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Germ plasm-related structures in marine medaka gametogenesis; novel sites of Vasa localization and the unique mechanism of germ plasm granule arising

Published online by Cambridge University Press:  08 October 2019

Arkadiy A. Reunov Open the ORCID record for Arkadiy A. Reunov [Opens in a new window] ,
Doris W. T. Au ,
Yana N. Alexandrova ,
Michael W. L. Chiang Open the ORCID record for Michael W. L. Chiang [Opens in a new window] ,
Miles T. Wan ,
Konstantin V. Yakovlev ,
Yulia A. Reunova ,
Alina V. Komkova ,
Napo K. M. Cheung  and
Drew R. Peterson
...Show all authors
Arkadiy A. Reunov*
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia St. Francis Xavier University, Department of Biology, Antigonish, NS B2G 2W5, Canada
Doris W. T. Au
Affiliation:
State Key Laboratory of Marine Pollution, Department of Chemistry, City University of Hong Kong, 83 Tat Cher Avenue, Kowloon, Hong Kong
Yana N. Alexandrova
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia
Michael W. L. Chiang
Affiliation:
State Key Laboratory of Marine Pollution, Department of Chemistry, City University of Hong Kong, 83 Tat Cher Avenue, Kowloon, Hong Kong
Miles T. Wan
Affiliation:
State Key Laboratory of Marine Pollution, Department of Chemistry, City University of Hong Kong, 83 Tat Cher Avenue, Kowloon, Hong Kong
Konstantin V. Yakovlev
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia
Yulia A. Reunova
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia
Alina V. Komkova
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia
Napo K. M. Cheung
Affiliation:
State Key Laboratory of Marine Pollution, Department of Chemistry, City University of Hong Kong, 83 Tat Cher Avenue, Kowloon, Hong Kong
Drew R. Peterson
Affiliation:
State Key Laboratory of Marine Pollution, Department of Chemistry, City University of Hong Kong, 83 Tat Cher Avenue, Kowloon, Hong Kong
Andrey V. Adrianov
Affiliation:
National Scientific Centre of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041; Russia Far Eastern Federal University, School of Natural Sciences, 10 Ajax Bay, Russky Island, Vladivostok 690950, Russia
*
Address for correspondence: Arkadiy Reunov. St. Francis Xavier University, Department of Biology, Antigonish, NS B2G 2W5, Canada. E-mail: areunov@stfx.ca
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Summary

Germ plasm, a cytoplasmic factor of germline cell differentiation, is suggested to be a perspective tool for in vitro meiotic differentiation. To discriminate between the: (1) germ plasm-related structures (GPRS) involved in meiosis triggering; and (2) GPRS involved in the germ plasm storage phase, we investigated gametogenesis in the marine medaka Oryzias melastigma. The GPRS of the mitosis-to-meiosis period are similar in males and females. In both sexes, five events typically occur: (1) turning of the primary Vasa-positive germ plasm granules into the Vasa-positive intermitochondrial cement (IMC); (2) aggregation of some mitochondria by IMC followed by arising of mitochondrial clusters; (3) intramitochondrial localization of IMC-originated Vasa; followed by (4) mitochondrial cluster degradation; and (5) intranuclear localization of Vasa followed by this protein entering the nuclei (gonial cells) and synaptonemal complexes (zygotene–pachytene meiotic cells). In post-zygotene/pachytene gametogenesis, the GPRS are sex specific; the Vasa-positive chromatoid bodies are found during spermatogenesis, but oogenesis is characterized by secondary arising of Vasa-positive germ plasm granules followed by secondary formation and degradation of mitochondrial clusters. A complex type of germ plasm generation, ‘the follicle cell assigned germ plasm formation’, was found in late oogenesis. The mechanisms discovered are recommended to be taken into account for possible reconstruction of those under in vitro conditions.

Keywords

Germ plasm formationGerm plasm-related structuresMarine medakaMeiotic differentiationOogenesisSpermatogenesisVasa
Type
Research Article
Information
Zygote , Volume 28 , Issue 1 , February 2020 , pp. 9 - 23
Copyright
© Cambridge University Press 2019 

