A screen for modifiers of cyclin E function in Drosophila melanogaster identifies Cdk2 mutations, revealing the insignificance of putative phosphorylation sites in Cdk2

Genetics

Volumn 155, Issue 1, 2000, Pages 233-244

  Lane, Mary Ellen ^a,b   Elend, Marion ^a,c   Heidmann, Doris ^a   Herr, Anabel ^a   Marzodko, Sandra ^a   Herzig, Alf ^a   Lehner, Christian F ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E;

ARTICLE; CELL CYCLE G1 PHASE; DROSOPHILA MELANOGASTER; GENE MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CDC2-CDC28 KINASES; CELL CYCLE PROTEINS; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; E2F TRANSCRIPTION FACTORS; ENHANCER ELEMENTS (GENETICS); EYE; EYE PROTEINS; GENES, INSECT; HOMEODOMAIN PROTEINS; INSECT PROTEINS; LARVA; MEMBRANE GLYCOPROTEINS; MUTAGENESIS; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR PROTEIN-TYROSINE KINASES; THREONINE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TYROSINE; ZYGOTE;

ARACHNIDA; DROSOPHILA MELANOGASTER; EUKARYOTA; HEXAPODA; MELANOGASTER;

EID: 0034058708     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (86)

1. ASANO, M., and R. P. WHARTON, 1999 E2F mediates developmental and cell cycle regulation of ORCI in Drosophila. EMBO J. 18: 2435-2448.
2. BASLER, K., B. CHRISTEN and E. HAFEN, 1991 Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64: 1069-1081.
3. BIER, E., H. VAESSIN, S. SHEPHERD, K. LEE, K. MCCALL et al., 1989 Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3: 1273-1287.
4. BLOMBERG, I., and I. HOFFMANN, 1999 Ectopic expression of Cdc25A accelerates the G1/S transition and leads to premature activation of cyclin E- and cyclin A-dependent kinases. Mol. Cell. Biol. 19: 6183-6194.
5. BREHM, A., E. A. MISKA, D. J. MCCANCE, J. L. REID, A. J. BANNISTER et al., 1998 Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391: 597-601.
6. BRITTON, J. S., and B. A. EDGAR, 1998 Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125: 2149-2158.
7. BROWN, V. D., R. A. PHILLIPS and B. L. GALLIE, 1999 Cumulative effect of phosphorylation of pRB on regulation of E2F activity. Mol. Cell. Biol. 19: 3246-3256.
8. CHEN, B., and A. E. PRZYBYIA, 1994 An efficient site-directed mutagenesis method based on PCR. Biotechniques 17: 657-659.
9. CLURMAN, B. E., R. J. SHEAFF, K. THRESS, M. GROUDINE and J. M. ROBERTS, 1996 Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev. 10: 1979-1990.
10. DENOOIJ, J. C., M. A. LETENDRE and I. K. HARIHARAN, 1996 A cyclin-dependent kinase inhibitor, dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87: 1237-1247.
11. DICKSON, B., and E. HAFEN, 1993 Genetic dissection of eye development in Drosophila, pp. 1327-1362 in The Development of Drosophila, edited by M. BATE and A. MARTINEZ ARIAS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
12. DICKSON, B. J., A. VANDERSTRATEN, M. DOMINGUEZ and E. HAFEN, 1996 Mutations modulating raf signaling in Drosophila eye development. Genetics 142: 163-171.
13. DU, W., and N. DYSON, 1999 The role of RBF in the introduction of G1 regulation during Drosophila embryogenesis. EMBO J. 18: 916-925.
14. DU, W., M. VIDAL, J. E. XIE and N. DYSON, 1996 RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev. 10: 1206-1218.
15. DULIC, V., E. LEES and S. I. REED, 1992 Association of human cyclin E with a periodic G(1)-S phase protein-kinase. Science 257: 1958-1961.
16. DURONIO, R. J., and P. H. O'FARRELL, 1995 Developmental control of the G1 to S transition in Drosophila - cyclin E is a limiting downstream target of E2F. Genes Dev. 9: 1456-1468.
17. DURONIO, R. J., P. H. O'FARRELL, J. E. XIE, A. BROOK and N. DYSON, 1995 The transcription factor E2F is required for S-phase during Drosophila embryogenesis. Genes Dev. 9: 1445-1455.
