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Science 20 December 1996:
Vol. 274. no. 5295, pp. 2075 - 2079
DOI: 10.1126/science.274.5295.2075
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Reports

Requirement for a Noncoding RNA in Drosophila Polar Granules for Germ Cell Establishment

Akira Nakamura, Reiko Amikura, Masanori Mukai, Satoru Kobayashi, Paul F. Lasko *

In Drosophila embryos, germ cell formation is induced by specialized cytoplasm at the posterior of the egg, the pole plasm. Pole plasm contains polar granules, organelles in which maternally produced molecules required for germ cell formation are assembled. An untranslatable RNA, called Polar granule component (Pgc), was identified and found to be localized in polar granules. Most pole cells in embryos produced by transgenic females expressing antisense Pgc RNA failed to complete migration and to populate the embryonic gonads, and females that developed from these embryos often had agametic ovaries. These results support an essential role for Pgc RNA in germline development.

A. Nakamura and P. F. Lasko, Department of Biology, McGill University, Montréal, Québec H3A 1B1, Canada.
R. Amikura, M. Mukai, S. Kobayashi, Institute of Biological Sciences, Gene Experiment Center, and Center for Tsukuba Advanced Research Alliance (TARA), University of Tsukuba, Tsukuba, Ibaraki 305, Japan.
*   To whom correspondence should be addressed. E-mail: paul_lasko{at}maclan.mcgill.ca


