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Dm nxf1/sbr gene affects the formation of meiotic spindle in female Drosophila melanogaster

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Abstract

The small bristles (sbr) gene of Drosophila melanogaster belongs to the family of nuclear export factor (NXF) genes that participate in mRNA nuclear export. During meiosis, females of Drosophila melanogaster that carry various combinations of mutant alleles of the Dm nxf1/sbr gene exhibit disruption of the division spindle and misalignment of chromosomes at the metaphase plate. Meiosis of sbr 5 /+ females is characterized by the formation of tripolar spindles during the first cell division. According to the sequencing results, the sbr 5 (l(1)K4) lethal allele is a deletion of 492 nucleotides. In SBR5 protein, 57 of the 146 amino acids that have been lost by deletion belong to the NTF2-like domain.

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Abbreviations

NPC:

nuclear pore complex

NTF2:

nuclear transport factor 2

NXF:

nuclear export factor

RBD:

RNA-binding domain

sbr :

small bristles gene

UBA:

ubiquitin-associated

References

  • Ashburner M, Golic K, Hawley S (2005) Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Babu JR, Jeganathan KB, Baker DJ, Wu X, Kang-Decker N, van Deursen JM (2003) Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J Cell Biol 160:341–353

    Article  CAS  PubMed  Google Scholar 

  • Bachi A, Braun IC, Rodrigues JP et al (2000) The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6:136–158

    Article  CAS  PubMed  Google Scholar 

  • Blevins MB, Smith AM, Phillips EM, Powers MA (2003) Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP. J Biol Chem 278:20979–20988

    Article  CAS  PubMed  Google Scholar 

  • Blower MD, Nachury M, Heald R, Weis K (2005) A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121:223–234

    Article  CAS  PubMed  Google Scholar 

  • Braun IC, Herold A, Rode M, Conti E, Izaurralde E (2001) Overexpression of TAP/p15 heterodimers by passes nuclear retention and stimulates nuclear mRNA export. J Biol Cell 276:20536–20543

    CAS  Google Scholar 

  • Braun IC, Herold A, Rode M, Izaurralde E (2002) Nuclear export of mRNA by TAP/NXF1 requires two nucleoporin-binding sites but not p15. Mol Cell Biol 22:5405–5418

    Article  CAS  PubMed  Google Scholar 

  • Compton D (2000) Spindle assembly in animal cells. Annu Rev Biochem 69:95–114

    Article  CAS  PubMed  Google Scholar 

  • Conti E, Izaurralde E (2001) Nucleocytoplasmic transport enters the atomic age. Curr Opin Cell Biol 13:310–319

    Article  CAS  PubMed  Google Scholar 

  • Cullen C, Ohkura H (2001) MSPS protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3:637–642

    Article  CAS  PubMed  Google Scholar 

  • Dammerman A, Desai A, Oegema K (2003) The minus end in sight. Curr Biol 13:614–624

    Article  Google Scholar 

  • Forler D, Rabut G, Ciccarelli F et al (2004) RanBP2/Nup358 provides a major binding site for NXF1–p15 dimers at the nuclear pore complex and functions in nuclear mRNA export. Mol Cell Biol 24:1155–116

    Article  CAS  PubMed  Google Scholar 

  • Fribourg S, Braun IC, Izaurralde E, Conti E (2001) Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol Cell 8:645–656

    Article  CAS  PubMed  Google Scholar 

  • Funabiki H (2005) Two birds with one stone—dealing with nuclear transport and spindle assembly. Cell 121:157–158

    Article  CAS  PubMed  Google Scholar 

  • Gatfield D, Izaurralde E (2002) REF1/Aly and the additional exon junction complex proteins and dispensable for nuclear mRNA export. J Cell Biol 159:579–588

    Article  CAS  PubMed  Google Scholar 

  • Gergely F, Draviam V, Raff J (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17:336–341

    Article  CAS  PubMed  Google Scholar 

  • Golubkova E, Nokkala S, Mamon L (2006) The nuclear export factor gene small bristles is involved in the control of early embryonic mitoses in Drosophila melanogaster. Dros Inf Serv 89:31–39

    Google Scholar 

  • Grant RP, Hurt E, Neuhaus D, Stewart M (2002) Structural basis for the interaction between the Tap C-terminal domain and FG repeat-containing nucleoporins. Nat Struct Biol 9:247–251

    Article  CAS  PubMed  Google Scholar 

  • Groisman I, Huang YS, Mendez R, Cao Q, Theurkauf W, Richter JD (2000) CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: Implications for local translational control of cell division. Cell 103:435–447

