The levels of the bancal product, a Drosophila homologue of vertebrate hnRNP K protein, affect cell proliferation and apoptosis in imaginal disc cells

Molecular and Cellular Biology

Volumn 19, Issue 11, 1999, Pages 7846-7856

  Charroux, Bernard ^a,b   Angelats, Corinne ^a   Fasano, Laurent ^a   Kerridge, Stephen ^a   Vola, Christine ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; ARTICLE; CELL PROLIFERATION; DROSOPHILA; GENE SEQUENCE; GROWTH REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY;

DROSOPHILA; VERTEBRATA;

EID: 0032744689     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.11.7846     Document Type: Article

References (90)

1. Alexandre, E., Y. Graba, L. Fasano, A. Gallet, L. Perrin, P. De Zulueta, J. Pradel, S. Kerridge, and B. Jacq. 1996. The Drosophila Teashirt homeotic protein is a DNA-binding protein and modulo, a HOM C regulated modifier of variegation, is a likely candidate for being a direct target gene. Mech. Dev. 59:191-204.
2. Amrein, H., M. Gorman, and R. Nothiger. 1988. The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55:1025-1035.
3. Baker, N. E., and G. M. Rubin. 1992. Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginai discs. Dev. Biol. 150:381-396.
4. Bell, L. R., E. M. Maine, P. Schedl, and T. W. Cline. 1988. Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell 55:1037-1046.
5. Bellen, H. J., S. Kooyer, D. D'Evelyn, and J. Pearlman. 1992. The Drosophila couch potato protein is expressed in nuclei of peripheral neuronal precursors and shows homology to RNA-binding proteins. Genes Dev. 6:2125-2136.
6. Bier, E., H. Vaessin, S. Shepherd, K. Lee, K. McCall, S. Barbel, L. Ackerman, R. Carretto, T. Uemura, E. Grell, et al. 1989. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3: 1273-1287.
7. Brand, A. H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. Buchenau, P., H. Saumweber, and D. J. Arndt-Jovin. 1997. The dynamic nuclear redistribution of an hnRNP K-homologous protein during Drosophila embryo development and heat shock. Flexibility of transcription sites in vivo. J. Cell Biol. 137:291-303.
9. Bump, N. J., M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, et al. 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-1888.
10. Caceres, J. F., S. Stamm, D. M. Helfman, and A. R. Krainer. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706-1709.
11. Choi, Y. D., P. J. Grabowski, P. A. Sharp, and G. Dreyfuss. 1986. Heterogeneous nuclear ribonucleoproteins: role in RNA splicing. Science 231: 1534-1539.
12. Dejgaard, K., and H. Leffers. 1996. Characterisation of the nucleic-acid-binding activity of KH domains. Different properties of different domains. Eur. J. Biochem. 241:425-431.
13. Dejgaard, K., H. Leffers, H. H. Rasmussen, P. Madsen, T. A. Kruse, B. Gesser, H. Nielsen, and J. E. Celis. 1994. Identification, molecular cloning, expression and chromosome mapping of a family of transformation upregulated hnRNP-K proteins derived by alternative splicing. J. Mol. Biol. 236: 33-48.
14. Denisenko, O. N., B. O'Neill, J. Ostrowski, I. Van Seuningen, and K. Bomsztyk. 1996. Zik1, a transcriptional represser that interacts with the heterogeneous nuclear ribonucleoprotein particle K protein. J. Biol. Chem. 271:27701-27706.
15. Dequin, R., H. Saumweber, and J. W. Sedat. 1984. Proteins shifting from the cytoplasm into the nuclei during early embryogenesis of Drosophila melanogaster. Dev. Biol. 104:37-48.
16. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
17. Edgar, B. A., and C. F. Lehner. 1996. Developmental control of cell cycle regulators: a fly's perspective. Science 274:1646-1652.
18. Fly base. 1993-1997, copyright date. [Online.] The Drosophila genetic database. Genetics Society of America. http://flybase.bio.indiana.edu. [7 May 1999, last date accessed.]
