© The Rockefeller University Press,
0021-9525/1997//817 $5.00
The Journal of Cell Biology, Volume 139, Number 3,
, 1997 817-829
A Sponge-like Structure Involved in the Association and Transport of Maternal Products during Drosophila Oogenesis
Michaela Wilsch-Bräuninger,
Heinz Schwarz, and
Christiane Nüsslein-Volhard
Max-Planck-Institut für Entwicklungsbiologie, D-72076 Tübingen, Germany
Localization of maternally provided RNAs during oogenesis is required for formation of the antero–posterior axis of the Drosophila embryo. Here we describe a subcellular structure in nurse cells and oocytes which may function as an intracellular compartment for assembly and transport of maternal products involved in RNA localization. This structure, which we have termed "sponge body," consists of ER-like cisternae, embedded in an amorphous electron-dense mass. It lacks a surrounding membrane and is frequently associated with mitochondria. The sponge bodies are not identical to the Golgi complexes. We suggest that the sponge bodies are homologous to the mitochondrial cloud in Xenopus oocytes, a granulo-fibrillar structure that contains RNAs involved in patterning of the embryo.
Exuperantia protein, the earliest factor known to be required for the localization of bicoid mRNA to the anterior pole of the Drosophila oocyte, is highly enriched in the sponge bodies but not an essential structural component of these. RNA staining indicates that sponge bodies contain RNA. However, neither the intensity of this staining nor the accumulation of Exuperantia in the sponge bodies is dependent on the amount of bicoid mRNA present in the ovaries. Sponge bodies surround nuage, a possible polar granule precursor. Microtubules and microfilaments are not present in sponge bodies, although transport of the sponge bodies through the cells is implied by their presence in cytoplasmic bridges. We propose that the sponge bodies are structures that, by assembly and transport of included molecules or associated structures, are involved in localization of mRNAs in Drosophila oocytes.
1. Abbreviations used in this paper: bcd, bicoid; capu, cappuccino; exu, exuperantia; GFP, green fluorescent protein; MT, microtubule; osk, oskar; spir, spire.
The serendipity fly stocks were a gift from A. Vincent, and T. Hazelrigg (Columbia University, New York) kindly provided the Exu–GFP-transgenic flies. The Vasa antibody was kindly provided by B. Hay (University of California Berkeley, CA). Inge Zimmermann has prepared some of the sections shown in this paper. We thank Jürg Müller and other members of the lab for critical comments on the manuscript.
Address all correspondence to Michaela Wilsch-Bräuninger, Max-Planck-Institut für Entwicklungsbiologie, Spemannstr. 35/III, D-72076 Tübingen, Germany. Tel.: (07 071) 601 490. Fax: (07 071) 601 384. E-mail: mibr{at}gen.mpib-tuebingen.mpg.de

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Szakmary, A., Reedy, M., Qi, H., Lin, H.
(2009). The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. JCB
185: 613-627
[Abstract]
[Full Text]
-
Roper, K.
(2007). Rtnl1 is enriched in a specialized germline ER that associates with ribonucleoprotein granule components. J. Cell Sci.
120: 1081-1092
[Abstract]
[Full Text]
-
Anne, J., Ollo, R., Ephrussi, A., Mechler, B. M.
(2007). Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila. Development
134: 137-146
[Abstract]
[Full Text]
-
Monzo, K., Papoulas, O., Cantin, G. T., Wang, Y., Yates, J. R. III, Sisson, J. C.
(2006). Fragile X mental retardation protein controls trailer hitch expression and cleavage furrow formation in Drosophila embryos. Proc. Natl. Acad. Sci. USA
103: 18160-18165
[Abstract]
[Full Text]
-
Schlichting, K., Wilsch-Brauninger, M., Demontis, F., Dahmann, C.
(2006). Cadherin Cad99C is required for normal microvilli morphology in Drosophila follicle cells. J. Cell Sci.
119: 1184-1195
[Abstract]
[Full Text]
-
Bokel, C., Dass, S., Wilsch-Brauninger, M., Roth, S.
(2006). Drosophila Cornichon acts as cargo receptor for ER export of the TGF{alpha}-like growth factor Gurken. Development
133: 459-470
[Abstract]
[Full Text]
-
Shiina, N., Shinkura, K., Tokunaga, M.
(2005). A Novel RNA-Binding Protein in Neuronal RNA Granules: Regulatory Machinery for Local Translation. J. Neurosci.
