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Germ plasm provides clues on meiosis: the concerted action of germ plasm granules and mitochondria in gametogenesis of the clam Ruditapes philippinarum

  • Arkadiy Reunov (a1) (a2), Yana Alexandrova (a2), Yulia Reunova (a2), Alina Komkova (a2) and Liliana Milani (a3)...

Summary

Germ plasm-related structures (GPRS) are known to accompany meiotic cell differentiation but their dynamics are still poorly understood. In this study, we analyzed the ultrastructural mechanisms of GPRS transformation during oogenesis and spermatogenesis of the bivalve mollusc Ruditapes philippinarum (Manila clam), exploring patterns of GPRS activity occurring at meiosis onset, sex-specific difference/similarity of such patterns, and the involvement of mitochondria during GPRS-assigned events. In the two sexes, the zygotene–pachytene stage of meiosis is anticipated by three shared steps. First, the dispersion of germ plasm granules containing the germ line determinant VASA occurs. Second, the VASA protein deriving from germ plasm granules enters neighbouring mitochondria and appears to induce mitochondrial matter release, as supported by cytochrome B localization outside the mitochondria. Third, intranuclear VASA entrance occurs and the protein appears involved in chromatin reorganization, as supported by VASA localization in synaptonemal complexes. In spermatogenesis, these three steps are sufficient for the normal course of meiosis. In oogenesis, these are followed by the action of ‘germ plasm granule formation complex’, a novel type of structure that appears alternative to the Balbiani body. The possibility of germ plasm involvement in reproductive technologies is also suggested.

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Corresponding author

Address for correspondence: Arkadiy Reunov. Electron Microscopy Laboratory, University of Ottawa Heart Institute, 40 Ruskin St, Ottawa ON K1Y 4W7, Canada. Tel: +1 613 761 5282. Fax: +1 613 761 4998. E-mail: areunov@ottawaheart.ca

