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The role of sbr/Dm nxf1 gene in syncytial development in Drosophila melanogaster

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Abstract

Syncytial development is a property of early embryogenesis and spermatogenesis in Drosophila melanogaster. All elements of syncytium are linked in a common cytoskeletal network, which provides equal conditions and synchronous divisions of each nucleus. The cytoskeleton is necessary for the formation and function of the spindle. Elements of the cytoskeleton form the major structural components of cilia and flagella. The cytoskeleton is important for intraand intercellular transport and morphogenetic processes both within a single cell and at the level of the whole organism. The sbr (small bristles) gene in Drosophila melanogaster belongs to an evolutionarily conserved nxf (nuclear export factor) family. The Dm nxf1 (sbr) gene, as well as its orthologs in other organisms, control export of all poly (A)-containing RNA from the nucleus to cytoplasm. Thus, the NXF1 proteins are usually located within the nucleus or at the nuclear rim. We showed that SBR protein is located not only in the nucleus, but also in to the cytoplasm, and marks characteristic cytoplasmic structures. We identified the cytoplasmic localization of the SBR protein and the disruptions of cytoskeleton in the sbr mutants of D. melanogaster. This may suggest the specialized functions of this protein associated with the dynamics of the cytoskeleton.

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Abbreviations

mRNA:

messenger or information ribonucleic acid

RNP:

ribonucleoprotein complex

NXF (Nuclear eXport Factor):

nuclear mRNA export factor

Sbr :

small bristles

Dm :

Drosophila melanogaster

References

  • Akhmanova, A., and Steinmetz, M.O., Tracking the ends: a dynamic protein network controls the fate of microtubule tips, Nat. Rev. Mol. Cell Biol., 2008, vol. 9, pp. 309–322.

    Article  CAS  PubMed  Google Scholar 

  • Ashburner, M., Drosophila: A Laboratory Handbook and Manual, in 2 vols., New York: Cold Spring Harbor Laboratory, 1989.

  • Atsapkina, A.A., Golubkova, E.V., Kasatkina, V.V., Avanesyan, E.O., Ivankova, N.A., and Mamon, L.A., Peculiarities of spermatogenesis in Drosophila melanogaster: role of main transport receptor of mRNA (Dm NXF1), Cell Tisue Biol., 2010, vol. 4, no. 5, pp. 429–435.

    Article  Google Scholar 

  • Bashirullah, A., Cooperstock, R.L., and Lipshitz, H.D., RNA localization in development, Annu. Rev. Biochem., 1998, vol. 67, pp. 335–394.

    Article  CAS  PubMed  Google Scholar 

  • Bear, J., Tan, W., Zolotukhin, A.S., Tabernero, C., Hudson, E.A., and Felber, B.K., Identification of novel import and export signals of human TAP, the protein that binds to the constitutive transport element to the type D retrovirus mRNAs, Mol. Cell Biol., 1999, vol. 19, pp. 6306–6317.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Besse, F. and Ephrussi, A., Translational control of localized mRNAs: restricting protein synthesis in space and time, Nat. Rev. Mol. Cell Biol., 2008, vol. 9, pp. 971–980.

    Article  CAS  PubMed  Google Scholar 

  • Blevins, M.B., Smith, A.M., Phillips, E.M., and Powers, M.A., Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP, J. Biol. Chem., 2003, vol. 278, pp. 20979–20988.

    Article  CAS  PubMed  Google Scholar 

  • Blower, M.D., Nachury, M., Heald, R., and Weis, K., A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly, Cell, 2005, vol. 121, pp. 223–234.

    Article  CAS  PubMed  Google Scholar 

  • Blower, M.D., Feric, E., Weis, K., and Heald, R., Genomewide analysis demonstrates conserved localization of messenger RNAs to mitotic microtubules, J. Cell Biol., 2007, vol. 179, pp. 1365–1373.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Braun, I.C., Herold, A., Rode, M., and Izaurralde, E., Nuclear export of mRNA by TAP/NXF1 requires two nucleoporin-binding sites but not p15, Mol. Cell. Biol., 2002, vol. 22, pp. 5405–5418.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carmena, M., Riparbelli, M.G., Minestrini, G., Tavares, A.M., Adams, R., Callaini, G., and Glover, D.M., Drosophila polo kinase is required for cytokinesis, J. Cell Biol., 1998, vol. 143, pp. 659–671.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Condeelis, J., and Singer, R.H., How and why does β-actin mRNA target? Biol. Cell., 2005, vol. 97, pp. 97–110.

