Mastermind mutations generate a unique constellation of midline cells within the drosophila CNS

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Zhang, Yi ^a,b   Wheatley, Randi ^a   Fulkerson, Eric ^a   Tapp, Amanda ^a   Estes, Patricia A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; DROSOPHILA PROTEIN; MASTERMIND PROTEIN, DROSOPHILA; NUCLEAR PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE MUTATION; GLIA; MASTERMIND GENE; MUTANT; NERVE CELL; NONHUMAN; SIGNAL TRANSDUCTION; WILD TYPE; ZYGOTE; ANIMAL; CELL LINEAGE; CYTOLOGY; DROSOPHILA; GENETICS; MUTATION; PHYSIOLOGY; PRENATAL DEVELOPMENT;

METAZOA;

ANIMALS; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYONIC DEVELOPMENT; MUTATION; NUCLEAR PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 80055056057     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026197     Document Type: Article

References (71)

1. Doe CQ, Skeath JB, (1996) Neurogenesis in the insect central nervous system. Current Opinion in Neurobiology 6: 18-24.
2. Guillemot F, (2007) Spatial and temporal specification of neural fates by transcription factor codes. Development 134: 3771-3780.
3. Thor S, Thomas JB, (2002) Motor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms. Current Opinion in Genetics & Development 12: 558-564.
4. Radtke F, Schweisguth F, Pear W, (2005) The Notch 'gospel'. Workshop on Notch signalling in development and cancer. Embo Reports 6: 1120-1125.
5. Skeath JB, Thor S, (2003) Genetic control of Drosophila nerve cord development. Current Opinion in Neurobiology 13: 8-15.
6. Wheeler SR, Stagg SB, Crews ST, (2008) Multiple Notch signaling events control Drosophila CNS midline neurogenesis, gliogenesis and neuronal identity. Development 135: 3071-3079.
7. Bray SJ, (2006) Notch signalling: a simple pathway becomes complex. Nature Reviews Molecular Cell Biology 7: 678-689.
8. Lai EC, (2004) Notch signaling: control of cell communication and cell fate. Development 131: 965-973.
9. Woodhoo A, Alonso MBD, Droggiti A, Turmaine M, D'Antonio M, et al. (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nature Neuroscience 12: 839-846.
10. Tamura K, Taniguchi Y, Minoguchi S, Sakai T, Tun T, et al. (1995) Physical interaction between a novel domain of the receptor Notch and the transcription factor RBP-J kappa/Su(H). Current Biology 5: 1416-1423.
11. Nam Y, Sliz P, Song LY, Aster JC, Blacklow SC, (2006) Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell 124: 973-983.
12. Petcherski AG, Kimble J, (2000) LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature 405: 364-368.
13. Wilson JJ, Kovall RA, (2006) Crystal structure of the CSL-Notch-Mastermind ternary complex bound to DNA. Cell 124: 985-996.
14. Wu LZ, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, et al. (2000) MAML1, a human homologue of Drosophila Mastermind, is a transcriptional co-activator for NOTCH receptors. Nature Genetics 26: 484-489.
15. Dickson BJ, (2002) Molecular mechanisms of axon guidance. Science 298: 1959-1964.
16. Araujo SJ, Tear G, (2003) Axon guidance mechanisms and molecules: Lessons from invertebrates. Nature Reviews Neuroscience 4: 910-922.
17. Crews ST, (1998) Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes & Development 12: 607-620.
18. Jacobs JR, (2000) The Midline Glia of Drosophila: a molecular genetic model for the developmental functions of Glia. Progress in Neurobiology 62: 475-508.
19. Klambt C, Jacobs JR, Goodman CS, (1991) The midline of the Drosophila central-nervous-system: a model for the genetic-analysis of cell fate, cell-migration, and growth cone guidance. Cell 64: 801-815.
20. Crews S, Thomas J, Goodman C, (1988) The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 15: 143-151.
21. Crews S, Franks R, Hu S, Matthews B, Nambu J, (1992) Drosophila single-minded gene and the molecular genetics of CNS midline development. Journal of Experimental Zoology 261: 234-244.
22. Nambu JR, Lewis JO, Wharton KA, Crews ST, (1991) The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67: 1157-1167.
23. Nambu JR, Franks RG, Hu S, Crews ST, (1990) The single-minded gene of Drosophila is required for the expression of genes important for the development of CNS midline cells. Cell 63: 63-75.