25: 4420-4434
[Abstract]
[Full Text]
-
Kloc, M., Etkin, L. D.
(2005). RNA localization mechanisms in oocytes. J. Cell Sci.
118: 269-282
[Abstract]
[Full Text]
-
Riechmann, V., Ephrussi, A.
(2004). Par-1 regulates bicoid mRNA localisation by phosphorylating Exuperantia. Development
131: 5897-5907
[Abstract]
[Full Text]
-
Chang, P., Torres, J., Lewis, R. A., Mowry, K. L., Houliston, E., King, M. L.
(2004). Localization of RNAs to the Mitochondrial Cloud in Xenopus Oocytes through Entrapment and Association with Endoplasmic Reticulum. Mol. Biol. Cell
15: 4669-4681
[Abstract]
[Full Text]
-
Snee, M. J., Macdonald, P. M.
(2004). Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J. Cell Sci.
117: 2109-2120
[Abstract]
[Full Text]
-
Sardet, C., Nishida, H., Prodon, F., Sawada, K.
(2003). Maternal mRNAs of PEM and macho 1, the ascidian muscle determinant, associate and move with a rough endoplasmic reticulum network in the egg cortex. Development
130: 5839-5849
[Abstract]
[Full Text]
-
Ventela, S., Toppari, J., Parvinen, M.
(2003). Intercellular Organelle Traffic through Cytoplasmic Bridges in Early Spermatids of the Rat: Mechanisms of Haploid Gene Product Sharing. Mol. Biol. Cell
14: 2768-2780
[Abstract]
[Full Text]
-
Cox, R. T., Spradling, A. C.
(2003). A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development
130: 1579-1590
[Abstract]
[Full Text]
-
Sinka, R., Jankovics, F., Somogyi, K., Szlanka, T., Lukacsovich, T., Erdelyi, M.
(2003). poirot, a new regulatory gene of Drosophila oskar acts at the level of the short Oskar protein isoform. Development
129: 3469-3478
[Abstract]
[Full Text]
-
Findley, S. D., Tamanaha, M., Clegg, N. J., Ruohola-Baker, H.
(2003). Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development
130: 859-871
[Abstract]
[Full Text]
-
Carre, D., Djediat, C., Sardet, C.
(2002). Formation of a large Vasa-positive germ granule and its inheritance by germ cells in the enigmatic Chaetognaths. Development
129: 661-670
[Abstract]
[Full Text]
-
Nakamura, A., Amikura, R., Hanyu, K., Kobayashi, S.
(2001). Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development
128: 3233-3242
[Abstract]
[Full Text]
-
Schisa, J., Pitt, J., Priess, J.
(2001). Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development
128: 1287-1298
[Abstract]
-
Castrillon, D. H., Quade, B. J., Wang, T. Y., Quigley, C., Crum, C. P.
(2000). The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl. Acad. Sci. USA
10.1073/pnas.160274797v1
[Abstract]
[Full Text]
-
Wilhelm, J. E., Mansfield, J., Hom-Booher, N., Wang, S., Turck, C. W., Hazelrigg, T., Vale, R. D.
(2000). Isolation of a Ribonucleoprotein Complex Involved in mRNA Localization in Drosophila Oocytes. JCB
148: 427-440
[Abstract]
[Full Text]
-
Sen, J, Goltz, J., Konsolaki, M, Schupbach, T, Stein, D
(2000). Windbeutel is required for function and correct subcellular localization of the Drosophila patterning protein Pipe. Development
127: 5541-5550
[Abstract]
-
Pare, C, Suter, B
(2000). Subcellular localization of Bic-D::GFP is linked to an asymmetric oocyte nucleus. J. Cell Sci.
113: 2119-2127
[Abstract]
-
Wickham, L., Duchaine, T., Luo, M., Nabi, I. R., DesGroseillers, L.
(1999). Mammalian Staufen Is a Double-Stranded-RNA- and Tubulin-Binding Protein Which Localizes to the Rough Endoplasmic Reticulum. Mol. Cell. Biol.
19: 2220-2230
[Abstract]
[Full Text]
-
Theurkauf, W., Hazelrigg, T.
(1998). In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development
125: 3655-3666
[Abstract]
-
Castrillon, D. H., Quade, B. J., Wang, T. Y., Quigley, C., Crum, C. P.
(2000). The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl. Acad. Sci. USA
97: 9585-9590
[Abstract]
[Full Text]