Evidence that the C-terminal domain (CtD) autoinhibits neural repression by Drosophila E(spl)M8

Genesis

Volumn 48, Issue 1, 2010, Pages 44-55

  Kahali, Bhaskar ^a   Kim, Jee Eun ^a   Karandikar, Umesh ^a   Bishop, Clifton P ^a   Bidwai, Ashok P ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

E(spl)D; Lateral inhibition; Nspl; Neurogenesis; Notch

Indexed keywords

ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DEVELOPMENTAL GENE; DROSOPHILA; ECTOPIC TISSUE; EYE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; MOLECULAR MODEL; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CASEIN KINASE II; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; FEMALE; HELIX-LOOP-HELIX MOTIFS; MALE; MOLECULAR SEQUENCE DATA; MUTATION; NERVOUS SYSTEM; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; REPRESSOR PROTEINS; SENSE ORGANS; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 74749101106     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20581     Document Type: Article

References (63)

1. Alifragis P, Poortinga G, Parkhurst SM, Delidakis C. 1997. A network of interacting transcriptional regulators involved in Drosophila neural fate specification revealed by the yeast two-hybrid system. Proc Natl Acad Sci USA 94:13099-13104.
2. Bailey AM, Posakony JW. 1995. Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9:2609-2622.
3. Baonza A, Freeman M. 2001. Notch signalling and the initiation of neural development in the Drosophila eye. Development 128:3889-3898.
4. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS. 2002. Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev 16:2415-2427.
5. Bidwai AP, Reed JC, Glover CVC. 1993. The phosphorylation of Calmodulin by the catalytic subunit of casein kinase II is inhibited by the regulatory subunit. Arch Biochem Biophys 300:265-270.
6. Bose A, Kahali B, Zhang S, Lin J-M, Allada R, Karandikar U, Bidwai A. 2006. Drosophila CK2 regulates lateral-inhibition during eye and bristle development. Mech Dev 123:649-664.
7. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. Bray SJ. 2006. Notch signalling: A simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678-689.
9. Brennan K, Tateson R, Lewis K, Arias AM. 1997. A functional analysis of notch mutations in Drosophila. Genetics 147:177-188.
10. Calleja M, Renaud O, Usui K, Pistillo D, Morata G, Simpson P. 2002. How to pattern an epithelium: Lessons from achaete-scute regulation on the notum of Drosophila. Gene 292:1-12.
11. Campos-Ortega JA. 1997. Neurogenesis in Drosophila: A historical perspective and some prospects. Perspect Dev Neurobiol 4:267-271.
12. Collins MO. 2009. Cell biology. Evolving cell signals. Science 325: 1635-1636.
13. Cooper MTD, Tyler DM, Furriols M, Chalkiadaki A, Delidakis C, Bray SJ. 2000. Spatially restricted factors cooperate with notch in the regulation of enhancer of split genes. Dev Biol 221:390-403.
14. Cubas P, de Celis JF, Campuzano S, Modolell J. 1991. Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5:996-1008.
15. Dambly-Chaudiere C, Vervoort M. 1998. The bHLH genes in neural development. Int J Dev Biol 42:269-273.
16. Dawson SR, Turner DL, Weintraub H, Parkhurst SM. 1995. Specificity for the hairy/enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Mol Cell Biol 15:6923-6931.
17. Dunker AK, Silman I, Uversky VN, Sussman JL. 2008. Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18:756-764.
18. Fisher AL, Ohsako S, Caudy M. 1996. The WRPW motif of the hairy-related bHLH repressor proteins acts as a 4-amino acid transcriptional repression and protein-protein interaction domain. Mol Cell Biol 16:2670-2677.
19. Frankfort BJ, Mardon G. 2002. R8 development in the Drosophila eye: A paradigm for neural selection and differentiation. Development 129:1295-1306.
20. Gardner KH, Montminy M. 2005. Can you hear me now? Regulating transcriptional activators by phosphorylation. Sci STKE 2005:pe44.
21. Garza AS, Ahmad N, Kumar R. 2009. Role of intrinsically disordered protein regions/domains in transcriptional regulation. Life Sci 84:189-193.
22. Giagtzoglou N, Alifragis P, Koumbanakis KA, Delidakis C. 2003. Two modes of recruitment of E(spl) repressors onto target genes. Development 130:259-270.
23. Gibert JM, Simpson P. 2003. Evolution of cis-regulation of the proneural genes. Int J Dev Biol 47:643-651.
24. Giebel B, Campos-Ortega JA. 1997. Functional dissection of the Drosophila enhancer of split protein, a suppressor of neurogenesis. Proc Natl Acad Sci USA 94:6250-6254.
25. Gratton M-O, Torban E, Jasmin SB, Theriault FM, German MS, Stifani S. 2003. Hes6 promotes cortical neurogenesis and inhibits Hes1 transcription repression activity by multiple mechanisms. Mol Cell Biol 23:6922-6935.
26. Gyuris J, Golemis E, Chertkov H, Brent R. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with cdk2. Cell 75:791-803.
27. Heitzler P, Bourouis M, Ruel L, Carteret C, Simpson P. 1996. Genes of the enhancer of split and achaete-scute complexes are required for a regulatory loop between notch and delta during lateral signalling in Drosophila. Develop 122:161-171.
28. Hinz U, Giebel B, Campos-ortega JA. 1994. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76:77-87.