References

  • AMIKURA, R, NONRADIOACTIVE IN-SITU HYBRIDIZATION METHODS FAR DROSOPHILA EMBRYOS DETECTING SIGNALS BY IMMUNOGOLD-SILVER OR IMMUNOPEROXIDASE METHOD FOR ELECTRON-MICROSCOPY, DEVELOPMENT GROWTH & DIFFERENTIATION 35: 617 (1993).
  • AMIKURA, R, Changes in subcellular localization of mtlrRNA outside mitochondria in oogenesis and early embryogenesis of Drosophila melanogaster, DEVELOPMENT GROWTH & DIFFERENTIATION 38: 489 (1996).
  • AMIKURA, R, unpublished data.
  • ASHBURNER, M, DROSOPHILA CODON TAB (1990).
  • BARDSLEY, A, DISTRIBUTION OF TUDOR PROTEIN IN THE DROSOPHILA EMBRYO SUGGESTS SEPARATION OF FUNCTIONS BASED ON SITE OF LOCALIZATION, DEVELOPMENT 119: 207 (1993).
  • BOSWELL, R.E., TUDOR, A GENE REQUIRED FOR ASSEMBLY OF THE GERM PLASM IN DROSOPHILA-MELANOGASTER, CELL 43: 97 (1985).
  • BREITWIESER, W, Oskar protein interaction with Vasa represents an essential step in polar granule assembly, GENES & DEVELOPMENT 10: 2179 (1996).
  • BROWN, N.H., FUNCTIONAL CDNA LIBRARIES FROM DROSOPHILA EMBRYOS, JOURNAL OF MOLECULAR BIOLOGY 203: 425 (1988).
  • CAVENER, D.R., ATLAS DROSOPHILA GEN 359 (1993).
  • CHOMCZYNSKI, P, SINGLE-STEP METHOD OF RNA ISOLATION BY ACID GUANIDINIUM THIOCYANATE PHENOL CHLOROFORM EXTRACTION, ANALYTICAL BIOCHEMISTRY 162: 156 (1987).
  • DEVRIES, G.E., CLONING, EXPRESSION, AND SEQUENCE-ANALYSIS OF THE BACILLUS-METHANOLICUS C1 METHANOL DEHYDROGENASE GENE, JOURNAL OF BACTERIOLOGY 174: 5346 (1992).
  • EDDY, E.M., GERM PLASM AND DIFFERENTIATION OF GERM-CELL LINE, INTERNATIONAL REVIEW OF CYTOLOGY-A SURVEY OF CELL BIOLOGY 43: 229 (1975).
  • EPHRUSSI, A, OSKAR ORGANIZES THE GERM PLASM AND DIRECTS LOCALIZATION OF THE POSTERIOR DETERMINANT NANOS, CELL 66: 37 (1991).
  • EPHRUSSI, A, INDUCTION OF GERM-CELL FORMATION BY OSKAR, NATURE 358: 387 (1992).
  • FORRISTALL, C, PATTERNS OF LOCALIZATION AND CYTOSKELETAL ASSOCIATION OF 2 VEGETALLY LOCALIZED RNAS, VG1 AND XCAT-2, DEVELOPMENT 121: 201 (1995).
  • FROHNHOFER, H.G., MANIPULATING THE ANTEROPOSTERIOR PATTERN OF THE DROSOPHILA EMBRYO, JOURNAL OF EMBRYOLOGY AND EXPERIMENTAL MORPHOLOGY 97: 169 (1986).
  • GRUNERT, S, RNA localization and the development of asymmetry during Drosophila oogenesis, CURRENT OPINION IN GENETICS & DEVELOPMENT 6: 395 (1996).
  • HAY, B, IDENTIFICATION OF A COMPONENT OF DROSOPHILA POLAR GRANULES, DEVELOPMENT 103: 625 (1988).
  • IKENISHI, K, DIRECT EVIDENCE FOR THE PRESENCE OF GERM-CELL DETERMINANT IN VEGETAL POLE CYTOPLASM OF XENOPUS-LAEVIS AND IN A SUBCELLULAR FRACTION OF IT, DEVELOPMENT GROWTH & DIFFERENTIATION 28: 563 (1986).
  • ILLMENSEE, K, TRANSPLANTATION OF POSTERIOR POLAR PLASM IN DROSOPHILA - INDUCTION OF GERM-CELLS AT ANTERIOR POLE OF EGG, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 71: 1016 (1974).
  • JONGENS, T.A., GERM CELL-LESS ENCODES A CELL-TYPE-SPECIFIC NUCLEAR PORE-ASSOCIATED PROTEIN AND FUNCTIONS EARLY IN THE GERM-CELL SPECIFICATION PATHWAY OF DROSOPHILA, GENES & DEVELOPMENT 8: 2123 (1994).
  • KLOC, M, TRANSLOCATION OF REPETITIVE RNA SEQUENCES WITH THE GERM PLASM IN XENOPUS-OOCYTES, SCIENCE 262: 1712 (1993).
  • KLOC, M, DELOCALIZATION OF VG1 MESSENGER-RNA FROM THE VEGETAL CORTEX IN XENOPUS-OOCYTES AFTER DESTRUCTION OF XLSIRT RNA, SCIENCE 265: 1101 (1994).
  • KOBAYASHI, S, RESTORATION OF POLE-CELL-FORMING ABILITY TO UV-IRRADIATED DROSOPHILA EMBRYOS BY INJECTION OF MITOCHONDRIAL LRRNA, DEVELOPMENT 107: 733 (1989).