18. DURONIO, R. J., A. BROOK, N. DYSON and P. H. O'FARRELL, 1996 E2F-induced S phase requires cyclin E. Genes Dev. 10: 2505-2513.
19. DURONIO, R. J., P. C. BONNETTE and P. H. O'FARRELL, 1998 Mutations of the Drosophila dDP, dE2F, and cyclin E genes reveal distinct roles for the E2F-DP transcription factor and cyclin E during the G1-S transition. Mol. Cell. Biol. 18: 141-151.
20. DYNLACHT, B. D., M. S. BROOK, M. S. DEMBSKI, L. YENUSH and N. DYSON, 1994 DNA-binding and trans-activation properties by Drosophila E2F and DP proteins. Proc. Natl. Acad. Sci. USA 91: 6359-6363.
21. DYSON, N., 1998 The regulation of E2F by pRB-family proteins. Genes Dev. 12: 2245-2262.
22. FIELD, S. J., F. Y. TSAI, F. KUO, A. M. ZUBIAGA, W. G. KAELIN, JR. et al., 1996 E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85: 549-561.
23. GELLON, G., K. W. HARDING, N. MCGINNIS, M. M. MARTIN and W. MCGINNIS, 1997 A genetic screen for modifiers of Deformed homeotic function identifies novel genes required for head development. Development 124: 3321-3331.
24. GENG, Y., W. WHORISKEY, M. Y. PARK, R. T. BRONSON, R. H. MEDEMA et al., 1999 Rescue of cyclin D1 deficiency by knockin cyclin E. Cell 97: 767-777.
25. GU, Y., J. ROSENBLATT and D. O. MORGAN, 1992 Cell cycle regulation of cdk2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11: 3995-4005.
26. GUADAGNO, T. M., and J. W. NEWPORT, 1996 Cdk2 kinase is required for entry into mitosis as a positive regulator of cdc2-cyclin B kinase activity. Cell 84: 73-82.
27. HAO, X. F., L. ALPHEY, L. R. BANDARA, E. W. F. LAM, D. GLOVER et al., 1995 Functional conservation of the cell cycle-regulating transcription factor DRTF1/E2F and its pathway of control in Drosophila melanogaster. J. Cell Sci. 108: 2945-2954.
28. HARBOUR, J. W., R. X. LUO, A. DEI SANTI, A. A. POSTIGO and D. C. DEAN, 1999 Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 98: 859-869.
29. HELIN, K., 1998 Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev. 8: 28-35.
30. HINCHCLIFFE, E. H., C. LI, E. A. THOMPSON, J. L. MALLER and G. SLUDER, 1999 Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283: 851-854.
31. HINDS, P. W., S. MITTNACHT, V. DULIC, A. ARNOLD, S. I. REED et al., 1992 Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70: 993-1006.
32. HOFFMANN, I., G. DRAETTA and E. KARSENTI, 1994 Activation of the phosphatase activity of human cdc25A by a cdk2/cyclin E-dependent phosphorylation at the G1/S transition. EMBO J. 13: 4302-4310.
33. HUA, X. H., and J. NEWPORT, 1998 Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J. Cell. Biol. 140: 271-281.
34. HUA, X. H., H. YAN and J. NEWPORT, 1997 A role for cdk2 kinase in negatively regulating DNA replication during S phase of the cell cycle. J. Cell. Biol. 137: 183-192.
35. Gpl. J. Cell Biol. 130: 755-769.
36. JINNO, S., K. SUTO, A. NAGATA, M. IGARASHI, Y. KANAOKA et al., 1994 Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J. 13: 1549-1556.
37. JOHNSTON, L. A., and B. A. EDGAR, 1998 Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394: 82-84.
38. KARR, T. L., 1991 Intracellular sperm egg interactions in Drosophila: a 3-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 34: 101-111.
39. KELLY, B. L., K. G. WOLFE and J. M. ROBERTS, 1998 Identification of a substrate-targeting domain in cyclin E necessary for phosphorylation of the retinoblastoma protein. Proc. Natl. Acad. Sci. USA 95: 2535-2540.
40. KIM, S. H., C. LI and J. L. MALLER, 1999 A maternal form of the phosphatase Cdc25A regulates early embryonic cell cycles in Xenopus laevis. Dev. Biol. 212: 381-391.
41. KITAGAWA, M., H. HIGASHI, H. K. JUNG, I. SUZUKITAKAHASHI, M. IKEDA et al., 1996 The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15: 7060-7069.
