fincher RR, Tang A, Osmani AH, Osmani SA (1998). Regulation of the anaphase-promoting complex/cyclosome by bimAAPC3 and proteolysis of NIMA. Mol Biol Cell 9, 3019-3030.
70. Ye XS, Xu G, Pu RT, Fincher RR, McGuire SL, Osmani AH, Osmani SA (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.
71. Yissachar N, Salem H, Tennenbaum T, Motro B (2006). Nek7 kinase is enriched at the centrosome, and is required for proper spindle assembly and mitotic progression. FEBS Lett 580, 6489-6495.