Importin-α3 is required at multiple stages of Drosophila development and has a role in the completion of oogenesis

Developmental Biology

Volumn 223, Issue 2, 2000, Pages 307-322

  Máthé, Endre ^a   Bates, Helen ^b   Huikeshoven, Hella ^b   Deák, Péter ^a   Glover, David M ^a   Cotterill, Sue ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Drosophila; Embryogenesis; Importin ; Karyopherin ; Nuclear transport; Oogenesis

Indexed keywords

KARYOPHERIN; ISOPROTEIN; NUCLEAR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BLASTODERM; CELL NUCLEUS; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; ANIMAL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL DIVISION; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; GENE; GENETICS; INSECT; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; MUTATION; PRENATAL DEVELOPMENT; PROTEIN BINDING; TRANSPORT AT THE CELLULAR LEVEL; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL DIFFERENTIATION; CELL DIVISION; DROSOPHILA MELANOGASTER; GENES, INSECT; KARYOPHERINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; OOGENESIS; PROTEIN BINDING; PROTEIN ISOFORMS; PUPA; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 0034660689     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2000.9743     Document Type: Article

References (51)

1. Adam E. J. H., Adam S. A. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 125:1994;547-555.
2. Bischoff F. R., Görlich D. RanBP1 is crucial for the release of RanGTP from importin-β related nuclear transport factors. FEBS Lett. 419:1997;249-254.
3. Bouvier D., Baldacci D. The N-terminus of fission yeast DNA polymerase alpha contains a basic pentapeptide that acts in vivo as a nuclear localisation signal. Mol. Biol. Cell. 6:1995;1697-1705.
4. Callaini G., Riparbelli M. G. Fertilization in Drosophila melanogaster: Centrosome inheritance and organization of the first mitotic spindle. Dev. Biol. 176:1996;199-208.
5. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 15:1987;1353-1361.
6. Chi N. C., Adam E. J. H., Visser G. D., Adam S. A. RanBP1 stabilises the interaction of Ran with p97 in nuclear protein import. J. Cell Biol. 135:1996;559-569.
7. Conti E., Uy M., Leighton L., Blobel G., Kuriyan J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell. 94:1998;193-204.
8. Deák P., Omar M. M., Saunders R. D. C., Pál M., Komonyi O., Szidonya J., Maróy P., Zhang Y., Ashburner M., Benos P., Savakis C., Siden-Kiamos I., Louis C., Bolshakov V., Kafatos F. C., Madueno E., Modelell J., Glover D. M. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: Correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics. 147:1997;1697-1722.
9. Dey J. K., Spradling A. The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis. Development. 126:1999;293-303.
10. Dingwall C., Laskey R. A. Nuclear import: A tale of two sites. Curr. Biol. 8:1998;922-924.
11. Erdélyi M., Máthé E., Szabad J. Genetic and developmental analysis of Ketel mutant alleles that identify the Drosophila importin-β homologue. Acta Biol. Hung. 48:1997;323-338.
12. Foe E. V., Odell G. M., Edgar B. A. Mitosis and morphogenesis in the Drosophila embryo: Point and counterpoint. Bate M., Martinez Arias A. The Development of Drosophila melanogaster. 1993;149-300 Cold Spring Harbor Laboratory Press, New York.
13. Görlich D., Kotska S., Kraft R., Dingwall C., Laskey R. A., Hartmann E., Prehn S. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 5:1995;383-392.
14. Görlich D., Henklein P., Laskey R. A., Hartmann E. A 41 amino acid motif in importin-α confers binding to importin-β and hence transit into the nucleus. EMBO J. 15:1996;1810-1817.
15. Görlich D. Nuclear protein import. Curr. Opin. Cell Biol. 9:1997;412-419.
16. Görlich D. Transport into and out of the cell nucleus. EMBO J. 17:1998;2721-2727.
17. Gyuris J., Golemis E., Chertkov H., Brent R. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell. 75:1993;791-803.
18. Herold A., Truant R., Wiegand H., Cullen B. R. Determination of the functional domain organisation of the importin α nuclear import factor. J. Cell Biol. 143:1998;309-318.
19. Huettner A. F. Maturation and fertilization in Drosophila melanogaster. J. Morphol. Physiol. 39:1924;249-265.
20. Izaurralde E., Kutay U., von Kobbe U., Mattaj I. W., Görlich D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 16:1997;6535-6547.
21. Kamei Y., Yuba S., Nakayama T., Yoneda Y. Three distinct classes of the alpha-subunit of the nuclear pore-targeting complex (importin-alpha) are differentially expressed in adult mouse tissues. J. Histochem. Cytochem. 47:1999;363-372.
22. Koepp D. M., Silver P. A. A GTPase controlling nuclear trafficking: Running the right way or walking randomly? Cell. 87:1996;1-4.
23. Kozak M. Adherence to the first-AUG rule when a second AUG codon follows closely upon the first. Proc. Natl. Acad. Sci. USA. 92:1995;7134.
