Drosophila Myt1 is the major Cdk1 inhibitory kinase for wing imaginal disc development

Genetics

Volumn 180, Issue 4, 2008, Pages 2123-2133

  Jin, Zhigang ^a,b   Homola, Ellen ^a   Tiong, Stanley ^a   Campbell, Shelagh D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MYT1; PROTEIN TYROSINE KINASE; PROTEIN WEE1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DROSOPHILA; FORELIMB; GENE INTERACTION; GENE MUTATION; IONIZING RADIATION; LARVAL DEVELOPMENT; MITOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; ZYGOTE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CDC2 PROTEIN KINASE; CELL CYCLE; CELL CYCLE PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; WING;

METAZOA;

EID: 61849108631     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.093195     Document Type: Article

References (69)

1. ABRAMS, J. M., 2002 Competition and compensation: coupled to death in development and cancer. Cell 110: 403-406.
2. BLAIR, S. S., 1993 Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila. Development 119: 339-351.
3. BOOHER, R. N., P. S. HOLMAN and A. FATTAEY, 1997 Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol. Chem. 272: 22300-22306.
4. BRODSKY, M. H., J. J. SEKELSKY, G. TSANG, R. S. HAWLEY and G. M. RUBIN, 2000 mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14: 666-678.
5. BURROWS, A. E., B. K. SCEURMAN, M. E. KOSINSKI, C. T. RICHIE, P. L. SADLER et al., 2006 The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133: 697-709.
6. CAMPBELL, S. D., F. SPRENGER, B. A. EDGAR and P. H. O'FARRELL, 1995 Drosophila Wee1 kinase rescues fission yeast from mitotic catastrophe and phosphorylates Drosophila Cdc2 in vitro. Mol. Biol. Cell 6: 1333-1347.
7. CORNWELL, W. D., P. J. KAMINSKI and J. R. JACKSON, 2002 Identification of Drosophila Myt1 kinase and its role in Golgi duringmitosis. Cell Signal 14: 467-476.
8. EDGAR, B. A., and P. H. O'FARRELL, 1989 Genetic control of cell division patterns in the Drosophila embryo. Cell 57: 177-187.
9. EDGAR, B. A., and P. H. O'FARRELL, 1990 The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell 62: 469-480.
10. EXTAVOUR, C., and A. GARCIA-BELLIDO, 2001 Germ cell selection in genetic mosaics in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 11341-11346.
11. FICHELSON, P., and M. GHO, 2004 Mother-daughter precursor cell fate transformation after Cdc2 down-regulation in the Drosophila bristle lineage. Dev. Biol. 276: 367-377.
12. GARCIA-BELLIDO, A., F. CORTES and M. MILAN, 1994 Cell interactions in the control of size in Drosophila wings. Proc. Natl. Acad. Sci. USA 91: 10222-10226.
13. GROSSHANS, J., and E. WIESCHAUS, 2000 A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101: 523-531.
14. HAGTING, A., C. KARLSSON, P. CLUTE, M. JACKMAN and J. PINES, 1998 MPF localization is controlled by nuclear export. EMBO J. 17: 4127-4138.
15. HEALD, R., M. MCLOUGHLIN and F. MCKEON, 1993 Human wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase. Cell 74: 463-474.
16. HENDZEL, M. J., Y. WEI, M. A. MANCINI, A. VAN HOOSER, T. RANALLI et al., 1997 Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
17. INOUE, D., and N. SAGATA, 2005 The Polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs. EMBO J. 24: 1057-1067.
18. IVANOVSKA, I., E. LEE, K. M. KWAN, D. D. FENGER and T. L. ORR-WEAVER, 2004 The Drosophila MOS ortholog is not essential for meiosis. Curr. Biol. 14: 75-80.
19. JACK, J., and Y. DELOTTO, 1992 Effect of wing scalloping mutations on cut expression and sense organ differentiation in the Drosophila wing margin. Genetics 131: 353-363.
20. JIN, Z., E. M. HOMOLA, P. GOLDBACH, Y. CHOI, J. A. BRILL et al., 2005 Drosophila Myt1 is a Cdk1 inhibitory kinase that regulates multiple aspects of cell cycle behavior during gametogenesis. Development 132: 4075-4085.
21. KIM, E. M., and D. J. BURKE, 2008 DNA damage activates the SAC in an ATM/ATR-dependent manner, independently of the kinetochore. PLoS Genet. 4: e1000015.