  • KOBAYASHI, S, LOCALIZATION OF MITOCHONDRIAL LARGE RIBOSOMAL-RNA IN GERMINAL GRANULES AND THE CONSEQUENT SEGREGATION OF GERM-LINE, INTERNATIONAL JOURNAL OF DEVELOPMENTAL BIOLOGY 38: 193 (1994).
  • KOBAYASHI, S, Essential role of the posterior morphogen nanos for germline development in Drosophila, NATURE 380: 708 (1996).
  • KOBAYASHI, S, PRESENCE OF MITOCHONDRIAL LARGE RIBOSOMAL-RNA OUTSIDE MITOCHONDRIA IN GERM PLASM OF DROSOPHILA-MELANOGASTER, SCIENCE 260: 1521 (1993).
  • LANTZ, V, THE DROSOPHILA ORB GENE IS PREDICTED TO ENCODE SEX-SPECIFIC GERMLINE RNA-BINDING PROTEINS AND HAS LOCALIZED TRANSCRIPTS IN OVARIES AND EARLY EMBRYOS, DEVELOPMENT 115: 75 (1992).
  • LAVOIE, C, J BIOL CHEM 269: 14625 (1996).
  • LEHMANN, R, ABDOMINAL SEGMENTATION, POLE CELL-FORMATION, AND EMBRYONIC POLARITY REQUIRE THE LOCALIZED ACTIVITY OF OSKAR, A MATERNAL GENE IN DROSOPHILA, CELL 47: 141 (1986).
  • LEHMANN, R, THE MATERNAL GENE NANOS HAS A CENTRAL ROLE IN POSTERIOR PATTERN-FORMATION OF THE DROSOPHILA EMBRYO, DEVELOPMENT 112: 679 (1991).
  • LIANG, P, DIFFERENTIAL DISPLAY OF EUKARYOTIC MESSENGER-RNA BY MEANS OF THE POLYMERASE CHAIN-REACTION, SCIENCE 257: 967 (1992).
  • MAHONE, M, LOCALIZED BICAUDAL-C RNA ENCODES A PROTEIN CONTAINING A KH DOMAIN, THE RNA-BINDING MOTIF OF FMR1, EMBO JOURNAL 14: 2043 (1995).
  • MAHOWALD, A.P., ULTRASTRUCTURE OF GERM PLASM IN EGGS AND EMBRYOS OF RANA-PIPIENS, DEVELOPMENTAL BIOLOGY 24: 37 (1971).
  • MAHOWALD, A.P., FINE STRUCTURE OF POLE CELLS AND POLAR GRANULES IN DROSOPHILA MELANOGASTER, JOURNAL OF EXPERIMENTAL ZOOLOGY 151: 201 (1962).
  • MAHOWALD, A.P., POLAR GRANULES OF DROSOPHILA .3. CONTINUITY OF POLAR GRANULES DURING LIFE CYCLE OF DROSOPHILA, JOURNAL OF EXPERIMENTAL ZOOLOGY 176: 329 (1971).
  • MOSQUERA, L, A MESSENGER-RNA LOCALIZED TO THE VEGETAL CORTEX OF XENOPUS OOCYTES ENCODES A PROTEIN WITH A NANOS-LIKE ZINC FINGER DOMAIN, DEVELOPMENT 117: 377 (1993).
  • NAKAMURA, A, unpublished data.
  • RONGO, C, Regulated synthesis, transport and assembly of the Drosophila germ plasm, TRENDS IN GENETICS 12: 102 (1996).
  • SPRADLING, A.C., TRANSPOSITION OF CLONED P ELEMENTS INTO DROSOPHILA GERM LINE CHROMOSOMES, SCIENCE 218: 341 (1982).
  • STJOHNSTON, D, DEV DROSOPHILA MELAN 325 (1993).
  • STROME, S, IMMUNOFLUORESCENCE VISUALIZATION OF GERM-LINE-SPECIFIC CYTOPLASMIC GRANULES IN EMBRYOS, LARVAE, AND ADULTS OF CAENORHABDITIS-ELEGANS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 79: 1558 (1982).
  • SUGIYAMA, S, CYTOPLASMIC FACTORS DETERMINING ANTEROPOSTERIOR POLARITY IN DROSOPHILA EMBRYOS, ROUXS ARCHIVES OF DEVELOPMENTAL BIOLOGY 198: 402 (1990).
  • TAUTZ, D, A NON-RADIOACTIVE INSITU HYBRIDIZATION METHOD FOR THE LOCALIZATION OF SPECIFIC RNAS IN DROSOPHILA EMBRYOS REVEALS TRANSLATIONAL CONTROL OF THE SEGMENTATION GENE HUNCHBACK, CHROMOSOMA 98: 81 (1989).
  • THUMMEL, C.S., DROS INF SERV 71: 150 (1992).
  • TIAN, S.S., AN ADHESION MOLECULE-LIKE PROTEIN THAT INTERACTS WITH AND IS A SUBSTRATE FOR A DROSOPHILA RECEPTOR-LINKED PROTEIN-TYROSINE-PHOSPHATASE, JOURNAL OF BIOLOGICAL CHEMISTRY 269: 28478 (1994).
  • WANG, C, NANOS IS THE LOCALIZED POSTERIOR DETERMINANT IN DROSOPHILA, CELL 66: 637 (1991).
  • WILLIAMS, M.A., ULTRASTRUCTURE OF GERMINAL-PLASM DURING MATURATION AND EARLY CLEAVAGE IN RANA-PIPIENS, DEVELOPMENTAL BIOLOGY 25: 568 (1971).


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