    Article  CAS  PubMed  Google Scholar 

  • Fabrizio, J.J., Hime, G., Lemmon, S.K., and Bazinet, C., Genetic Dissection of sperm individualization in Drosophila melanogaster, Development, 1998, vol. 125, pp. 1833–1843.

    CAS  PubMed  Google Scholar 

  • Foe, V.E., Field, C.M., and Odell, G.M., Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos, Development, 2000, vol. 127, pp. 1767–1787.

    CAS  PubMed  Google Scholar 

  • Frescas, D., Mavrakis, M., Lorenz, H., DeLotto, R., and Lippincott-Schwartz, J., The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei, J. Cell Biol., 2006, vol. 173, pp. 219–230.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fribourg, S., Braun, I.C., Izaurralde, E., and Conti, E., Structural basis for the recognition of a nucleoporin FGrepeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor, Mol. Cell., 2001, vol. 8, pp. 645–656.

    Article  CAS  PubMed  Google Scholar 

  • Fuller, M.T., Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis, Semin. Cell Develop. Biol., 1998, vol. 9, pp. 433–444.

    Article  CAS  Google Scholar 

  • Gaspar, I., Microtubule-based motor-mediated mRNA localization in Drosophila oocytes and embryos, Biochem. Soc. Trans., 2011, vol. 39, pp. 1197–1201.

    Article  CAS  PubMed  Google Scholar 

  • Giansanti, M.G., Bonnaccorsi, S., Bucciarelli, E., and Gatti, M., Drosophila male meiosis as a model system for the study of cytokinesis in animal cells, Cell Struct. Function, 2001, vol. 26, pp. 609–617.

    Article  CAS  Google Scholar 

  • Golubkova, E.V., Nokkala, S., and Mamon, L.A., The nuclear export factor gene small bristles is involved in the control of early embryonic mitoses in Drosophila melanogaster, Drosophila Inform. Serv., 2006, vol. 89, pp. 31–39.

    Google Scholar 

  • Golubkova, E.V., Markova, E.G., Markov, A.V., Avanesyan, E.O., Nokkala, S., and Mamon, L.A., Dm Nxf1/sbr gene affects the formation of meiotic spindle in female Drosophila melanogaster, Chromosome Res., 2009, vol. 17, pp. 833–845.

    Article  CAS  PubMed  Google Scholar 

  • Golubkova, E., Mamon, L., Nikulina, A., Merezhko, M., Ginanova, V., and Evgen’ev, M., The evolutionarily conserved family of nuclear export factor (NXF) in Drosophila melanogaster, in Drosophila melanogaster: Life Cycle, Genetics and Development, Universitat Ulm, Germany: Nova Sci. Publishers, 2012, pp. 63–82.

    Google Scholar 

  • Goode, B.L., Drubin, D.G., and Barnes, G., Functional cooperation between the microtubule and actin cytoskeletons, Curr. Opin. Cell Biol., 2000, vol. 12, pp. 63–71.

    Article  CAS  PubMed  Google Scholar 

  • Grill, S.W., and Hyman, A.A., Spindle positioning by cortical pulling forces, Develop. Cell., 2005, vol. 8, pp. 461–465.

    Article  CAS  Google Scholar 

  • Hautbergue, G.M., Hung, M.-L., Golovanov, A.P., Lian, L.-Y., and Wilson, S.A., Mutually exclusive interaction drive handover of mRNA from export adaptor to TAP, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 5154–5159.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi, I., Wilde, A., Mal, T.K., and Ikura, M., Structural basis for the activation of microtubule assembly by the EB1 and P150glued complex, Mol. Cell., 2005, vol. 19, pp. 449–460.

