A role for phosphorylation by casein kinase II in modulating antennapedia activity in Drosophila

Genes and Development

Volumn 11, Issue 10, 1997, Pages 1327-1340

  Jaffe, Leah ^a   Ryoo, Hyung Don ^a   Mann, Richard S ^a  

^a The New York Presbyterian Hospital   (United States)

Author keywords

Antennapedia; casein kinase II; extradenticle; Homeotic protein (HOX); phenotypic suppression; phosphorylation

Indexed keywords

CASEIN KINASE II;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; DROSOPHILA; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TARGET CELL;

EID: 0031007898     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.10.1327     Document Type: Article

References (84)

1. Berberich, S.J. and M.D. Cole. 1992. Casein kinase II inhibits the DNA-binding activity of Max homodimers but not Myc/ Max heterodimers. Genes & Dev. 6: 166-176.
2. Bienz, M. 1994. Homeotic genes and positional signaling in the Drosophila viscera. Trends Genet. 10: 22-26.
3. Bier, E., L.Y. Jan, and Y.N. Jan. 1990. rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes & Dev. 4: 190-203.
4. Botas, J. 1993. Control of morphogenesis and differentiation by HOM/Hox genes. Curr. Opin. Cell Biol. 5: 1015-1022.
5. Bourbon, J.-M., E. Martin-Blanco, D. Rosen, and T.B. Kornberg. 1995. Phosphorylation of the Drosophila engrailed protein at a site outside its homeodomain enhances DNA binding. J. Biol. Chem. 270: 11130-11139.
6. Burglin, T. 1994. A comprehensive classification of homeobox genes. In Guidebook to the homeobox genes (ed. D. Duboule), pp. 26-71. Oxford University Press, Oxford, UK.
7. Celniker, S.E., D.J. Keelan, and E.B. Lewis. 1989. The molecular genetics of the bithorax complex of Drosophila: Characterization of the products of the Abdominal-B domain. Genes & Dev. 3: 1424-1436.
8. Chan, S.-K. and R.S. Mann. 1993. The segment identity functions of Ultrabithorax are contained within its homeo domain and carboxy-terminal sequences. Genes & Dev. 7: 796-811.
9. Chan, S.-K., L. Jaffe, M. Capovilla, J. Botas, and R.S. Mann. 1994. The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with Extradenticle, another homeoprotein. Cell 78: 603-615.
10. Chan, S.-K., H. Pöpperl, R. Krumlauf, and R.S. Mann. 1996. An extradenticle-induced conformational change in a HOX protein overcomes an inhibitory function of the conserved hexapeptide motif. EMBO J. 15: 2477-2488.
11. Chien, C.-T., P. Bartel, R. Sternglanz, and S. Fields. 1991. The two-hybrid system: A method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. 88: 9578-9582.
12. Chisaka, O., T.S. Musci, and M.R. Capecchi. 1992. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature 355: 516-520.
13. Cohen, S.M., G. Bronner, F. Kuttner, G. Jürgens, and H. Jäckle. 1989. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338: 432-434.
14. Colberg-Poley, A.M., S.D. Voss, K. Chowdhury, C.L. Stewart, E.F. Wagner, and P. Gruss. 1985. Clustered homeo boxes are differentially expressed during murine development. Cell 43: 39-45.
15. Cowley, S., H. Paterson, P. Kemp, and C.J. Marshall. 1994. Activation of MAP kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH3T3 cells. Cell 77: 841-852.
16. Dalton, D., R. Chadwick, and W. McGinnis. 1989. Expression and embryonic function of empty spiracles: A Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes & Dev. 3: 1940-1956.
17. Desplan, C., J. Theis, and P.H. O'Farrell. 1985. The Drosophila developmental gene, engrailed, encodes a sequence-specific DNA binding activity. Nature 318: 630-635.