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References

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, 17–23.CrossRefGoogle Scholar
Amikura, R, Kashikawa, M, Nakamura, A and Kobayashi, S (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. PNAS 98, 9133–8.CrossRefGoogle ScholarPubMed
Amikura, R, Sato, K and Kobayashi, S (2005) Role of mitochondrial ribosome dependent translation in germline formation in Drosophila embryos. Mech Dev 122, 1087–93.CrossRefGoogle ScholarPubMed
Au, DWT, Reunov, AA and Wu, RSS (1998) Four lines of spermatid development and dimorphic spermatozoa in the sea urchin Anthocidaris crassispina (Echinodermata, Echinoidea). Zoomorphology 118, 159–68.Google Scholar
Billard, R (1983) Spermiogenesis in the rainbow trout (Salmo gairdneri); An ultrastructural study. Cell Tissue Res 233, 265–84.CrossRefGoogle Scholar
Billard, R (1984) Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia reticulata during spermatogenesis. Cell Tissue Res 237, 219–26.CrossRefGoogle ScholarPubMed
Bontems, F, Stein, A, Marlow, F, Lyautey, J, Gupta, T, Mullins, MC and Dosch, R (2009) Bucky ball organizes germ plasm assembly in zebrafish. Curr Biol 19, 414–22.CrossRefGoogle ScholarPubMed
Braat, AK, Speksnijder, JE and Zivkovic, D (1999) Germ line development in fishes. Int J Dev Biol 43, 745–60.Google ScholarPubMed
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, 661–70.Google ScholarPubMed
Castrillon, DH, Quade, BJ, Wang, TY, Quigley, C and Crum, CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. PNAS 17, 9585–90.CrossRefGoogle Scholar
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, 4669–81.CrossRefGoogle ScholarPubMed
Chuma, S, Hosokawa, M, Tanaka, T and Nakatsuji, N (2009) Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol Cell Endocrinol 306, 17–23.CrossRefGoogle ScholarPubMed
Cox, RT and Spradling, AC (2003). A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130, 1579–90.CrossRefGoogle ScholarPubMed
Eckelbarger, KJ (2005). Oogenesis and oocytes. Hydrobiologia 535/536, 179–98.Google Scholar
Eddy, EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43, 229–80.CrossRefGoogle ScholarPubMed
Fawcett, DW (1972) Observations on cell differentiation and organelle continuity in spermatogenesis. Proceeding of the Edinburgh Symposium. On the genetics of the spermatozoon. Bogtrykkeriet Forum. Copenhagen, pp. 37–68.Google Scholar
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, 859–71.CrossRefGoogle ScholarPubMed
Flores, JA and Burns, JR (1993) Ultrastructural study of embryonic and early adult germ cells, and their support cells, in both sexes of Xiphophorus (Teleostei: Poeciliidae). Cell Tissue Res 271, 263–70.CrossRefGoogle Scholar
Gur, Y and Breitbart, H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20, 411–6.CrossRefGoogle ScholarPubMed
Gur, Y and Breitbart, H (2008) Protein syntesis in sperm: dialog between mitochondria and cytoplasm. Mol Cell Endocrinol 282, 45–55.CrossRefGoogle Scholar
Gustafson, EA and Wessel, GM (2010) DEAD-box helicases: posttranslational regulation and function. Biochem Biophys Res Commun 395, 1–6.CrossRefGoogle ScholarPubMed
Hamaguchi, S (1982) A light and electron microscopic study of the migration of primordial germ cells in the teleost Oryzias latipes . Cell Tissue Res 227, 139–51.CrossRefGoogle ScholarPubMed
Hamaguchi, S (1985) Changes in the morphology of the germinal dense bodies in primordial germ cells of the teleost Oryzias latipes . Cell Tiss Res 240, 669–73.CrossRefGoogle Scholar
Hartung, O, Forbes, MM and Marlow, FL (2014) Zebrafish Vasa is required for germ-cell differentiation and maintenance. Mol Reprod Dev 81, 946–61.CrossRefGoogle ScholarPubMed
Hay, B, Jan, LY and Jan, YN (1990) Localization of Vasa, a component of Drosophila polar granules, in maternal effect mutants that alter embryonic anteroposterior polarity, Development 109, 425–33.Google ScholarPubMed
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, 285–96.CrossRefGoogle ScholarPubMed
Higaki, S, Shimada, M, Kawamoto, K, Todo, T, Kawasaki, T, Tooyama, I, Fujioka, Y, Sakai, N and Takada, T (2017) In vitro differentiation of fertile sperm from cryopreserved spermatogonia of the endangered endemic cyprinid honmoroco (Gnathopogon caerulescens). Sci Rep 7, 42852.CrossRefGoogle Scholar