42. KNOBLICH, J. A., K. SAUER, L. JONES, H. RICHARDSON, R. SAINT et al., 1994 Cyclin E controls S phase progression and its downregulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77: 107-120.
43. KOFF, A., A. GIORDANO, D. DESAI, K. YAMASHITA, J. W. HARPER et al., 1992 Formation and activation of a cyclin E-cdk2 complex during the G1-phase of the human cell cycle. Science 257: 1689-1694.
44. KOLODZIEJ, P. A., L. Y. JAN and Y. N. JAN, 1995 Mutations that affect the length, fasciculation, or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron 15: 273-286.
45. KUANG, B., S. WU, Y. SHIN, K.A. MACE, L. LUO and P. KOLODZIEJ, 1999 split ends is required for axon growth and guidance in Drosophila embryos and encodes a member of a new family of proteins containing RNP motifs. Development 127: 1517-1529.
46. LACEY, K. R., P. K. JACKSON and T. STEARNS, 1999 Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. USA 96: 2817-2822.
47. LANE, M. E., K. SAUER, K. WALLACE, Y. N. JAN, C. F. LEHNER et al., 1996 Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87: 1225-1236.
48. LEHNER, C. F., and P. H. O'FARRELL, 1989 Expression and function of Drosophila cyclin A during embryonic cell cycle progression. Cell 56: 957-968.
49. LEHNER, C. F., and P. H. O'FARRELL, 1990 Drosophila cdc2 homologs - a functional homolog is coexpressed with a cognate variant. EMBO J. 9: 3573-3581.
50. LEHNER, C. F., N. YAKUBOVICH and P. H. O'FARRELL, 1991 Exploring the role of Drosophila cyclin A in the regulation of S-phase. Cold Spring Harbor Symp. Quant. Biol. 56: 465-475.
51. LENG, X. H., L. CONNELLCROWLEY, D. GOODRICH and J. W. HARPER, 1997 S-phase entry upon ectopic expression of G1 cyclin-dependent kinases in the absence of retinoblastoma protein phosphorylation. Curr. Biol. 7: 709-712.
52. LEW, D. J., V. DULIC and S. I. REED, 1991 Isolation of three novel human cyclins by rescue of G1 cyclin (CLN) function in yeast. Cell 66: 1197-1206.
53. LUKAS, J., T. HERZINGER, K. HANSEN, M. C. MORONI, D. RESNITZKY et al., 1997 Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes Dev. 11: 1479-1492.
54. LUNDBERG, A. S., and R. A. WEINBERG, 1998 Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol. Cell. Biol. 18: 753-761.
55. LUO, R. X., A. A. POSTIGO and D. C. DEAN, 1998 Rb interacts with histone deacetylase to repress transcription. Cell 92: 463-473.
56. MAGNAGHI-JAULIN, L., R. GROISMAN, I. NAGUIBNEVA, P. ROBIN, S. LORAIN et al., 1998 Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391: 601-605.
57. MATSUMOTO, Y., K. HAYASHI and E. NISHIDA, 1999 Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr. Biol. 9: 429-432.
58. MITTNACHT, S., 1998 Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8: 21-27.
59. MONTAGNOLI, A., F. FIORE, E. EYTAN, A. C. CARRANO, G. F. DRAETTA et al., 1999 Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev. 13: 1181-1189.
60. OHTANI, K., and J. R. NEVINS, 1994 Functional properties of a Drosophila homolog of the E2F1 gene. Mol. Cell. Biol. 14: 1603-1612.
61. PIRROTTA, V., 1988 Vectors for P-element transformation in Drosophila, pp. 437-456 in Vectors. A Survey of Cloning Vectors and Their Uses, edited by R. L. RODRIGUEZ and D. T. DENHARDT. Butterworths, Boston and London.
62. RESNITZKY, D., and S. I. REED, 1995 Different roles for cyclin D1 and cyclin E in regulation of the G1 to S transition. Mol. Cell. Biol. 15: 3463-3469.
63. RICHARDSON, H. E., L. V. O'KEEFE, S. I. REED and R. SAINT, 1993 A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis. Development 119: 673-690.
64. RICHARDSON, H., L. V. O'KEEFE, T. MARTY and R. SAINT, 1995 Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121: 3371-3379.
65. ROYZMAN, I., A. J. WHITTAKER and T. L. ORR-WEAVER, 1997 Mutations in Drosophila DP and E2F distinguish G(1)-S progression from an associated transcriptional program. Genes Dev. 11: 1999-2011.