    Article  CAS  PubMed  Google Scholar 

  • Herold, A., Suyama, M., Rodrigues, J.P., Braun, I.C., Kutay, U., Carmo-Fonseca, M., Bork, P., and Izaurralde, E., TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture, Mol. Cell. Biol., 2000, vol. 20, pp. 8996–9008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hime, G.R., Brill, J.A., and Fuller, M.T., Assembly of ring canals in the male germ line from structural components of contractile ring, J. Cell Sci., 1996, vol. 109, pp. 2779–2788.

    CAS  PubMed  Google Scholar 

  • Honnappa, S., Gouveia, S.M., Weisbrich, A., Damberger, F.F., Bhavesh, N.S., Jawhari, H., Grigoriev, I., van, Rijssel, F.J.A., Buey, R.M., Lawera, A., Jelesarov, I., Winkler, F.K., Wüthrich, K., Akhmanova, A., and Steinmetz, M.O., An EB1-binding motif acts as a microtubule tip localization signal, Cell, 2009, vol. 138, pp. 366–376.

    Article  CAS  PubMed  Google Scholar 

  • Howard, J. and Hyman, A.A., Dynamics and mechanics of the microtubule plus end, Nature, 2003, vol. 422, pp. 753–758.

  • Huang, Y., Yario, T.A., and Steitz, J.A., A molecular link between SRprotein dephosphorylation and mRNA export, Proc. Natl Acad. Sci. USA, 2004, vol. 101, pp. 9666–9670.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ji, J.-Y., Squirrell, J.M., and Schubiger, G., Both cyclin B levels and DNA-replication checkpoint control the early embryonic mitoses in Drosophila, Development, 2004, vol. 131, pp. 401–411.

    Article  CAS  PubMed  Google Scholar 

  • Job, D., Valiron, O., and Oakley, B., Microtubule nucleation, Curr. Opin., 2003, vol. 15, pp. 111–117.

    Article  CAS  Google Scholar 

  • Karr, T.L., and Alberts, B.M., Organization of the cytoskeleton in early Drosophila embryos, J. Cell Biol., 1986, vol. 102, pp. 1494–1509.

    Article  CAS  PubMed  Google Scholar 

  • Katahira, J., Straßer, K., Podtelejnikov, A., Mann, M., Jung, J.U., and Hurt, E., The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human, EMBO J., 1999, vol. 18, pp. 2593–2609.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Katahira, J., Straesser, K., Saiwaki, T., Yoneda, Y., and Hurt, E., Complex formation between Tap and p15 affects binding to FG-repeat nucleoporins and nucleocytoplasmic shuttling, J. Biol. Chem., 2002, vol. 277, pp. 9242–9246.

    Article  CAS  PubMed  Google Scholar 

  • Kellogg, D.R., Mitchison, T.J., and Alberts, B.M., Behaviour of microtubules and actin filaments in living Drosophila embryos, Development, 1988, vol. 103, pp. 675–686.

    CAS  PubMed  Google Scholar 

  • Lécuyer, E., Yoshida, H., Parthasarathy, N., Alm, C., Babak, T., Cerovina, T., Hughes, T.R., Tomancak, P., and Krause, H.M., Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function, Cell, 2007, vol. 131, pp. 174–187.

    Article  PubMed  Google Scholar 

  • Lai, D., Sakkas, D., and Huang, Y., The fragile X mental retardation protein interacts with a distinct mRNA nuclear export factor NXF2, RNA, 2006, vol. 12, pp. 1446–1449.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mans, B.J., Anantharaman, V., Aravind, L., and Koonin, E.V., Comparative genomics, evolution and origins of the nuclear envelope and pore complex, Cell Cycle, 2004, vol. 3, pp. 1612–1637.

    Article  CAS  PubMed  Google Scholar 

  • Maurer, S.P., Fourniol, F.J., Bohner, G., Moores, C.A., and Surrey, T., EBs recognize a nucleotide-dependent structural cap at growing microtubule ends, Cell, 2012, vol. 149, pp. 371–382.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Medioni, C., Mowry, K., and Besse, F., Principles and roles of mRNA localization in animal development, Development, 2012, vol. 139, pp. 3263–3276.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miki, H., Setou, M., Kaneshiro, K., and Hirokawa, N., All kinesin superfamily protein, KIF, genes in mouse and human, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 7004–7011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mimori-Kiyosue, Y., and Tsukita, S., “Search-and-capture” of microtubules through plus-end-binding proteins (+TIPs), J. Biochem., 2003, vol. 134, pp. 321–326.