References

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Ables, ET (2015) Drosophila oocytes as a model for understanding meiosis: an educational primer to accompany ‘Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila. Genetics 199, 1723.
Amikura, R, Kashikawa, M, Nakamura, A and Kobayashi, S (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci USA 98, 91339138.
Amikura, R, Sato, K and Kobayashi, S (2005) Role of mitochondrial ribosome dependent translation in germline formation in Drosophila embryos. Mech Dev 122, 10871093.
Bilinski, SM, Kloc, M and Tworzydlo, W (2017) Selection of mitochondria in female germline cells: is Balbiani body implicated in this process? J Assist Reprod Genet 34, 14051412.
Carré, D, Djediat, C and Sardet, C (2002) Formation of a large Vasa-positive germ granule and its inheritance by germ cells in the enigmatic Chaetognaths. Development 129, 661670.
Castrillon, DH, Quade, BJ, Wang, TY, Quigley, C, Crum, CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 97, 95859590.
Chang, P, Torres, J, Lewis, RA, Mowry, KL, Houliston, E and King, ML (2004) Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15, 46694681.
Cox, RT and Spradling, AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130, 15791590.
Cuykendall, TN and Houston, DW (2010) Identification of germ plasm-associated transcripts by microarray analysis of Xenopus vegetal cortex RNA. Dev Dyn 239, 18381848.
Delgado, M and Perez-Camacho, A (2007) Comparative study of gonadal development of Ruditapes philippinarum (Adams and Reeve) and Ruditapes decussates (L.) (Mollusca; Bivalvia): influence of temperature. Scientia Marina 71, 471484.
Eckelbarger, KJ (2005) Oogenesis and oocytes. Hydrobiologia 535/536, 179198.
Findley, SD, Tamanaha, M, Clegg, NJ and 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, 859871.
Gur, Y and Breitbart, H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20, 411416.
Gur, Y and Breitbart, H (2008) Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Mol Cell Endocrinol 282, 4555.
Gustafson, EA and Wessel, GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32, 626637.
Hendriks, S, Dancet, EAF, van Pelt, AMM, Hamer, G and Repping, S (2015) Artificial gametes: a systematic review of biological progress towards clinical application. Hum Reprod Update 21, 285296.
Kalt, MR (1973) Ultrastructural observations on the germ line of Xenopus laevis . Z. Zellforsch 138, 4162.
Kashikawa, M, Amikura, R and Kobayashi, S (2001) Mitochondrial small ribosomal RNA is a component of germinal granules in Xenopus embryos. Mech Dev 101, 7177.
Kashir, J, Jones, C, Child, T, Williams, SA and Coward, K (2012) Viability assessment for artificial gametes: the need for biomarkers of functional competency. Biol Reprod 87, 111.
Kloc, M, Bilinski, S, Chan, AP and Etkin, LD (2001) Mitochondrial ribosomal RNA in the germinal granules in Xenopus embryos revisited. Differentiation 67, 8083.
Kloc, M, Dougherty, MT, Bilinski, S, Chan, AP, Brey, E, King, ML, Patrick, CW Jr and Etkin, LD (2002) Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus . Dev Biol 241, 7993.
Kobayashi, S, Amikura, R and Okada, M (1993) Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster . Science 260, 15211524.
Kobayashi, S, Amikura, R and Okada, M (1994) Localization of mitochondrial large rRNA in germinal granules and the consequent segregation of germ line. Int J Dev Biol 38, 193199.
Kobayashi, S, Amikura, R and Mukai, M (1998) Localization of mitochondrial large ribosomal RNA in germ plasm of Xenopus embryos. Curr Biol 8, 11171120.
Lasko, PF and Ashburner, M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611617.
Liang, L, Diehl-Jones, W and Lasko, P (1994) Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120, 12011211.
Lippai, M, Gobet, I, Tomkowiak, M, Durocher, Y, Leclerc, C, Moreau, M and Guerrier, P (1995) Thimerosal triggers meiosis reinitiation in oocytes of the Japanese clam Ruditapes philippinarum by eliciting an intracellular Ca2+ surge. Int J Dev Biol 39, 401407.
Mahowald, AP (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster. J Exp Zool 151, 201205.
Matova, N and Cooley, L (2001) Comparative aspects of animal oogenesis. Dev Biol 231, 291320.
Medrano, JV, Reijo Pera, RA and Simon, C (2013) Germ cell differentiation from pluripotent cells. Semin Reprod Med 31, 1423.
Milani, L, Ghiselli, F, Maurizii, MG and Passamonti, M (2011) Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS One 6, e28194.
Milani, L, Ghiselli, F, Pecci, A, Maurizii, MG and Passamonti, M (2015) The expression of a novel mitochondrially-encoded gene in gonadic precursors may drive paternal inheritance of mitochondria. PLoS One 10, e0137468
Milani, L, Pecci, A, Ghiselli, F, Passamonti, M, Bettini, S, Franceschini, V, Maurizii, MG (2017) VASA expression suggests shared germ line dynamics in bivalve molluscs. Histochem Cell Biol 148, 157171.
Moreno, I, Miguez-Forjan, JM and Simon, C (2015) Artificial gametes from stem cells. Clin Exp Reprod Med 42, 3344.
Nikolic, A, Volarevic, V, Armstrong, L, Lako, M and Stojkovic, M (2016) Primordial germ cells: current knowledge and perspectives. Stem Cell Int Article ID 1741072, http://dx.doi.org/10.1155/2016/1741072.
Ninomiya, Y and Ichinose, S (2007) Subcellular distribution of mitochondrial ribosomal RNA in the mouse oocyte and zygote. PLoS One 2, e1241.
Pek, JW and Kai, T (2011) A role for Vasa in regulating mitotic chromosome condensation in Drosophila . Curr Biol 21, 3944.
Raz, E (2000) The function and regulation of vasa-like genes in germ-cell development. Genome Biol 1, 16.
Reunov, AA (2004) Is there a germ plasm in mouse oocytes? Zygote 12, 329332.
Reunov, AA and Reunova, YA (2015) In mouse oocytes the mitochondrion-originated germinal body-like structures accumulate mouse Vasa homologue (MVH) protein. Zygote 23, 501506.
Reunov, AA, Isaeva, VV, Au, DWT and Wu, RSS (2000) Nuage constituents arising from mitochondria: is it possible? Dev Growth Differ 42, 139143.
Reunov, AA, Yurchenko, OV, Alexandrova, YN and Radashevsky, VI (2009) Spermatogenesis in Boccardiella hamata (Polychaeta: Spionidae) from the sea of Japan: sperm formation mechanisms as characteristics for future taxonomic revision. Acta Zoologica 91, 447456.
Saffman, EE and Lasko, P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55, 11411163.
Strome, S and Wood, WB (1983) Generation of asymmetry and segregation of germ line granules in early C elegans embryos. Cell 35, 1125.
Villegas, J, Araya, P, Bustos-Obregon, E and Burzio, LO (2002) Localization of the 16S mitochondrial rRNA in the nucleus of mammalian spermatogenic cells. Mol Hum Reprod 8, 977983.
Watanabe, M, Itoh, K, Abe, K, Akizawa, T, Ikenishi, K and Furusawa, M (1992) Immuno-localization of DEAD family proteins in germ line cells of Xenopus embryos. Dev Growth Differ 34, 223231.
Wilk, K, Bilinski, S, Dougherty, MT and Kloc, M (2004) 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, 1721.
Williamson, A and Lehmann, R (1996) Germ cell development in Drosophila . Annu Rev Cell Dev Biol 12, 365391.
Wolf, PM, Priess, J and Hirsh, D (1983) Segregation of germline granules in early embryos of Caenorhabditis elegans. An electron microscopic analysis. J Embryol Exp Morphol 73, 297306.
Yajima, M and Wessel, GM (2011) The multiple hats of Vasa function and its regulation of cell cycle progression. Mol Reprod Dev 78, 861867.
Yakovlev, KV (2016) Localization of germ plasm-related structures during sea urchin oogenesis. Dev Dynam 245, 5666.

Keywords

Germ plasm provides clues on meiosis: the concerted action of germ plasm granules and mitochondria in gametogenesis of the clam Ruditapes philippinarum

  • Arkadiy Reunov (a1) (a2), Yana Alexandrova (a2), Yulia Reunova (a2), Alina Komkova (a2) and Liliana Milani (a3)...

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