19. Foe, V. E., and B. M. Alberts. 1983. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61:31-70.
20. Foe, V. E. 1989. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1-22.
21. Fumagalli, S., N. F. Totty, J. J. Hsuan, and S. A. Courtneidge. 1994. A target for Src in mitosis. Nature 368:871-874.
22. Gaillard, C., E. Cabannes, and F. Strauss. 1994. Identity of the RNA-binding protein K of hnRNP particles with protein H16, a sequence-specific single strand DNA-binding protein. Nucleic Acids Res. 22:4183-4186.
23. Gallet, A., A. Erkner, B. Charroux, L. Fasano, and S. Kerridge. 1998. Trunk-specific modulation of Wingless signalling in Drosophila by Teashirt binding to Armadillo. Curr. Biol. 8:893-902.
24. Goralski, T. J., J. E. Edstrom, and B. S. Baker. 1989. The sex determination locus transformer-2 of Drosophila encodes a polypeptide with similarity to RNA binding proteins. Cell 56:1011-1018.
25. Hammond, L. E., D. Z. Rudner, R. Kanaar, and D. C. Rio. 1997. Mutations in the hrp48 gene, which encodes a Drosophila heterogeneous nuclear ribonucleoprotein particle protein, cause lethality and developmental defects and affect P-element third-intron splicing in vivo. Mol. Cell. Biol. 17:7260-7267.
26. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
27. Hay, B. A., T. Wolff, and G. M. Rubin. 1994. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120:2121-2129.
28. Hay, B. A., D. A. Wassarman, and G. M. Rubin. 1995. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83:1253-1262.
29. Hepker, J., Q. T. Wang, C. K. Motzny, R. Holmgren, and T. V. Orenic. 1997. Drosophila Cubitus Interruptus forms a negative feedback loop with Patched and regulates expression of Hedgehog target genes. Development 124:549-558.
30. Ito, K., K. Sato, and H. Endo. 1994. Cloning and characterization of a single-stranded DNA binding protein that specifically recognizes deoxycytidine stretch. Nucleic Acids Res. 22:53-58.
31. Johnston, L. A., and G. Schubiger. 1996. Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination. Development 122:3519-3529.
32. Kamma, H., D. S. Portman, and G. Dreyfuss. 1995. Cell type-specific expression of hnRNP proteins. Exp. Cell Res. 221:187-196.
33. Karsch-Mizrachi, I., and S. R. Haynes. 1993. The Rb97D gene encodes a potential RNA-binding protein required for spermatogenesis in Drosophila. Nucleic Acids Res. 21:2229-2235.
34. Kelley, R. L. 1993. Initial organization of the Drosophila dorsoventral axis depends on an RNA-binding protein encoded by the squid gene. Genes Dev. 7:948-960.
35. Kerridge, S. Unpublished data.
36. Kiledjian, M., and G. Dreyfuss. 1992. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 11: 2655-2664.
37. Kimmel, B. E., U. Heberlein, and G. M. Rubin. 1990. The homeo domain protein Rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev. 4:712-727.
38. Krejci, E., V. Garzino, C. Mary, N. Bennani, and J. Pradel. 1989. Modulo, a new maternally expressed Drosophila gene encodes a DNA-binding protein with distinct acidic and basic regions. Nucleic Acids Res. 17:8101-8115.
39. Lambertsson, A. 1998. The minute genes in Drosophila and their molecular functions. Adv. Genet. 38:69-134.
40. Lee, M. H., S. Mori, and P. Raychandhuri. 1996. Trans-activation by the hnRNP K protein involves an increase in RNA synthesis from the reporter genes. J. Biol. Chem. 271:3420-3427.
41. Madhavan, M., and H. A. Schneiderman. 1977. Histological analysis of the dynamics of growth of imaginai discs and histoblast nests during the larval development of Drosophila melanogaster. Roux's Arch. Dev. Biol. 183:269.
42. Mahone, M., E. E. Saffman, and P. F. Lasko. 1995. Localized Bicaudal-C RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J. 14:2043-2055.
43. Marrus, S. B., H. Zeng, and M. Rosbash. 1996. Effect of constant light and arcadian entrainment of perS flies: evidence for light-mediated delay of the negative feedback loop in Drosophila. EMBO J. 15:6877-6886.