    Article  CAS  PubMed  Google Scholar 

  • Minestrini, G., Harley, A.S., and Glover, D.M., Localization of Pavarotti-KLP in living Drosophila embryos suggests roles in reorganizing in cortical cytoskeleton during mitotic cycle, Mol. Biol. Cell., 2003, vol. 14, pp. 4028–4038.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mingle, L.A., Okuhama, N.N., Shi, J., Singer, R.H., Condeelis, J., and Liu, G., Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts, J. Cell Sci., 2005, vol. 118, pp. 2425–2433.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nikitina, E.A., Komarova, A.V., Golubkova, E.V., Tretyakova, I.V., and Mamon, L.A., Semidominant effects of l(1)ts403 (sbr10) mutation on sex chromosomes disjunction in meiosis in Drosophila melanogaster females exposed to heat, Russ. J. Genet., 2003, vol. 39, no. 3, pp. 269–275.

    Article  CAS  Google Scholar 

  • Noguchi, T. and Miller, K.G., A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster, Development, 2003, vol. 130, pp. 1805–1816.

    Article  CAS  PubMed  Google Scholar 

  • Palacios, I.M. and St. Johnston, D., Kinesin light chainindependent function of the kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte, Development, 2002, vol. 129, pp. 5473–5485.

    Article  CAS  PubMed  Google Scholar 

  • Pokrywka, N.J. and Stephenson, E.C., Microtubules are a general component of mRNA localization systems in Drosophila oocytes, Dev. Biol., 1995, vol. 167, pp. 363–370.

    Article  CAS  PubMed  Google Scholar 

  • Riparbelli, M.G., Callaini, G., and Schejter, E., Microtubule-dependent organization of subcortical microfilaments in the early Drosophila embryo, Develop. Dynamics., 2007, vol. 236, pp. 662–670.

    Article  CAS  Google Scholar 

  • Rodrigues, J.P., Rode, M., Gatfield, D., Blencowe, B.J., and Carmo-Fonseca, M., REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 1030–1035.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez, O.C., Schaefer, A.W., Mandato, C.A., Forscher, P., Bement, W.M., and Waterman-Storer, C.M., Conserved microtubule–actin interactions in cell movement and morphogenesis, Nat. Cell Biol., 2003, vol. 5, pp. 599–609.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, S.L., Rogers, G.C., Sharp, D.J., and Vale, R.D., Drosophila EB1 is important for proper assembly, dynamic, and positioning of the mitotic spindle, J. Cell Biol., 2002, vol. 158, pp. 873–884.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schejter, E.D. and Weischaus, E., Functional elements of the cytoskeleton in the early Drosophila embryo, Annu. Rev. Cell Biol., 1993, vol. 9, pp. 67–99.

    Article  CAS  PubMed  Google Scholar 

  • Schuyler, S.C. and Pellman, D., Microtubule “plus-endtracking proteins”: the end is just the beginning, Cell, 2001, vol. 105, pp. 421–424.

    Article  CAS  PubMed  Google Scholar 

  • Sharp, J.A., Plant, J.J., Ohsumi, T.K., Borowsky, M., and Blower, M.D., Functional analysis of the microtubuleinteracting transcriptome, Mol. Biol. Cell, 2011, vol. 22, pp. 4312–4323.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson, V., Hudson, A., Cooley, L., and Theurkauf, W.E., Arp2/3-dependent pseudocleavage furrow assembly in syncytial Drosophila embryos, Curr. Biol., 2002, vol. 12, pp. 705–711.

    Article  CAS  PubMed  Google Scholar 

  • Straight, A.F. and Field, C.M., Microtubules, membranes and cytokinesis, Curr. Biol., 2000, vol. 10, pp. R760–R770.