66. SAUER, K., J. A. KNOBLICH, H. RICHARDSON and C. F. LEHNER, 1995 Distinct modes of cyclin E/cdc2c kinase regulation and S phase control in mitotic and endoreduplication cycles of Drosophila embryogenesis. Genes Dev. 9: 1327-1339.
67. SAWADO, T., M. YAMAGUCHI, Y. NISHIMOTO, K. OHNO, K. SAKAGUCHI et al., 1998 dE2F2, a novel E2F-family transcription factor in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 251: 409-415.
68. SECOMBE, J., J. PISPA, R. SAINT and H. RICHARDSON, 1999 Analysis of a Drosophila cyclin E hypomorphic mutation suggests a novel role of Cyclin E in cell proliferation control during eye imaginal disc development. Genetics 149: 1867-1882.
69. SEXL, V., J. A. DIEHL, C. J. SHERR, R. ASHMUN, D. BEACH et al., 1999 A rate limiting function of cdc25A for S phase entry inversely correlates with tyrosine dephosphorylation of Cdk2. Oncogene 18: 573-582.
70. SHEAFF, R. J., M. GROUDINE, M. GORDON, J. M. ROBERTS and B. E. CLURMAN, 1997 Cyclin E-CDK2 is a regulator of p27(Kip1). Genes Dev. 11: 1464-1478.
71. SPRADLING, A. C., D. M. STERN, I. KISS, J. ROOTE, T. LAVERTY et al., 1995 Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92: 10824-10830.
72. SPRENGER, F., N. YAKUBOVICH and P. H. O'FARRELL, 1997 S phase function of Drosophila cyclin A and its downregulation in G1 phase. Curr. Biol. 7: 488-499.
73. STAEHLING-HAMPTON, K., P. J. CIAMPA, A. BROOK and N. DYSON, 1999 A genetic screen for modifiers of E2F in Drosophila melanogaster. Genetics 153: 275-287.
74. STERN, B., G. RIED, N. J. CLEGG, T. A. GRIGLIATTI and C. F. LEHNER, 1993 Genetic analysis of the Drosophila cdc2 homolog. Development 117: 219-232.
75. STRAUSFELD, U. P. M., M. HOWELL, P. DESCOMBES, S. CHEVALIER, R. E. REMPEL et al., 1996 Both cyclin A and cyclin E have S-phase promoting (SPF) activity in Xenopus egg extracts. J. Cell Sci. 109: 1555-1563.
76. THOMAS, B. J., D. A. GUNNING, J. CHO and S. L. ZIPURSKY, 1994 Cell cycle progression in the developing Drosophila eye - roughex encodes a novel protein required for the establishment of G1. Cell 77: 1003-1014.
77. VLACH, J., S. HENNECKE and B. AMATI, 1997 Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27(Kip1). EMBO J. 16: 5334-5344.
78. WANG, Z., and S. LINDQUIST, 1998 Developmentally regulated nuclear transport of transcription factors in Drosophila embryos enables the heat shock response. Development 125: 4841-4850.
79. WEINBERG, R. A., 1995 The retinoblastoma protein and cell-cycle control. Cell 81: 323-330.
80. WIELLETTE, E. L., K. W. HARDING, K. A. MACE, M. R. RONSHAUGEN, F. Y. WANG et al., 1999 spen encodes an RNP motif protein that interacts with hox pathways to repress the development of head-like sclerites in the Drosophila trunk. Development 126: 5373-5385.
81. WOLFF, T., and D. F. READY, 1993 Pattern formation in the Drosophila retina, pp. 1277-1326 in The Development of Drosophila melanogaster, edited by M. BATE and A. MATINEZ ARIAS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
82. WON, K. A., and S. I. REED, 1996 Activation of cyclin E/CDK2 is coupled to site-specific autophosphorylation and ubiquitin-dependent degradation of cyclin. EMBO J. 15: 4182-4193.
83. XU, X., and S. P. BURKE, 1996 Roles of active-site residues and the NH2-terminal domain in the catalysis and substrate-binding of human cdc25. J. Biol. Chem. 271: 5118-5124.
84. YAMASAKI, L., T. JACKS, R. BRONSON, E. GOILLOT, E. HARLOW et al., 1996 Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 85: 537-548.
85. ZARKOWSKA, T., and S. MITTNACHT, 1997 Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J. Biol. Chem. 272: 12738-12746.
86. ZHANG, H. S., A. A. POSTIGO and D. C. DEAN, 1999 Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16INK4a, TGFbeta, and contact inhibition. Cell 97: 53-61.