18. _. 1988. The sequence specificity of homeodomain-DNA interaction. Cell 54: 1081-1090.
19. Duboule, D. 1991. Patterning in the vertebrate limb. Curr. Opin. Gen. Dev. 1: 211-216.
20. Durfee, T., K. Becherer, P.-L. Chen, S.-H. Yeh, Y. Yang, A.E. Kilburn, W.-H. Lee, and S.J. Elledge. 1993. The retinoblastoma protein associates with the protein phosphatase type I catalytic subunit. Genes & Dev. 7: 555-569.
21. Ekker, S.C., D.G. Jackson, D.P. von Kessler, B.I. Sun, K.E. Young, and P.A. Beachy. 1994. The degree of variation in DNA sequence recognition among four Drosophila homeotic proteins. EMBO J. 13: 3551-3560.
22. Frasch, M., T. Hoey, C. Rushlow, H. Doyle, and M. Levine. 1987. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 6: 749-759.
23. Freeman, M., C. Klambt, C.S. Goodman, and G.M. Rubin. 1992. The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye. Cell 69: 963-975.
24. Garcia-Bellido, A. 1975. Genetic control of wing disc development in Drosophila. In Cell patterning, Ciba Found. Symp. (ed. S. Brenner), pp. 161-182. Associated Scientific Publishers, New York, NY.
25. Gavis, E.R. and D.S. Hogness. 1991. Phosphorylation, expression and function of the Ultrabithorax protein family in Drosophila melanogaster. Devopment 112: 1077-1093.
26. Gibson, G. and W.J. Gehring. 1988. Head and thoracic transformation caused by ectopic expression of Antennapedia during Drosophila development. Development 102: 657-675.
27. Gibson, G., A. Schier, P. LeMotte, and W.J. Gehring. 1990. The specificities of Sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell 62: 1087-1103.
28. Glicksman, M.A. and D.L. Brower. 1988. Misregulation of homeotic gene expression in Drosophila larvae resulting from mutations at the extra sex combs locus. Dev. Biol. 126: 219-227.
29. Glover, C.V.C., E.R. Shelton, and D.L. Brutlag. 1983. Purification and characterization of a type II casein kinase from Drosophila melanogaster. J. Biol. Chem. 258: 3258-3265.
30. Gonzalez-Reyes, A. and G. Morata. 1990. The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products. Cell 61: 515-522.
31. Gonzalez-Reyes, A., N. Urquia, W.J. Gehring, G. Struhl, and G. Morata. 1990. Are cross-regulatory interactions between homoeotic genes functionally significant? Nature 344: 78-80.
32. Hanes, S.D. and R. Brent. 1989. DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57: 1275-1283,
33. Hoey, T., R. Warrior, J. Manak, and M. Levine. 1988. DNA-binding activities of the Drosophila melanogaster evenskipped protein are mediated by its homeo domain and influenced by protein context. Mol. Cell. Biol. 8: 4598-4607.
34. Hupp, T.R., D.W. Meek, C.A. Midgley, and D.P. Lane. 1992. Regulation of the specific DNA binding function of p53. Cell 71: 875-886.
35. Ip, Y.T., R.E. Park, D. Kosman, E. Bier, and M. Levine. 1992. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes & Dev. 6: 1728-1739.
36. Jiang, J., D. Kosman, Y.T. Ip, and M. Levine. 1991. The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes & Dev. 5: 1881-1891.
37. Jones, B. and W. McGinnis. 1993. The regulation of empty spiracles by Abdominal-B mediates an abdominal segment identity function. Genes & Dev. 7: 229-240.
38. Karch, F., W. Bender, and B. Weiffenbach. 1990. abdA expression in Drosophila embryos. Genes & Dev. 4: 1573-1587.
39. Kenyon, C. and B. Wang. 1991. A cluster of Antennapedia-class homeobox genes in a nonsegmented animal. Science 253: 516-517.
40. Knighton, D.R., J. Zheng, L.F. Ten Eyck, V.A. Ashford, N.-H. Xuong, and J.M. Sowadski. 1991a. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253: 407-414.