    Article  CAS  PubMed  Google Scholar 

  • Hatsumi M, Endow S (1992) Mutants of the microtubule motor protein, nonclaret disjunctional, affect spindle structure and chromosome movement in meiosis and mitosis. J Cell Sci 101:547–559

    PubMed  Google Scholar 

  • Heald R, Tournebize R, Blank T (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420–425

    Article  CAS  PubMed  Google Scholar 

  • Herold A, Suyama M, Rodrigues J et al (2000) TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol 20:8996–9008

    Article  CAS  PubMed  Google Scholar 

  • Herold A, Klymenko T, Izaurralde E (2001) NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila. RNA 7:1768–1780

    CAS  PubMed  Google Scholar 

  • Herold A, Teixeira L, Izaurralde E (2003) Genome-wide analysis of nuclear mRNA export pathways in Drosophila. EMBO J 22:2472–2483

    Article  CAS  PubMed  Google Scholar 

  • Hetzer M, Gruss O, Mattaj W (2002) The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly (review). Nature Cell Biol 4:177–184

    Article  Google Scholar 

  • Huang Y, Gattoni R, Stevenin J, Steitz JA (2003) SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 11:837–843

    Article  CAS  PubMed  Google Scholar 

  • Izaurralde E (2001) A conserved family of nuclear export receptors mediates the exit of messenger RNA to the cytoplasm. Cell Mol Life Sci 58:1105–1112

    Article  CAS  PubMed  Google Scholar 

  • Jun L, Frints S, Duhamel H et al (2001) NXF5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation. Curr Biol 11:1381–1391

    Article  CAS  PubMed  Google Scholar 

  • K’ergaard A, Mamon L (2007) Hyperthermia of male Drosophila melanogaster meiocytes induces abnormalities in both paternal and maternal sex chromosome sets of the offspring. Russ J Genet 43:1153–1160

    Article  Google Scholar 

  • Karsenti E, Vernos I (2001) The mitotic spindle: a self-made machine. [Review]. Science 294:543–547

    Article  CAS  PubMed  Google Scholar 

  • Kataoka N, Yong J, Kim VN, Velazquez F, Perkinson RA, Wang F, Dreyfuss G (2000) Pre-mRNA splicing imprints mRNA in the nucleus with a novel RNA-binding protein that persists in the cytoplasm. Molecular Cell 6:673–682

    Article  CAS  PubMed  Google Scholar 

  • Korey CA, Wilkie GS, Davis I, Van Vactor D (2001) small bristles, DmNXF1, is required for the morphogenesis of multiple tissues during Drosophila development. Genetics 159:1659–1670

    CAS  PubMed  Google Scholar 

  • Kwon M, Scholey J (2004) Spindle mechanics and dynamics during mitosis in Drosophila. Trends Cell Biol 14:194–205

    Article  CAS  PubMed  Google Scholar 

  • Le Hir H, Gatfield D, Braun IC, Forler D, Izaurralde E (2001) The protein Mago provides a link between splicing and mRNA localization. EMBO J 2:1119–1124

    Article  Google Scholar 

  • Mamon L (2005) The relationship between nuclear-cytoplasmic transport and chromosome segregation. Tsitologiia 47:263–276

    CAS  PubMed  Google Scholar 

  • Mamon L (2008) The centrosome as “brain” of the animal cell. Tsitologiia 50:5–17

    CAS  PubMed  Google Scholar 

  • Mamon L, Kutskova Y (1993) The role of the heat shock proteins in restoration of the damages of mitotic chromosomes induced by a heat shock in D. melanogaster. Russ J Genet 29:606–612

    Google Scholar 

  • Mamon L, Mazur E, Churkina I, Barabanova LV (1990) Influence of the heat shock on frequency of the nondisjunction and losses of the sex chromosomes in l(1)ts403 females of Drosophila melanogaster with defect in the system of heat shock protein. Russ J Genet 26:554–556

    CAS  Google Scholar 

  • Matthies H, McDonald H, Goldstein L, Theurkauf WE (1996) Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein. J Cell Biol 134:455–464

    Article  CAS  PubMed  Google Scholar 

  • McKim K, Hawley R (1995) Chromosomal control of meiotic cell division. Science 270:1595–1601

    Article  CAS  PubMed  Google Scholar 

  • Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, Weis K (2001) Importin β is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104:95–106

    Article  Google Scholar 

  • Nikitina EA, Komarova AV, Golubkova EV, Tretyakova IV, Mamon LA (2003) Dominant effects of l(1)ts403 (sbr 10) mutation at the disjunction of sex chromosomes in meiosis of Drosophila melanogaster female after heat shock. Russ J Genet 39:341–348