44. Mattox, W., M. E. McGuffin, and B. S. Baker. 1996. A negative feedback mechanism revealed by functional analysis of the alternative isoforms of the Drosophila splicing regulator Transformer-2. Genetics 143:303-314.
45. Matunis, E. L., M. J. Matunis, and G. Dreyfuss. 1992. Characterization of the major hnRNP proteins from Drosophila melanogaster. J. Cell Biol. 116: 257-269.
46. Matunis, E. L., M. J. Matunis, and G. Dreyfuss. 1993. Association of individual hnRNP proteins and snRNPs with nascent transcripts. J. Cell Biol. 121:219-228.
47. Matunis, M. J., E. L. Matunis, and G. Dreyfuss. 1992. Isolation of hnRNP complexes from Drosophila melanogaster. J. Cell Biol. 116:245-255.
48. Matunis, M. J., W. M. Michael, and G. Dreyfuss. 1992. Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol. Cell. Biol. 12:164-171.
49. Mayeda, A., S. H. Munroe, J. F. Caceres, and A. R. Krainer. 1994. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 13:5483-5495.
50. Miau, L. H., C. J. Chang, B. J. Shen, W. H. Tsai, and S. C. Lee. 1998. Identification of heterogeneous nuclear ribonucleoprotein K (hnRNP K) as a represser of C/EBPbeta-mediated gene activation. J. Biol. Chem. 273: 10784-10791.
51. Michael, W. M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83:415-422.
52. Michael, W. M., P. S. Eder, and G Dreyfuss. 1997. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J. 16:3587-3598.
53. Michelotti, E. F., G. A. Michelotti, A. I. Aronsohn, and D. Levens. 1996. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 16:2350-2360.
54. Michelotti, E. F., T. Tomonaga, H. Krutzsch, and D. Levens. 1995. Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene. J. Biol. Chem. 270:9494-9499.
55. Moses, K., M. C. Ellis, and G. M. Rubin. 1989. The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340: 531-536.
56. Musco, G., G. Stier, C. Joseph, M. A. Castiglione Morelli, M. Nilges, T. J. Gibson, and A. Pastore. 1996. Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell 85:237-245.
57. Nandabalan, K., L. Price, and G. S. Roeder. 1993. Mutations in U1 snRNA bypass the requirement for a cell type-specific RNA splicing factor. Cell 73: 407-415.
58. Ostrowski, J., I. Van Seuningen, R. Seger, C. T. Rauch, P. R. Sleath, B. A. McMullen, and K. Bomsztyk. 1994. Purification, cloning, and expression of a murine phosphoprotein that binds the kappa B motif in vitro identifies it as the homolog of the human heterogeneous nuclear ribonucleoprotein K protein. Description of a novel DNA-dependent phosphorylation process. J. Biol. Chem. 269:17626-17634.
59. Peifer, M., and E. Wieschaus. 1990. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63:1167-1176.
60. Pinol-Roma, S., Y. D. Choi, M. J. Matunis, and G. Dreyfuss. 1988. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev. 2:215-227.
61. Pinol-Roma, S., and G. Dreyfuss. 1991. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science 253: 312-314.
62. Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
63. Pirrotta, V. 1988. Vectors for P-mediated transformation in Drosophila. Bio/Technology 10:437-456.
64. Pollard, V. W., W. M. Michael, S. Nakielny, M. C. Siomi, F. Wang, and G. Dreyfuss. 1996. A novel receptor-mediated nuclear protein import pathway. Cell 86:985-994.
65. Regnier, P., M. Grunberg-Manago, and C. Portier. 1987. Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. Homology of the primary structure of the protein with the RNA-binding domain of ribosomal protein S1. J. Biol. Chem. 262:63-68.
66. Robertson, H. M., C. R. Preston, R. W. Phillis, D. M. Johnson-Schlitz, W. K. Benz, and W. R. Engels. 1988. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461-470.
67. Roth, S., and T. Schupbach. 1994. The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120:2245-2257.