41. Knighton, D.R., J. Zheng, L.F. Ten Eyck, N.-H. Xuong, S. Taylor, and J.M. Sowadski. 1991b. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253: 414-420.
42. Lamka, M.L., A.M. Boulet, and S. Sakonju. 1992. Ectopic expression of UBX and ABD-B proteins during Drosophila embryogenesis: Competition, not a functional hierarchy, explains phenotypic suppression. Development 116: 841-854.
43. Lewis, E.B. 1978. A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
44. Lin, A., J. Frost, T. Deng, T. Smeal, N. Al-Alawi, U. Kikkawa, T. Hunter, D. Brenner, and M. Karin. 1992. Casein kinase II is a negative regulator of c-Jun DNA binding and AP-1 activity. Cell 70: 777-789.
45. Lin, L. and W. McGinnis. 1992. Mapping functional specificity in the Dfd and Ubx homeo domains. Genes & Dev. 6: 1071-1081.
46. Lohs-Schardin, M., C. Cremer, and V.C. Nüsslein. 1979. A fate map for the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev. Biol. 73: 239-255.
47. Lopez, A.J. and D.S. Hogness. 1991. Immunochermcal dissection of the Ultrabithorax homeoprotein family in Drosophila melanogaster. Proc. Natl. Acad. Sci. 88: 9924-9928.
48. Luban, J., K.L. Bossolt, E.K. Franke, G.V. Kalpana, and S.P. Goff. 1993. Human immunodeficeincy virus type I Gag protein binds to cyclophilins A and Ab. Cell 73: 1067-1078.
49. Lufkin, T., M. Mark, C.P. Hart, P. Dolle, M. LeMeur, and P. Chambon. 1992. Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 359: 835-841.
50. Manak, J.R., N. de-Bisschop, R.M. Kris, and R. Prywes. 1990. Casein kinase II enhances the DNA binding activity of serum response factor. Genes &. Dev. 4: 955-967.
51. Mann, R.S. and S.-K. Chan. 1996. Extra specificity from extradenticle: The partnership between HOX and exd/pbx homeodomain proteins. Trends Genet. 12: 258-262.
52. Mann, R.S. and D.S. Hogness. 1990. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell 60: 597-610.
53. Marchiori, F., F. Meggio, O. Marin, G. Borin, A. Calderan, P. Ruzza, and L.A. Pinna. 1988. Synthetic peptide substrates for casein kinase 2. Assessment of minimum structural requirements for phosphorylation. Biochim. Biophys. Acta. 971: 332-338.
54. Mayer, U. and V.C. Nüsslein. 1988. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes & Dev. 2: 1496-1511.
55. McCormick, A., N. Core, S. Kerridge, and M.P. Scott. 1995. Homeotic response elements are tightly linked to tissue-specific elements in a transcriptional enhancer of the teashirt gene. Development 121: 2799-2812.
56. Njlstad, P.R., A. Molven, J. Apold, and A. Fjose. 1990. The zebrafish homeobox gene hox-2.2: Transcription unit, potential regulatory regions and in situ localization of transcripts. EMBO J. 9: 515-524.
57. Padgett, R.W., D. St. Johnston, and W.M. Gelbart. 1987. A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature 325: 81-84.
58. Panganiban, G.E., R. Reuter, M.P. Scott, and F.M. Hoffmann, 1990. A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110: 1041-1050.
59. Papavassiliou, A.G., M. Treier, and D. Bohmann. 1995. Intra-molecular signal transduction in cJUN. EMBO J. 14: 2014-2019.
60. Price, J.V., R.J. Clifford, and T. Schupbach. 1989. The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog. Cell 56: 1085-1092.
61. Rauskolb, C. and E. Wieschaus 1994. Coordinate regulation of downstream genes by extradenticle and the homeotic selector proteins. EMBO J. 13: 3561-3569.
62. Raz, E. and B.Z. Shilo. 1993. Establishment of ventral cell fates in the Drosophila embryonic ectoderm requires DER, the EGF receptor homolog. Genes & Dev. 7: 1937-1948.