22. KONDYLIS, V., S. E. GOULDING, J. C. DUNNE and C. RABOUILLE, 2001 Biogenesis of Golgi stacks in imaginal discs of Drosophila melanogaster. Mol. Biol. Cell 12: 2308-2327.
23. KORNBLUTH, S., B. SEBASTIAN, T. HUNTER and J. NEWPORT, 1994 Membranelocalization of the kinase which phosphorylates p34cdc2 on threonine 14. Mol. Biol. Cell 5: 273-282.
24. LAMITINA, S. T., and S. W. L'HERNAULT, 2002 Dominant mutations in the Caenorhabditis elegans Myt1 ortholog wee-1.3 reveal a novel domain that controls M-phase entry during spermatogenesis. Development 129: 5009-5018.
25. LEE, S., and L. COOLEY, 2007 Jagunal is required for reorganizing the endoplasmic reticulum during Drosophila oogenesis. J. Cell Biol. 176: 941-952.
26. LEHMAN, D. A., B. PATTERSON, L. A. JOHNSTON, T. BALZER, J. S. BRITTON et al., 1999 Cis-regulatory elements of the mitotic regulator, string/Cdc25. Development 126: 1793-1803.
27. LEISE, W., III, and P. R. MUELLER, 2002 Multiple Cdk1 inhibitory kinases regulate the cell cycle during development. Dev. Biol. 249: 156-173.
28. LIU, F., C. ROTHBLUM-OVIATT, C. E. RYAN and H. PIWNICA-WORMS, 1999 Overproduction of human Myt1 kinase induces a G2 cell cycle delay by interfering with the intracellular trafficking of Cdc2-cyclin B1 complexes. Mol. Cell. Biol. 19: 5113-5123.
29. LIU, F., J. J. STANTON, Z. WU and H. PIWNICA-WORMS, 1997 The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex. Mol. Cell. Biol. 17: 571-583.
30. LUNDGREN, K., N. WALWORTH, R. BOOHER, M. DEMBSKI, M. KIRSCHNER et al., 1991 mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64: 1111-1122.
31. MASUI, Y., 1992 Towards understanding the control of the division cycle in animal cells. Biochem. Cell Biol. 70: 920-945.
32. MATA, J., S. CURADO, A. EPHRUSSI and P. RORTH, 2000 Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101: 511-522.
33. MILAN, M., S. CAMPUZANO and A. GARCIA- BELLIDO, 1996 Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc. Natl. Acad. Sci. USA 93: 640-645.
34. MUELLER, P. R., T. R. COLEMAN, A. KUMAGAI and W. G. DUNPHY, 1995 Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270: 86-90.
35. MURAKAMI, M. S., S. A. MOODY, I. O. DAAR and D. K. MORRISON, 2004 Morphogenesis during Xenopus gastrulation requires Wee1-mediated inhibition of cell proliferation. Development 131: 571-580.
36. MUSARO, M., L. CIAPPONI, B. FASULO, M. GATTI and G. CENCI, 2008 Unprotected Drosophila melanogaster telomeres activate the spindle assembly checkpoint. Nat. Genet. 40: 362-366.
37. NAKAJIMA, H., S. YONEMURA, M. MURATA, N. NAKAMURA, H. PIWNICA-WORMS et al., 2008 Myt1 protein kinase is essential for Golgi and ER assembly during mitotic exit. J. Cell Biol. 181: 89-103.
38. NAKANISHI, M., H. ANDO, N. WATANABE, K. KITAMURA, K. ITO et al., 2000 Identification and characterization of human Wee1B, a new member of the Wee1 family of Cdk-inhibitory kinases. Genes Cells 5: 839-847.
39. NEEL, J. V., 1940 The pattern of supernumerary macrochaetae in certain Drosophila mutants. Genetics 25: 251-277.
40. NEUFELD, T. P., A. F. DE LA CRUZ, L. A. JOHNSTON and B. A. EDGAR, 1998 Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183-1193.
41. NIGG, E. A., W. KREK and M. PETER, 1991 Vertebrate cdc2 kinase: its regulation by phosphorylation and its mitotic targets. Cold Spring Harbor Symp. Quant. Biol. 56: 539-547.
42. NIIDA, H., and M. NAKANISHI, 2006 DNA damage checkpoints in mammals. Mutagenesis 21: 3-9.
43. NURSE, P., and P. THURIAUX, 1980 Regulatory genes controlling mitosis in the fission yeast Schizosaccharomyces pombe. Genetics 96: 627-637.
44. O'BROCHTA, D. A., and P. J. BRYANT, 1985 A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature 313: 138-141.
45. O'CONNELL, M. J., J. M. RALEIGH, H. M. VERKADE and P. NURSE, 1997 Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16: 545-554.
46. OKAMOTO, K., N. NAKAJO and N. SAGATA, 2002 The existence of two distinct Wee1 isoforms in Xenopus: implications for the developmental regulation of the cell cycle. EMBO J. 21: 2472-2484.