68. Rubin, G. M., and A. C. Spradling. 1982. Genetic transformation of Drosophila with transposable element vectors. Science 218:348-353.
69. 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.
70. Segalat, L., and J. A. Lepesant. 1992. Spatial distribution of the Sm antigen in Drosophila early embryos. Biol. Cell 75:181-185.
71. Shen, J., K. Zu, C. L. Cass, A. L. Beyer, and J. Hirsh. 1995. Exon skipping by overexpression of a Drosophila heterogeneous nuclear ribonucleoprotein in vivo. Proc. Nati. Acad. Sci. USA 92:1822-1825.
72. Siebel, C. W., R. Kanaar, and D. C. Rio. 1994. Regulation of tissue-specific P-element pre-mRNA splicing requires the RNA-binding protein PSI. Genes Dev. 8:1713-1725.
73. Singh, R., J. Valcarcel, and M. R. Green. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268:1173-1176.
74. Siomi, H., M. J. Matunis, W. M. Michael, and G. Dreyfuss. 1993. The pre-mRNA binding K protein contains a novel evolutionarily conserved motif. Nucleic Acids Res. 21:1193-1198.
75. Siomi, H., M. C. Siomi, R. L. Nussbaum, and G. Dreyfuss. 1993. The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74:291-298.
76. Siomi, H., M. Choi, M. C. Siomi, R. L. Nussbaum, and G. Dreyfuss. 1994. Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell 77:33-39.
77. Siomi, M. C., M. Fromont, J. C. Rain, L. Wan, F. Wang, P. Legrain, and G. Dreyfuss. 1998. Functional conservation of the transportin nuclear import pathway in divergent organisms. Mol. Cell. Biol. 18:4141-4148.
78. Spreij, T. E. 1971. Cell death during the development of imaginal discs of Calliphora erythrocephala. Neth. J. Zool. 21:221-264.
79. Swanson, M. S., and G. Dreyfuss. 1988. Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol. Cell. Biol. 8:2237-2241.
80. Takimoto, M., T. Tomonaga, M. Matunis, M. Avigan, H. Krutzsch, G. Dreyfuss, and D. Levens. 1993. Specific binding of heterogeneous ribonucleoprotein particle protein K to the human c-myc promoter, in vitro. J. Biol. Chem. 168:18249-18258.
81. Taylor, S. J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368:867-871.
82. Thummel, C. S., A. M. Boulet, and H. D. Lipshitz. 1988. Vectors for Drosophita P-element-mediated transformation and tissue culture transfection. Gene 74:445-456.
83. Tomonaga, T., and D. Levens. 1995. Heterogeneous nuclear ribonucleoprotein K is a DNA-binding transactivator. J. Biol. Chem. 270:4875-4881.
84. Usui, K., and K. I. Kimura. 1992. Sensory mother cells are selected from among mitotically quiescent cluster of cells in the wing disc of Drosophila. Development 116:601-610.
85. Van Seuningen, I., J. Ostrowski, X. R. Bustelo, P. R. Sleath, and K. Bomsztyk. 1995. The K protein domain that recruits the interleukin 1-responsive K protein kinase lies adjacent to a cluster of c-Src and Vav SH3-binding sites. Implications that K protein acts as a docking platform. J. Biol. Chem. 270:26976-26985.
86. Weng, Z., S. M. Thomas, R. J. Rickles, J. A. Taylor, A. W. Brauer, C. Seidel-Dugan, W. M. Michael, G. Dreyfuss, and J. S. Brugge. 1994. Identification of Src, Fyn, and Lyn SH3-binding proteins: implications for a function of SH3 domains. Mol. Cell. Biol. 14:4509-4521.
87. White, K., M. E. Grether, J. M. Abrams, L. Young, K. Farrell, and H. Steller. 1994. Genetic control of programmed cell death in Drosophila. Science 264: 677-683.
88. Yang, X., M. R. Bani, S. J. Lu, S. Rowan, Y. Ben-David, and B. Chabot. 1994. The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proc. Natl. Acad. Sci. USA 91: 6924-6928.
89. Zahler, A. M., K. M. Neugebauer, W. S. Lane, and M. B. Roth. 1993. Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260: 219-222.
90. Zu, K., M. L. Sikes, S. R. Haynes, and A. L. Beyer. 1996. Altered levels of the Drosophila HRB87F/hrp36 hnRNP protein have limited effects on alternative splicing in vivo. Mol. Biol. Cell. 7:1059-1073.