24. Kasai Y, Nambu JR, Lieberman PM, Crews ST, (1992) Dorsal ventral patterning in Drosophila: DNA-binding of snail protein to the single-minded gene. Proceedings of the National Academy of Sciences of the United States of America 89: 3414-3418.
25. Kasai Y, Stahl S, Crews S, (1998) Specification of the Drosophila CNS midline cell lineage: direct control of single-minded transcription by dorsal/ventral patterning genes. Gene Expr 7: 171-189.
26. Morel V, Schweisguth F, (2000) Repression by Suppressor of Hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes & Development 14: 377-388.
27. Bossing T, Brand AH, (2006) Determination of cell fate along the anteroposterior axis of the Drosophila ventral midline. Development 133: 1001-1012.
28. Bossing T, Technau GM, (1994) The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single-cell labeling. Development 120: 1895-1906.
29. Kearney JB, Wheeler SR, Estes P, Parente B, Crews ST, (2004) Gene expression profiling of the developing Drosophila CNS midline cells. Developmental Biology 275: 473-492.
30. Dong R, Jacobs JR, (1997) Origin and differentiation of supernumerary midline glia in Drosophila embryos deficient for apoptosis. Developmental Biology 190: 165-177.
31. Wheeler SR, Kearney JB, Guardiola AR, Crews ST, (2006) Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells. Developmental Biology 294: 509-524.
32. Smoller D, Friedel C, Schmid A, Bettler D, Lam L, et al. (1990) The Drosophila neurogenic locus mastermind encodes a nuclear protein unusually rich in amino acid homopolymers. Genes & Development 4: 1688-1700.
33. Xu T, Rebay I, Fleming RJ, Scottgale TN, Artavanis-Tsakonas S, (1990) The Notch locus and the genetic circuitry involved in early Drosophila neurogenesis. Genes & Development 4: 464-475.
34. Yedvobnick B, Smoller D, Young P, Mills D, (1988) Molecular analysis of the neurogenic locus mastermind of Drosophila melanogaster. Genetics 118: 483-497.
35. Petcherski AG, Kimble J, (2000) Mastermind is a putative activator for Notch. Current Biology 10: R471-473.
36. Fryer CJLE, Turbachova I, Kintner C, Jones KA, (2002) Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev 16: 1397-1411.
37. Fryer CJ, White JB, Jones KA, (2004) Mastermind recruits CycC: CDK8 to phosphorylate the notch ICD and coordinate activation with turnover. Molecular Cell 16: 509-520.
38. Nam Y, Weng AP, Aster JC, Blacklow SC, (2003) Structural requirements for assembly of the CSL.Intracellular Notch1.Mastermind-like 1 transcriptional activation complex. Journal of Biological Chemistry 278: 21232-21239.
39. Wallberg AE, Pedersen K, Lendahl U, Roeder RG, (2002) p300 and PCA act cooperatively to mediate transcriptional activation from chromatin templates by Notch intracellular domains in vitro. Molecular and Cellular Biology 22: 7812-7819.
40. Schuldt A, Brand A, (1999) Mastermind acts downstream of notch to specify neuronal cell fates in the Drosophila central nervous system. Developmental Biology 205: 287-295.
41. Yedvobnick B, Kumar A, Chaudhury P, Opraseuth J, Mortimer N, et al. (2004) Differential effects of Drosophila mastermind on asymmetric cell fate specification and neuroblast formation. Genetics 166: 1281-1289.
42. Jimenez F, Campos-Ortega JA, (1982) Maternal effects of zygotic mutants affecting early neurogenesis in Drosophila. Wilhelm Rouxs Archives of Developmental Biology 191: 191-201.
43. Watson JD, Wheeler SR, Stagg SB, Crews ST, (2011) Drosophila hedgehog signaling and engrailed-runt mutual repression direct midline glia to alternative ensheathing and non-ensheathing fates. Development 138: 1285-1295.
44. Bergmann A, Tugentman M, Shilo BZ, Steller H, (2002) Regulation of cell number by MAPK-dependent control of apoptosis: A mechanism for trophic survival signaling. Developmental Cell 2: 159-170.
45. Stemerdink C, Jacobs JR, (1997) Argos and Spitz group genes function to regulate midline glial cell number in Drosophila embryos. Development 124: 3787-3796.
46. Noordermeer JN, Kopczynski CC, Fetter RD, Bland KS, Chen WY, et al. (1998) Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21: 991-1001.
47. Kovall RA, (2007) Structures of CSL, Notch and Mastermind proteins: piecing together an active transcription complex. Current Opinion in Structural Biology 17: 117-127.