29. Hsiung F, Moses K. 2002. Retinal development in Drosophila: Specifying the first neuron. Hum Mol Genet 11:1207-1214.
30. Jarman AP, Grell EH, Ackerman L, Jan LY, Jan YN. 1994. Atonal is the proneural gene for Drosophila photoreceptors. Nature 369:398-400.
31. Jarman A, Sun Y, Jan L, Jan Y. 1995. Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121:2019-2030.
32. Kahali B, Trott R, Paroush Z, Allada R, Bishop CP, Bidwai AP. 2008. Drosophila CK2 phosphorylates Hairy and regulates its activity in vivo. Biochem Biophys Res Commun 373:637-642.
33. Kahali B, Bose A, Karandikar U, Bishop CP, Bidwai A. 2009. On the mechanism underlying the divergent retinal and bristle defects of M8* (E(spl)D) in Drosophila. Genesis 47:456-468.
34. Karandikar U, Trott RL, Yin J, Bishop CP, Bidwai AP. 2004. Drosophila CK2 regulates eye morphogenesis via phosphorylation of E(spl)M8. Mech Dev 121:273-286.
35. Karandikar U, Shaffer J, Bishop CP, Bidwai AP. 2005. Drosophila CK2 phosphorylates Deadpan, a member of the HES family of basic-helix-loop-helix (bHLH) repressors. Mol Cell Biochem 274:133-139.
36. Kuenzel EA, Krebs EG. 1985. A synthetic substrate specific for casein kinase II. Proc Natl Acad Sci USA 82:737-741.
37. Kunttas-Tatli E, Bose A, Kahali B, Bishop CP, Bidwai AP. 2009. Functional dissection of Timekeeper (Tik) implicates opposite roles for CK2 and PP2A during Drosophila neurogenesis. Genesis 47:647-658.
38. Lecourtois M, Schweisguth F. 1995. The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev 9:2598-2608.
39. Lee D, Redfern O, Orengo C. 2007. Predicting protein function from sequence and structure. Nat Rev Mol Cell Biol 8:995-1005.
40. Lehmann R, Jimenez F, Dietrich U, Campos-Ortega JA. 1983. On the phenotype and development of mutants of early development in Drosophila melanogaster. Roux's Arch Dev Biol 192:62-74.
41. Li Y, Lei L, Irvine KD, Baker NE. 2003. Notch activity in neural cells triggered by a mutant allele with altered glycosylation. Develop 130:2829-2840.
42. Ligoxygakis P, Yu SY, Delidakis C, Baker NE. 1998. A subset of Notch functions during Drosophila eye development require Su(H) and E(spl) gene complex. Development 125:2893-2900.
43. Ligoxygakis P, Bray SJ, Apidianakis Y, Delidakis C. 1999. Ectopic expression of individual E(spl) genes has differential effects on different cell fate decisions and underscores the biphasic requirement for notch activity in wing margin establishment in Drosophila. Development 126:2205-2214.
44. Modolell J, Campuzano S. 1998. The achaete-scute complex as an integrating device. Int J Dev Biol 42:275-282.
45. Nagel AC, Preiss A. 1999. Notch spl is deficient for inductive processes in the eye, and E(spl)D enhances split by interfering with proneural activity. Dev Biol 208:406-415.
46. Nagel A, Yu Y, Preiss A. 1999. Enhancer of Split [E(spl)D] is a Gro-independent, hypermorphic mutation in Drosophila. Dev Genet 25:168-179.
47. Nakao K, Campos-Ortega JA. 1996. Persistent expression of genes of the enhancer of split complex suppress neural development in Drosophila. Neuron 16:275-286.
48. Paroush Z, Finley RL, Kidd T, Wainwright SM, Ingham PW, Brent R, Ish-Horowcz D. 1994. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy related bHLH proteins. Cell 79:805-815.
49. Powell LM, Zur Lage PI, Prentice DR, Senthinathan B, Jarman AP. 2004. The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol Cell Biol 24:9517-9526.
50. Qin BY, Liu C, Lam SS, Srinath H, Delston R, Correia JJ, Derynck R, Lin K. 2003. Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation. Nat Struct Biol 10:913-921.
51. Schlessinger J. 2003. Autoinhibition control. Science 300:750-752.
52. Schrons H, Knust E, Campos-Ortega JA. 1992. The enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal cells. Genetics 132:481-503.
53. Shepard SB, Broverman SA, Muskavitch MA. 1989. A tripartite interaction among alleles of notch, delta, and enhancer of split during imaginal development of Drosophila melanogaster. Genetics 122:429-438.
54. Simpson P. 1990. Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. Development 109:509-519.
55. Skeath JB, Carroll SB. 1991. Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev 5:984-995.
56. Smock RG, Gierasch LM. 2009. Sending signals dynamically. Science 324:198-203.
57. Sun Y, Jan L, Jan Y. 1998. Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Develop 125:3731-3740.
58. Tietze K, Oellers N, Knust E. 1992. Enhancer of SplitD, a dominant mutation of Drosophila, and its use in the study of functional domains of a helix-loop-helix protein. Proc Natl Acad Sci USA 89:6152-6156.
59. Tokuriki N, Tawfik DS. 2009. Protein dynamism and evolvability. Science 324:203-207.
60. Tompa P. 2002. Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533.
61. Trott RL, Kalive M, Paroush Z, Bidwai AP. 2001. Drosophila melanogaster casein kinase II interacts with and phosphorylates the basic-helix-loop-helix (bHLH) proteins m5, m7, and m8 derived from the enhancer of split complex. J Biol Chem 276:2159-2167.
62. Welshons WJ. 1956. Analysis of a gene in Drosophila. Science 150:1122-1129.
63. Wolff T, Ready D. 1991. The beginning of pattern formation in the Drosophila compound eye: The morphogenetic furrow and the second mitotic wave. Development 113:841-850.