24. Köhler M., Ansieau S., Prehn S., Leutz A., Haller H., Haller H., Hartmann E. Cloning of two novel human importin-α subunits and analysis of the expression pattern of the importin-α protein family. FEBS Lett. 417:1997;104-108.
25. Kussel P., Frasch M. Pendulin, a Drosophila protein with cell cycle-dependent nuclear localization, is required for normal cell proliferation. J. Cell Biol. 129:1995;1491-1507.
26. Kutay U., Bischoff F. R., Kostka S., Kraft R., Görlich D. Export of importin-α from the nucleus is mediated by a specific nuclear transport factor. Cell. 90:1997;1061-1071.
27. Lindsley D. L., Zimm G. G. The Genome of Drosophila melanogaster. 1992;Academic Press, San Diego/London.
28. Maldonado-Codina G., Glover D. M. Cyclin A and B associate with chromatin and the polar regions of spindles, respectively, and do not undergo a complete degradation at anaphase in syncytial Drosophila embryos. J. Cell Biol. 116:1992;967-976.
29. Máthé E., Boros I., Jósvay K., Kaijun L., Puro J., Kaufman T. C., Szabad J. The Tomaj mutant alleles of αTubulin67C reveal a requirement for the encoded maternal specific tubulin isoform in the sperm aster, the cleavage spindle apparatus and neurogenesis during embryonic development in Drosophila. J. Cell Sci. 111:1998;887-896.
30. Mattaj I. W., Engelmeier L. Nucleocytoplasmic transport: The soluble phase. Annu. Rev. Biochem. 67:1998;265-306.
31. Moroianu J., Blobel G., Radu A. Previously identified protein of uncertain function is karyopherin alpha and together with karyopherin beta docks import substrate at nuclear pore complexes. Proc. Natl. Acad. Sci. USA. 92:1995a;2008-2011.
32. Moroianu J., Hijikata M., Blobel G., Radu A. Mammalian karyopherin a1b and a2b heterodimers: a1 or a2 subunit binds nuclear localisation sequence and b subunit interacts with peptide repeat containing nucleoporins. Proc. Natl. Acad. Sci. USA. 92:1995b;6532-6536.
33. Nigg E. A. Nucleocytoplasmic transport: Signals, mechanisms and regulation. Nature. 386:1997;779-787.
34. Paddy M. R., Belmont A. S., Saumweber H., Agard D. A., Sedat J. Interphase nuclear envelope lamins form a discontinuous network that interacts with only a fraction of the chromatin in the nuclear periphery. Cell. 62:1990;89-106.
35. Peifer M., McCrea P. D., Green K. J., Wieschaus E., Gumbiner B. M. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol. 118:1992;681-691.
36. Peifer M., Wieshaus E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobulin. Cell. 63:1995;1167-1176.
37. Prieve M. G., Guttridge K. L., Munguia J. E., Waterman M. L. The nuclear localization signal of lymphoid enhancer factor-1 is recognized by two differentially expressed Srp1-nuclear localization sequence receptor proteins. J. Biol. Chem. 271:1996;7654-7658.
38. Rexach M., Blobel G. Protein import into nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell. 83:1995;683-692.
39. Riggleman B., Wieschaus E., Schedl P. Molecular analysis of the armadillo locus: Uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev. 3:1989;96-113.
40. Ruden D. M., Ma J., Li Y., Wood K., Ptashne M. Generating yeast transcriptional activators containing no yeast protein sequences. Nature. 350:1991;250-252.
41. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
42. Spradling A. C. Developmental genetics of oogenesis. Bate M., Martinez Arias A. The Development of Drosophila melanogaster. 1993;1-70 Cold Spring Harbor Laboratory Press, New York.
43. Stochaj U., Rother K. L. Nucleocytoplasmic trafficking of proteins: With or without ran? BioEssays. 21:1999;579-589.
44. Stutz F., Rosbash M. Nuclear RNA export. Genes Dev. 12:1998;3303-3319.
45. Sunkel C. E., Glover D. M. Polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J. Cell Sci. 89:1988;25-38.
46. Török I., Strand D., Schmitt G., Tick T., Török T., Kiss I., Mechler B. M. The overgrown hematopoietic organs-31 tumor suppressor gene of Drosophila encodes an Importin-like protein accumulating in the nucleus at the onset of mitosis. J. Cell Biol. 129:1995;1473-1489.
47. Tsuji L., Takumi T., Imamoto N., Yoneda Y. Identification of novel homologues of mouse importin-α, the α subunit of nuclear pore-targetting complex, and their tissue-specific expression. FEBS Lett. 416:1997;30-34.
48. Ullman K. S., Powers M. A., Forbes D. J. Nuclear export receptors: From importin to exportin. Cell. 90:1997;967-970.
49. Weis K., Ryder U., Lamond A. I. The conserved amino terminal domain of hSRP1α is essential for nuclear protein import. EMBO J. 15:1996;1818-1825.
50. Yasuda G. K., Baker J., Schubinger G. Temporal regulation of gene expression in the blastoderm Drosophila embryo. Gen. Dev. 5:1991;1800-1812.
51. Zervos A. S., Gyuris J., Brent R. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell. 72:1993;223-232.