Abstract
The oocytes of many organisms, including frogs and fish, contain a distinct cytoplasmic organelle called the Balbiani body. Because of the scarcity of published information and the tremendous variability in the appearance, ultrastructure, and composition of Balbiani bodies between species, the function of the Balbiani body and its inter-species homology remain a mystery. In Xenopus laevis, the Balbiani body is known to play a role in transporting germ cell determinants and localized RNAs to the oocyte vegetal cortex. In fish, however, the molecular composition of the Balbiani body has not been studied to date, and its function remains completely unknown. We have studied the ultrastructure and molecular composition of previtellogenic oocytes of the sturgeon, Acipenser gueldenstaedtii, by using electron microscopy, in situ hybridization, and immunostaining. We have found that sturgeon oocytes contain two distinct zones of cytoplasm: homogeneous (organelle-free) and granular (organelle-rich). We have also found that the granular ooplasm, which we term the Balbiani cytoplasm, shares important homologies, in both ultrastructure and molecular composition, with Xenopus Balbiani bodies.
Similar content being viewed by others
References
Azevedo C (1984) Development and ultrastructural autoradiographic studies of nucleolus-like bodies (nuages) in oocytes of a viviparous teleost (Xiphophorus helleri). Cell Tissue Res 238:121–128
Beams HW, Kessel RG (1973) Oocyte structure and early vitellogenesis in the trout, Salmo gairdneri. Am J Anat 136:105–121
Begovac PC, Wallace RA (1988) Stages of oocyte development in the pipefish, Syngnathus scovelli. J Morphol 197:353–369
Bilinski SM, Jaglarz MK, Szymanska B, Etkin LD, Kloc M (2004) Sm proteins, the constituents of the spliceosome, are components of nuage and mitochondrial cement in Xenopus oocytes. Exp Cell Res 299:171–178
Bradley JT, Kloc M, Wolfe KG, Estridge BH, Bilinski SM (2001) Balbiani bodies in cricket oocytes: development, ultrastructure, and presence of localized RNAs. Differentiation 67:117–127
Chan AP, Kloc M, Etkin LD (1999) Fatvg encodes a new localized RNA that uses a 25-nucleotide element (FVLE1) to localize to the vegetal cortex of Xenopus oocytes. Development 126:4943–4953
Chan AP, Kloc M, Bilinski S, Etkin LD (2001) The vegetally localized mRNA Fatvg is associated with the germ plasm in the early embryo and is later expressed in the fat body. Mech Dev 100:137–140
Chang P, Torres J, Lewis RA, Mowry KL, Houliston E, King ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15:4669–4681
Deshler JO, Highett MI, Schnapp BJ (1997) Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276:1128–1131
Deshler JO, Highett MI, Abramson T, Schnapp BJ (1998) A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates. Curr Biol 8:489–496
Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280
Forristall C, Pondel M, Chen L, King ML (1995) Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat2. Development 121:201–208
Heasman J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev Biol 105:458–469
Houston DW, King ML (2000) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127:447–456
Hudson C, Woodland HR (1998) Xpat, a gene expressed specifically in germ plasm and primordial germ cells of Xenopus laevis. Mech Dev 73:159–168
Johnson AD, Drum M, Bachvarova RF, Masi T, White ME, Crother BI (2003) Evolution of predetermined germ cells in vertebrate embryos: implications for macroevolution. Evol Dev 5:414–431
Kloc M, Etkin LD (1995) Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development 121:287–297
Kloc M, Etkin LD (1998) Apparent continuity between the METRO and late RNA localization pathways during oogenesis in Xenopus. Mech Dev 73:95–106
Kloc M, Etkin LD (1999) Analysis of localized RNAs in Xenopus oocytes. In: Richter J (ed) Advances in molecular biology. A comparative methods approach to the study of oocytes and embryos. Oxford University Press, Oxford, pp 256–278
Kloc M, Larabell C, Chan A-P, Etkin LD (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75:81–93
Kloc M, Dougherty M, Bilinski S, Chan A-P, Brey E, King ML, Patrick P, Etkin LD (2002) Three dimensional ultrastructural analysis of RNA distribution in germinal granules in Xenopus. Dev Biol 241:79–93
Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD (2004a) Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266:43–61
Kloc M, Bilinski S, Etkin LD (2004b) The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59:1–36
Kobayashi H, Iwamatsu T (2000) Development and fine structure of the yolk nucleus of previtellogenic oocytes in the medaka Oryzias latipes. Dev Growth Differ 42:623–631
Nüsslein-Volhard C, Frohnhofer HG, Lehmann R (1987) Determination of anteroposterior polarity in Drosophila. Science 238:1675–1681
Selman K, Wallace RA (1986) Gametogenesis in Fundulus heteroclitus. Am Zool 26:173–192
Selman K, Wallace AR (1989) Cellular aspects of oocyte growth in teleosts. Zool Sci 6:211–231
Song H-W, Cauffman K, Chan A-P, Zhou Y, King ML, Etkin LD, Kloc M (2007) Hermes RNA binding protein targets RNAs encoding proteins involved in meiotic maturation, early cleavage, and germline development. Differentation (in press)
Wilk K, Bilinski S, Dougherty MT, Kloc M (2005) Delivery of germinal granules and localized RNAs via the messenger transport organizer pathway to the vegetal cortex of Xenopus oocytes occurs through directional expansion of the mitochondrial cloud. Int J Dev Biol 49:17–21
Zelazowska M, Kilarski W, Bilinski S (2006) Sturgeons’ previtellogenic ovarian follicles—ultrastructural and histological analysis. Acta Biol Crac Ser Bot 48 (Suppl 1):75
Acknowledgements
The authors are grateful to Prof. R. Kolman (Institute of Inland Fisheries, Olsztyn-Kortowo, Poland) who shared his passion and knowledge of sturgeons with us and who performed the ovarian biopsies, to the staff of the Institute of Ichthyology and Fisheries (Agricultural Academy, Krakow, Poland) for the specimens of Acipenser gueldenstaedtii, to Prof. E. Pyza (Institute of Zoology, Jagiellonian University, Krakow, Poland) for electron microscopy facilities, and to Mrs. B. Szymanska, Mrs. W. Jankowska, and Mrs. E. Kisiel for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by funds from the research grant BW/IZ/2005 to M.Z.
Rights and permissions
About this article
Cite this article
Zelazowska, M., Kilarski, W., Bilinski, S.M. et al. Balbiani cytoplasm in oocytes of a primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani body (mitochondrial cloud) of Xenopus laevis oocytes. Cell Tissue Res 329, 137–145 (2007). https://doi.org/10.1007/s00441-007-0403-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-007-0403-9