  • Stutz, F., Bachi, A., Doerks, T., Braun, I.C., Seraphin, B., Wilm, M., Bork, P., and Izaurralde, E., REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export, RNA, 2000, vol. 6, pp. 638–650.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sundell, C.L. and Singer, R.H., Requirement of microfilaments in sorting of actin messenger RNA, Science, 1991, vol. 253, pp. 1275–1277.

    Article  CAS  PubMed  Google Scholar 

  • Takano, K., Miki, T., Katahira, J., and Yoneda, Y., NXF2 is involved in cytoplasmic mRNA dynamics through interactions with motor proteins, Nucleic Acids Res., 2007, vol. 35, pp. 2513–2521.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura, N. and Draviam, V.M., Microtubule plus-ends within a mitotic cell are 'moving platforms' with anchoring, signalling and force-coupling roles, Open Biol. 2012, vol. 2, p. 120132. doi: 10.1098/rsob.120132

    Article  PubMed Central  PubMed  Google Scholar 

  • Tan, W., Zolotukhin, A.S., Tretyakova, I., Bear, J., Lindtner, S., Smulevitch, S.V., and Felber, B.K., Identification and characterization of the mouse nuclear export factor (Nxf) family members, Nucleic Acids Res., 2005, vol. 33, pp. 3855–3865.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Telley, I.A., Gáspár, I., Ephrussi, A., and Surrey, T., Aster migration determines the length scale of nuclear separation in the Drosophila syncytial embryo, J. Cell Biol., 2012, vol. 197, pp. 887–895.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tortosa, E., Galjart, N., Avila, J., and Sayas, C.L., MAP1B regulates microtubule dynamics by sequestering EB1/3 in the cytosol of developing neuronal cells, EMBO J., 2013, vol. 32, pp. 1293–1306.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tretyakova, I., Zolotukhin, A.S., Tan, W., Bear, J., Propst, F., Ruthel, G., and Felber, B.K., Nuclear export factor family protein participates in cytoplasmic mRNA trafficking, J. Biol. Chem., 2005, vol. 280, pp. 31981–31990.

    Article  CAS  PubMed  Google Scholar 

  • Vandecandelaere, A., Pedrotti, B., Utton, M.A., Calvert, R.A., and Bayley, P.M., Differences in the regulation of microtubule dynamics by microtubule-associated proteins MAP1B and MAP2, Cell Motil. Cytoskeleton, 1996, vol. 35, pp. 134–146.

    Article  CAS  PubMed  Google Scholar 

  • Wiegand, H.L., Coburn, G.A., Zeng, Y., Kang, Y., Bogerd, H.P., and Cullen, B.R., Formation of Tap/NXT1 heterodimers activates Tap-dependent nuclear mRNA export by enhancing recruitment to nuclear pore complexes, Mol. Cell. Biol., 2002, vol. 22, pp. 245–256.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoon, D.W., Lee, H., Seol, W., DeMaria, M., Rosenzweig, M., and Jung, J.U., Tap: a novel protein that interacts with tip of herpesvirus saimiri and induces lymphocyte aggregation, Immunity, 1997, vol. 6, pp. 571–582.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H.L., Singer, R.H., and Bassell, G.J., Neurotrophin regulation of ß-actin mRNA and protein localization within growth cones, J. Cell Biol., 1999, vol. 147, pp. 59–70.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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  1. Department of Genetics and Biotechnology, St. Petersburg State University, St. Petersburg, 199034, Russia

    E. V. Golubkova, A. A. Atsapkina & L. A. Mamon

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  1. E. V. Golubkova
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  2. A. A. Atsapkina
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  3. L. A. Mamon
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Original Russian Text © E.V. Golubkova, A.A. Atsapkina, L.A. Mamon, 2015, published in Tsitologiya, 2015, Vol. 57, No. 4, pp. 294–304.

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Golubkova, E.V., Atsapkina, A.A. & Mamon, L.A. The role of sbr/Dm nxf1 gene in syncytial development in Drosophila melanogaster . Cell Tiss. Biol. 9, 271–283 (2015). https://doi.org/10.1134/S1990519X15040057

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