Hodgson, AN and Reunov, AA (1994) Ultrastructure of the spermatozoon and spermatogenesis of the brachiopods Discinisca tenuis (Inarticulata) and Kraussina rubra (Articulata). Invert Reprod Dev 25, 23–31.CrossRefGoogle Scholar
Kalt, MR (1973) Ultrastructural observations on the germ line of Xenopus laevis . Z. Zellforsch 138, 41–62.CrossRefGoogle ScholarPubMed
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, 1–11.CrossRefGoogle ScholarPubMed
Kawasaki, T, Saito, K, Shinya, M, Olsen, LC and Sakai, N (2010) Regeneration of spermatogenesis and production of functional sperm by grafting of testicular cell aggregates in zebrafish (Danio rerio). Biol Reprod 83, 533–9.CrossRefGoogle Scholar
Kawasaki, T, Saito, K, Sakai, C, Shinya, M and Sakai, N (2012) Production of zebrafish offspring from cultured spermatogonial stem cells. Genes Cells 17, 316–25.CrossRefGoogle ScholarPubMed
Kawasaki, T, Siegfried, KR and Sakai, N (2016) Differentiation of zebrafish spermatogonial stem cells to functional sperm in culture. Development 143, 566–574.CrossRefGoogle ScholarPubMed
Kerr, JB and Dixon, KE (1974) An ultrastructural study of germ plasm in spermatogenesis of Xenopus laevis . J Embryol Exp Morph 32, 573–92.Google ScholarPubMed
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, 79–93.CrossRefGoogle ScholarPubMed
Knaut, H, Pelegri, F, Bohmann, K, Schwarz, H and Nüsslein-Volhard, C (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J Cell Biol 149, 875–88.CrossRefGoogle Scholar
Kobayashi, T, Kajiura-Kobayashi, H and Nagahama, Y (2000) Differential expression of Vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus . Mech Dev 99, 139–42.CrossRefGoogle Scholar
Lacerda, SM, Costa, GM, and De França, LR (2014) Biology and identity of fish spermatogonial stem cell. Gen Comp Endocrinol 207, 56–65.CrossRefGoogle ScholarPubMed
Lasko, PF and Ashburner, M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611–7.CrossRefGoogle ScholarPubMed
Leal, MC, Cardoso, ER, Nóbrega, RH, Batlouni, SR and Bogerd, J (2009) Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod 81, 177–87.CrossRefGoogle ScholarPubMed
Mahowald, AP (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster . J Exp Zool 151, 201–5.CrossRefGoogle Scholar
Matova, N and Cooley, L (2001). Comparative aspects of animal oogenesis. Dev Biol 231, 291–320.CrossRefGoogle ScholarPubMed
Mattei, C and Mattei, X (1978) La spermiogenese d’un poisson teleosteen (Lepadogaster lepadogaster). I. La spermatide. Biol Cell 32, 257–66.Google Scholar
Medrano, JV, Reijo Pera, RA and Simon, C (2013). Germ cell differentiation from pluripotent cells. Semin Reprod Med 31, 14–23.Google ScholarPubMed
Meikar, O, Ros, MD, Korhonen, H and Kotaja, N (2011) Chromatoid body and small RNAs in male germ cells. Reproduction 142, 195–209.CrossRefGoogle ScholarPubMed
Milani, L, Pecci, A, Ghiselli, F, Passamonti, M, Bettini, S, Franceschini, V and Maurizii, MG (2017) VASA expression suggests shared germ line dynamics in bivalve molluscs. Histochem Cell Biol 148, 157–71.CrossRefGoogle ScholarPubMed
Mochizuki, K, Nishiyama-Fujisawa, C and Fujisawa, T (2001) Universal occurrence of the Vasa-related genes among metazoans and their germline expression in Hydra . Dev Genes 211, 299–308.CrossRefGoogle ScholarPubMed
Moreno, I, Miguez-Forjan, JM and Simon, C (2015) Artificial gametes from stem cells. Clin Exp Reprod Med 42, 33–44.CrossRefGoogle ScholarPubMed
Muñoz, M, Sàbat, M, Mallol, S, Casadevall, M (2002) Gonadal structure and gametogenesis of Trigla lyra (Pisces: Triglidae). Zool Stud 41, 412–20.Google Scholar
Nikolic, A, Volarevic, V, Armstrong, L, Lako, M and Stojkovic, M (2016) Primordial germ cells: current knowledge and perspectives. Stem Cells Int 2016, 1741072.CrossRefGoogle Scholar
Onohara, Y and Yokota, S (2012) Expression of DDX25 in nuage components of mammalian spermatogenic cells: immunofluorescence and immunoelectron microscopic study. Histochem Cell Biol 137, 37–51.CrossRefGoogle ScholarPubMed
Pek, JW and Kai, T (2011). A role for Vasa in regulating mitotic chromosome condensation in Drosophila . Current Biology 21, 39–44.CrossRefGoogle ScholarPubMed
Raz, E (2000) The function and regulation of Vasa-like genes in germ-cell development. Genome Biol 1, 1–6.CrossRefGoogle ScholarPubMed