63. Roder, L., C. Vola, and S. Kerridge. 1992. The role of the teashirt gene in trunk segmental identity in Drosophila. Development 115: 1017-1033.
64. Rutledge, B.J., K. Zhang, E. Bier, Y.N. Jan, and N. Perrimon. 1992. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes & Dev. 6: 1503-1517.
65. Saxena, A., R. Padmanabha, and C.V. Glover. 1987. Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II. Mol. Cell. Biol. 7: 3409-3417.
66. Schejter, E.D. and B.-Z. Shilo. 1989. The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell 56: 1093-1104.
67. Schiestle, R.H. and R.D. Geitz. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16: 339-346.
68. Schneuwly, S., A. Kuriowa, P. Baumgartner, and W.J. Gehring. 1986. Structural organization and sequence of the homeotic gene Antennapedia of Drosophila melanogaster. EMBO J. 5: 733-739.
69. Schughart, K., M.F. Utset, A. Awgulewitsch, and F.H. Ruddle. 1988. Structure and expression of Hox-2.2, a murine homeobox-containing gene. Proc. Natl. Acad. Sci. 85: 5582-5586.
70. Schughart, K., D. Pravtcheva, M.S. Newman, L.W. Hunihan, Z. Jiang, and F.H. Ruddle. 1989. Isolation and regional localization of the murine homeobox-containing gene Hox-3.3 to mouse chromosome region 15E. Genomics 5: 76-83.
71. St. Johnston, D. and W.M. Gelbart. 1987. Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 6: 2785-2791.
72. Strathern, J.N. and D.R. Higgins. 1991. Recovery of plasmids from yeast into Escherichia coli: Shuttle vectors. In Guide to yeast genetics and molecular biology (ed. C. Guthrie and G.R. Fink), pp. 319-328. Academic Press, San Diego, CA.
73. Stroeher, V.L., E.M. Jorgensen, and R.L. Garber. 1986. Multiple transcripts from the Antennapedia gene of Drosophila melanogaster. Mol. Cell. Biol. 6: 4667-4675.
74. Sturtevant, M.A., M. Roark, and E. Bier. 1993. The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes & Dev. 7: 961-973.
75. Sunkel, C.E. and J.R.S. Whittle. 1987. Brista: A gene involved in the specification and differentiation of distal cephalic and thoracic structures in Drosophila melanogaster. Wilhelm Roux's Arch. Dev. Biol. 196: 124-132.
76. Taylor, S.S. and E. Radzio-Andzelm. 1994. Three protein kinase structures define a common motif. Structure 2: 345-355.
77. Treisman, J., P. Gonczy, M. Vashishtha, E. Harris, and C. Desplan. 1989. A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59: 553-562.
78. Vachon, G., B. Cohen, C. Pfeifle, M.E. McGuffin, J. Botas, and S. Cohen. 1992. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell 71: 437-450.
79. Wedden, S.E., K. Pang, and G. Eichele. 1989. Expression pattern of homeobox-containing genes during chick embryogenesis. Development 105: 639-650.
80. White, R.A.H. and M. Wilcox. 1985. Distribution of Ultrabithorax proteins in Drosophila. EMBO J. 4: 2035-2043.
81. Wieschaus, E. and C. Nüsslein-Volhard. 1986. Looking at embryos. In Drosophila, A practical approach (ed. D.B. Roberts), pp. 199-228. IRL Press Limited, Oxford, UK.
82. Wright, C.V., K.W. Cho, A. Fritz, T.R. Burglin, and R.E. De. 1987. A Xenopus laevis gene encodes both homeobox-containing and homeobox-less transcripts. EMBO J. 6: 4083-4094.
83. Zak, N.B. and B.Z. Shilo. 1992. Localization of DER and the pattern of cell divisions in wild-type and Ellipse eye imaginal discs. Dev. Biol. 149: 448-456.
84. Zeng, W., D.J. Andrew, L.D. Mathies, M.A. Horner, and M.P. Scott. 1993. Ectopic expression and function of the Antp and Scr homeotic genes: The N terminus of the homeodomain is critical to functional specificity. Development 118: 339-352.