    CAS  Google Scholar 

  • Nokkala S, Nokkala C (2003) Cytological analysis of oogenesis. In: Henderson D (ed) Methods in Molecular Biology, vol. 247: Drosophila Cytogenetics Protocols. Humana Press Inc, Totowa, NJ, pp 129–135

    Chapter  Google Scholar 

  • Ooe N, Saito K, Mikami N, Nakatuka I, Kaneko H (2004) Identification of a novel basic helix-loop-helix-PAS factor, NXF, reveals a Sim2 competitive, positive regulatory role in dendritic-cytoskeleton modulator Drebrin gene expression. Mol Cell Biol 24:608–619

    Article  CAS  PubMed  Google Scholar 

  • Pougatcheva OM, Mamon LA (2005) The genetic nature of abnormal larval development in the progeny of l(1)ts403(sbr 10 ) females Drosophila melanogaster. Tsitologiia 47:623–636

    Google Scholar 

  • Rodrigues J, Rode M, Gatfield D, Blencowe BJ, Carmo-Fonseca M, Izaurralde E (2001) REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proc Natl Acad Sci U S A 98:1030–1035

    Article  CAS  PubMed  Google Scholar 

  • Ryan K, Wente S (2000) The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr Opin Cell Biol 12:361–371

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning, A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sasaki M, Takeda E, Takano K, Yomogida K, Katahira J, Yoneda Y (2005) Molecular cloning and functional characterization of mouse Nxf family gene products. Genomics 85:641–653

    Article  CAS  PubMed  Google Scholar 

  • Segref A, Sharma K, Doye V et al (1997) Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J 16:3256–3271

    Article  CAS  PubMed  Google Scholar 

  • Sitterlin D (2004) Characterization of the Drosophila Rae1 protein as a G1 phase regulator of the cell cycle. Gene 326:107–116

    Article  CAS  PubMed  Google Scholar 

  • Skold H, Komma D, Endow S (2005) Assembly pathway of the anastral Drosophila oocyte meiosis I spindle. J Cell Sci 118:1745–1755

    Article  PubMed  Google Scholar 

  • Stutz F, Bachi A, Doerks T et al (2000) REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 6:638–650

    Article  CAS  PubMed  Google Scholar 

  • Tan W, Zolotukhin AS, Bear J, Patenaude DJ, Felber BK (2000) The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA 6:1762–1772

    Article  CAS  PubMed  Google Scholar 

  • Theurkauf W, Hawley R (1992) Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesine-like protein. J Cell Biol 116:1167–1180

    Article  CAS  PubMed  Google Scholar 

  • Tretyakova IV, Lyozin GT, Markova EG, Evgen’ev MB, Mamon LA (2001) The sbr gene product in Drosophila melanogaster and its orthologs in yeast (Mex67p) and human (TAP). Russ J Genet 37:593–602

    Article  CAS  Google Scholar 

  • Tretyakova I, Zolotukhin A, Tan W et al (2005) NXF family protein participates in cytoplasmic mRNA trafficking. J Biol Chem 280:31981–31990

    Article  CAS  PubMed  Google Scholar 

  • Wiese C, Wilde A, Moore MS, Adam SA, Merdes A, Zheng Y (2001) Role of importin-β in coupling Ran to downstream targets in microtubule assembly. Science 291:653–656

    Article  CAS  PubMed  Google Scholar 

  • Wong R, Blobel G, Coutavas E (2006) Rae1 interaction with NuMA is required for bipolar spindle formation. Proc Natl Acad Sci USA 103:19783–19787

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank M. B. Evgen’ev and I. F. Zhimulev for the sbr mutants strains. The study has been supported by grant CRDF-Ministry of Education ST-012, awarded by the leading schools, and by grants RFBR-06-04-49519 and SciSch-197.2008.4.

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Authors and Affiliations

  1. Department of Genetics, St. Petersburg State University, Universitetskaya nab., 7/9, 199034, Saint-Petersburg, Russia

    Elena V. Golubkova, Ekaterina G. Markova, Anton V. Markov, Elina O. Avanesyan & Ludmila A. Mamon

  2. Laboratory of Genetics, Department of Biology, University of Turku, 20014, Turku, Finland

    Seppo Nokkala

Authors
  1. Elena V. Golubkova
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  2. Ekaterina G. Markova
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  3. Anton V. Markov
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  6. Ludmila A. Mamon
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Correspondence to Elena V. Golubkova.

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Golubkova, E.V., Markova, E.G., Markov, A.V. et al. Dm nxf1/sbr gene affects the formation of meiotic spindle in female Drosophila melanogaster . Chromosome Res 17, 833–845 (2009). https://doi.org/10.1007/s10577-009-9046-x

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