Reunov, AA and Rice, M (1993) Ultrastructural observations on spermatogenesis in Phascolion cryptum (Sipuncula). Trans Am Microsc Soc 112, 195–207.CrossRefGoogle Scholar
Reunov, AA and Klepal, W (1997) Ultrastructural investigation of spermatogenesis in nemertine worm Procephalothrix sp. (Palaeonemertini, Anopla). Helgoland Meer 51, 125–35.CrossRefGoogle Scholar
Reunov, AA and Klepal, W (2004) Ultrastructural study of spermatogenesis in Phoronopsis harmeri (Lophophorata, Phoronida). Helgol Mar Res 58, 1–10.CrossRefGoogle Scholar
Reunov, AA, Isaeva, VV, Au, DWT and Wu, RSS (2000). Nuage constituents arising from mitochondria: is it possible? Dev Growth Differ 42, 139–43.CrossRefGoogle ScholarPubMed
Reunov, AA, Yurchenko, OV, Alexandrova, YN and Radashevsky, VI (2010) Spermatogenesis in Boccardiella hamata (Polychaeta: Spionidae) from the Sea of Japan: sperm formation mechanisms as characteristics for future taxonomic revision. Acta Zool 91, 447–56.CrossRefGoogle Scholar
Reunov, AA, Alexandrova, YN, Reunova, YA, Komkova, AV and Milani, L (2018) Germ plasm provides clues on meiosis: the concerted action of germ plasm granules and mitochondria in the clam. Zygote 27, 25–35.CrossRefGoogle ScholarPubMed
Riesco, MF, Valcarce, DG, Alfonso, J, Herráez, MP and Robles, V (2014) In vitro generation of zebrafish PGC-like cells. Biol Reprod 91, 1–11.CrossRefGoogle ScholarPubMed
Saffman, EE and Lasko, P (1999). Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55, 1141–63.CrossRefGoogle ScholarPubMed
Sakai, N (2002) Transmeiotic differentiation of zebrafish germ cells into functional sperm in culture. Development 129, 3359–65.Google ScholarPubMed
Satoh, N (1974) An ultrastructural study of sex differentiation in the teleost Oryzias latipes . J Embryol Exp Morphol 32, 195–215.Google ScholarPubMed
Schulz, RW, de França, LR, Lareyre, J-J, LeGac, F, Chiarini-Garcia, H, Nóbrega, RH and Miura, T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165, 390–411.CrossRefGoogle Scholar
Shang, P, Baarends, WM, Hoogerbrugge, J, Ooms, MP, van Cappellen, WA, de Jong, AAW, Dohle, GR, van Eenennaam, H, Gossen, JA and Grootegoed, JA (2010) Functional transformation of the chromatoid body in mouse spermatids requires testis-specific serine/threonine kinases. J Cell Sci 123, 331–9.CrossRefGoogle ScholarPubMed
Strome, S and Wood, WB (1983) Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 11–25.CrossRefGoogle ScholarPubMed
Sunagara, T, Saito, Y and Kawamura, K (2006) Postembryonic epigenesist of Vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian Botryllus primigenus . Dev Growth Differ 48, 87–100.CrossRefGoogle Scholar
Timmermans, LPM and Taverne, N (1989) Segregation of primordial germ cells: their numbers and fate during early development of Barbus conchonius (Cyprinidae, Teleostei) as indicated by 3H-thymidine incorporation. J. Morphol 202, 225–37.CrossRefGoogle Scholar
Toyooka, Y, Tsunekawa, N, Takahashi, Y, Matsui, Y, Satoh, M and Noce, T (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93, 139–49.CrossRefGoogle ScholarPubMed
Tzung, K-W, Goto, R, Saju, JM, Sreenivasan, R, Saito, T, Arai, K, Yamaha, E, Hossain, M., Calvert, MEK and Orbán, L (2014) Early depletion of primordial germ cells in zebrafish promotes testis formation. Stem Cell Rep 4, 61–73.CrossRefGoogle ScholarPubMed
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, 977–83.CrossRefGoogle ScholarPubMed
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, 17–21.CrossRefGoogle Scholar
Williamson, A and Lehmann, R (1996) Germ cell development in Drosophila . Annu Rev Cell Dev Biol 12, 365–91.CrossRefGoogle ScholarPubMed
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, 297–306.Google ScholarPubMed
Xu, H, Gui, J and Hong, Y (2005) Differential expression of Vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Dev Dynam 233, 872–82.CrossRefGoogle Scholar
Yajima, M and Wessel, GM (2011) The multiple hats of Vasa function and its regulation of cell cycle progression. Mol Reprod Dev 78, 861–7.CrossRefGoogle Scholar
Yakovlev, KV (2016) Localization of germ plasm-related structures during sea urchin oogenesis. Dev Dynam 245, 56–66.CrossRefGoogle ScholarPubMed
Yuan, Y, Li, M and Hong, Y (2014) Light and electron microscopic analyses of Vasa expression in adult germ cells of the fish medaka. Gene 545, 15–22.CrossRefGoogle ScholarPubMed