48. Vied C, Kalderon D, (2009) Hedgehog-stimulated stem cells depend on non-canonical activity of the Notch co-activator Mastermind. Development 136: 2177-2186.
49. Kolev V, Mandinova A, Guinea-Viniegra J, Hu B, Lefort K, et al. (2008) EGFR signalling as a negative regulator of Notch1 gene transcription and function in proliferating keratinocytes and cancer. Nature Cell Biology 10: 902-911.
50. Hasson P, Egoz N, Winkler C, Volohonsky G, Jia ST, et al. (2005) EGFR signaling attenuates Groucho-dependent repression to antagonize Notch transcriptional output. Nature Genetics 37: 101-105.
51. Price JV, Savenye ED, Lum D, Breitkreutz A, (1997) Dominant enhancers of Egfr in Drosophila melanogaster: Genetic links between the Notch and Egfr signaling pathways. Genetics 147: 1139-1153.
52. Estes P, Fulkerson E, Zhang Y, (2008) Identification of motifs that are conserved in 12 Drosophila species and regulate midline glia vs. neuron expression. Genetics 178: 787-799.
53. Kidd S, Lieber T, Young MW, (1998) Ligand-induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes & Development 12: 3728-3740.
54. Chou TB, Noll E, Perrimon N, (1993) Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germline chimeras. Development 119: 1359-1369.
55. Hartley DA, Xu T, Artavanis-Tsakonas S, (1987) The embryonic expression of the Notch locus of Drosophila melanogaster and the implications of point mutations in the extracellular EGF-like domain of the predicted protein. Embo Journal 6: 3407-3417.
56. Menne TV, Klambt C, (1994) The formation of commissures in the Drosophila CNS depends on the midline cells and on the Notch gene. Development 120: 123-133.
57. Martin-Bermudo MD, Carmena A, Jimenez F, (1995) Neurogenic genes control gene-expression at the transcriptional level in early neurogenesis and in mesectoderm specification. Development 121: 219-224.
58. Stagg S, Guardiola A, Crews S, (2011) Dual role for Drosophila lethal of scute in CNS midline precursor formation and dopaminergic neuron and motoneuron cell fate. Development 138: 2171-2183.
59. Shen H, McElhinny AS, Cao Y, Gao P, Liu J, et al. (2006) The Notch Coactivator, MAML1, functions as a novel coactivator for MEF2C-mediated transcription and is required for normal myogenesis. Genes & Development 20: 675-688.
60. Alves-Guerra MC, Ronchini C, Capobianco AJ, (2007) Mastermind-like 1 is a specific coactivator of beta-catenin transcription activation and is essential for colon carcinoma cell survival. Cancer Research 67: 8690-8698.
61. Moellering RE, Cornejo M, Davis TN, Del Bianco C, Aster JC, et al. (2009) Direct inhibition of the NOTCH transcription factor complex. Nature 462: 182-188.
62. Yedvobnick B, Moberg K, (2010) Linking model systems to cancer therapeutics: the case of Mastermind. Disease Models & Mechanisms 3: 540-544.
63. Lindsley DLZG, eds. (1992) The genome of Drosophila melanogaster Academic Press.
64. Shepard SB, Broverman SA, Muskavitch MAT, (1989) A tripartite interaction among alleles of Notch, Delta, and Enhancer of Split during imaginal development of Drosophila melanogaster. Genetics 122: 429-438.
65. Xiao H, Hrdlicka LA, Nambu JR, (1996) Alternate functions of the single-minded and rhomboid genes in development of the Drosophila ventral neuroectoderm. Mechanisms of Development 58: 65-74.
66. Giraldez AJ, Perez L, Cohen SM, (2002) A naturally occuring alternative product of the mastermind locus that represses Notch signalling. Mechanisms of Development 115: 101-105.
67. Schweitzer R, Shilo BZ, (1997) A thousand and one roles for the Drosophila EGF receptor. Trends in Genetics 13: 191-196.
68. Patel NH, Snow PM, Goodman CS, (1987) Characterization and cloning of fasciclin-III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48: 975-988.
69. Ward M, Mosher J, Crews S, (1998) Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125: 1599-1608.
70. Neckameyer WS, Woodrome S, Holt B, Mayer A, (2000) Dopamine and senescence in Drosophila melanogaster. Neurobiology of Aging 21: 145-152.
71. JC R, V C, (1998) Evidence for a novel Notch pathway required for muscle precursor selection in Drosophila. Mechanisms of Development 79: 39-50.