47. OKUMURA, E., T. FUKUHARA, H. YOSHIDA, S. HANADA SI, R. KOZUTSUMI et al., 2002 Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat. Cell Biol. 4: 111-116.
48. PALMER, A., A. C. GAVIN and A. R. NEBREDA, 1998 A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 17: 5037-5047.
49. PARKER, L. L., P. J. SYLVESTRE, M. J. BYRNES, 3RD, F. LIU and H. PIWNICA-WORMS, 1995 Identification of a 95-kDa WEE1-like tyrosine kinase in HeLa cells. Proc. Natl. Acad. Sci. USA 92: 9638-9642.
50. PETER, M., J. C. LABBE, M. DOREE and E. MANDART, 2002 A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. Development 129: 2129-2139.
51. POON, R. Y., M. S. CHAU, K. YAMASHITA and T. HUNTER, 1997 The role of Cdc2 feedback loop control in the DNA damage checkpoint in mammalian cells. Cancer Res. 57: 5168-5178.
52. PRICE, D., S. RABINOVITCH, P. H. O'FARRELL and S. D. CAMPBELL, 2000 Drosophila wee1 has an essential role in the nuclear divisions of early embryogenesis. Genetics 155: 159-166.
53. PRICE, D. M., Z. JIN, S. RABINOVITCH and S. D. CAMPBELL, 2002 Ectopic expression of the Drosophila Cdk1 inhibitory kinases, Wee1 and Myt1, interferes with the second mitotic wave and disrupts pattern formation during eye development. Genetics 161: 721-731.
54. PROKOPENKO, S. N., and W. CHIA, 2005 When timing is everything: role of cell cycle regulation in asymmetric division. Semin. Cell Dev. Biol. 16: 423-437.
55. RHIND, N., B. FURNARI and P. RUSSELL, 1997 Cdc2 tyrosine phosphorylation is required for the DNA damage checkpoint in fission yeast. Genes Dev. 11: 504-511.
56. RHIND, N., and P. RUSSELL, 2001 Roles of the mitotic inhibitors Wee1 and Mik1 in the G(2) DNA damage and replication checkpoints. Mol. Cell. Biol. 21: 1499-1508.
57. ROYOU, A., H. MACIAS and W. SULLIVAN, 2005 The Drosophila Grp/ Chk1 DNA damage checkpoint controls entry into anaphase. Curr. Biol. 15: 334-339.
58. SANCHEZ, Y., J. BACHANT, H. WANG, F. HU, D. LIU et al., 1999 Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286: 1166-1171.
59. SEHER, T. C., and M. LEPTIN, 2000 Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr. Biol. 10: 623-629.
60. STUMPFF, J., T. DUNCAN, E. M. HOMOLA, S. D. CAMPBELL and T. T. SU, 2004 Drosophila Wee1 kinase regulates Cdk1 and mitotic entry during embryogenesis. Curr. Biol. 14: 2143-2148.
61. TILNEY, L. G., and D. J. DEROSIER, 2005 How to make a curved Drosophila bristle using straight actin bundles. Proc. Natl. Acad. Sci. USA 102: 18785-18792.
62. TIO, M., G. UDOLPH, X. YANG and W. CHIA, 2001 cdc2 links the Drosophila cell cycle and asymmetric division machineries. Nature 409: 1063-1067.
63. TOMINAGA, Y., C. LI, R. H. WANG and C. X. DENG, 2006 Murine Wee1 plays a critical role in cell cycle regulation and pre-implantation stages of embryonic development. Int. J. Biol. Sci. 2: 161-170.
64. WELLS, N. J., N. WATANABE, T. TOKUSUMI, W. JIANG, M. A. VERDECIA et al., 1999 The C-terminal domain of the Cdc2 inhibitory kinase Myt1 interacts with Cdc2 complexes and is required for inhibition of G(2)/M progression. J. Cell Sci. 112(Pt 19): 3361-3371.
65. WILSON, M. A., R. V. HOCH, N. R. ASHCROFT, M. E. KOSINSKI and A. GOLDEN, 1999 A Caenorhabditis elegans wee1 homolog is expressed in a temporally and spatially restricted pattern during embryonic development. Biochim. Biophys. Acta 1445: 99-109.
66. WULFKUHLE, J. D., N. S. PETERSEN and J. J. OTTO, 1998 Changes in the F-actin cytoskeleton during neurosensory bristle development in Drosophila: the role of singed and forked proteins. Cell Motil. Cytoskeleton 40: 119-132.
67. YANG, J., H. SONG, S. WALSH, E. S. BARDES and S. KORNBLUTH, 2001 Combinatorial control of cyclin B1 nuclear trafficking through phosphorylation at multiple sites. J. Biol. Chem. 276: 3604-3609.
68. YU, S. Y., S. J. YOO, L. YANG, C. ZAPATA, A. SRINIVASAN et al., 2002 A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129: 3269-3278.
69. ZHOU, Y., J. B. ATKINS, S. B. ROMPANI, D. L. BANCESCU, P. H. PETERSEN et al., 2007 The mammalian Golgi regulates numb signaling in asymmetric cell division by releasing ACBD3 during mitosis. Cell 129: 163-178.