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Presence of the matrix metalloproteinases during the migration of the primordial germ cells in zebrafish gonadal ridge

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Abstract

In vertebrates, the primordial germ cells (PGCs) differentiate from extragonadal regions, migrating to gonadal ridge during the embryonic development. However, recent studies in mammals indicate that the PGCs originate from the epiblast and subsequently migrate into the yolk sac. Cell and molecular bases involved in routes during the migration of these cells are still not well understood. Thus, in an attempt to evaluate the participation of matrix metalloproteinases (MMPs) during the gonadal primordium formation in Danio rerio (zebrafish), the route of migration of PGCs was analyzed. In zebrafish, during the migration of the PGCs to the forming gonad, they bind by cytoplasmic processes to the extracellular matrix and migrate through amoeboid movements until they reach the gonadal ridge. During the epiboly, MMPs were not detected. However, after organogenesis, three MMP types were expressed in the somatic cells that were located ahead of the PGCs in the migration route. This expression was maintained throughout the mesentery and was not detected in the PGCs. Upon reaching the gonadal ridge, the PGCs and somatic cells express MMPs and epithelium begins to be formed. After the formation of the basement membrane, the germinal epithelium is delineated by the somatic cells, which remodeling the extracellular matrix. So, a PGC organization occurs through the tissue, forming the gonadal primordium. Concomitantly, granulocytes expressing different MMPs are present. This data in exposing the role of MMPs during the PGC migration to the forming gonad, may point a new way in understanding the reproductive biology of the vertebrates in general.

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References

  • Bendel-Stenzel MR, Gomperts M, Anderson R, Heasman J, Wylie C (2000) The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91:143–152

    CAS  PubMed  Google Scholar 

  • Blaser H, Reicman-Fried M, Castanon I, Dumstrei K, Marlow FL, Kawakami K, Solnica-Kreze L, Heisenberg CP, Raz E (2006) Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 11:613–627

    CAS  PubMed  Google Scholar 

  • Braat AK, Speksnijder JE, Zivkovic D (1999a) Germ line development in fishes. Int J Dev Biol 43:45–760

    Google Scholar 

  • Braat AK, Zandbergen T, Van De Water S, Goos HJ, Zivkovic D (1999b) Characterization of Zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dynam 216:153–167

    CAS  Google Scholar 

  • Carvalho L, Heisenberg CP (2010) The yolk syncytial layer in early zebrafish development. Trends Cell Biol 20:586–592

    CAS  PubMed  Google Scholar 

  • Çek Ş (2006) Early gonadal development and sex differentiation in rosy barb (Puntius conchonius). Anim Biol 56(3):335–350

    Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    CAS  Google Scholar 

  • Di Carlo A, De Felici M (2000) A role for E-cadherin in mouse primordial germ cell development. Dev Biol 226:209–219

    PubMed  Google Scholar 

  • Díez-Torre A, Díaz-Núñez M, Eguizabal C, Silvan U, Arechaga J (2013) Evidence for a role of matrix metalloproteinases and their inhibitors in primordial germ cell migration. Andrology 1(5):779–786

    PubMed  Google Scholar 

  • Foyle TP (1993) A histological description of gonadal development and sex differentiation in the salmon (Oncorhynchus kisutch) for both untreated and estradiol immersed fry. J Fish Biol 42:699–712

    CAS  Google Scholar 

  • Fujimoto T, Miayayama T, Fujita M (1977) The origin, migration and fine morphology of human primordial germ cells. Anat Rec 188:315–330

    CAS  PubMed  Google Scholar 

  • García-Castro M, Anderson R, Heasman J, Wylie C (1997) Interactions between germ cells and extracellular matrix glycoproteins during migration and gonad assembly in the mouse embryo. J Cell Biol 138:471–480

    PubMed  PubMed Central  Google Scholar 

  • Gevers P, Timmermans LPM (1991) Dye-coupling and the formation and fate of the hypoblast in the teleost fish embryo, Barbus conchonius. Development 112:431–438

    CAS  PubMed  Google Scholar 

  • Gevers P, Dulos J, Schipper H, Timmermans LPM (1992) Origin of primordial germ cells, as characterized by the presence of nuage in embryos of the teleost fish Barbus conchonius. Eur J Morphol 30:195–204

    CAS  PubMed  Google Scholar 

  • Gilbert SF, Barresi MJF (2016) Developmental biology, 11th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Gomperts M, Garcia-Castro M, Wylie C, Heasman J (1994) Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135–141

    CAS  PubMed  Google Scholar 

  • Hamaguchi S (1982) A light- and electron-microscopic study on the migration of primordial germ cells in the teleost, Oryzias latipes. Cell Tissue Res 227:139–151

    CAS  PubMed  Google Scholar 

  • Heasman J, Wylie CC (1981) Contact relations and guidance of primordial germ cells on their migratory route in embryos of Xenopus laevis. Proc R Soc Lond Series B Biol Sci 213:41–58

    CAS  Google Scholar 

  • Ho RK (1992) Cell movements and cell fate during zebrafish gastrulation. Development 116(Supp):65–73

    Google Scholar 

  • Howe K, Clark MD, Stemple DL (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hulboy DL, Rudolph LA, Matrisian LM (1997) Matrix metalloproteinases as mediators of reproductive function. Mol Hum Reprod 3:27–45

    CAS  PubMed  Google Scholar 

  • Jaglarz MK, Howard KR (1994) Primordial germ cell migration in Drosophila melanogaster is controlled by somatic tissue. Development 120:83–89

    CAS  PubMed  Google Scholar 

  • Janssens E, Gaublomme D, De Groef L, Darras VM, Arckens L, Delorme N, Claes F, Hove IV, Moons L (2013) Matrix metalloproteinase 14 in the zebrafish: an eye on retinal and retinotectal development. PLoS One 8:e52915

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jia R, Nie L-W, Wang N, Wang J (2009) Molecular cloning and expression patterns of the Vasa gene from Rana nigromaculata (Amphibia: Anura). Zoologia 26:316–322

    Google Scholar 

  • Johanson Z, Underwood C, Richter M (2019) Evolution and development of fishes. Cambridge University Press, New York, USA

    Google Scholar 

  • Khokha R, Murthy A, Weiss A (2013) Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol 13:649–665

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (2000) Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis of a teleost fish, tilapia, Oreochromis niloticus. Mech Develop 99:139–142

    CAS  Google Scholar 

  • Kunz YW (2004) Developmental biology of teleost fishes. Springer, Dordrecht

    Google Scholar 

  • Kurilo LF (1981) Oogenesis in antenatal development in man. Hum Genet 57:86–92

    CAS  PubMed  Google Scholar 

  • Lawson KA, Dunn NR, Roelen BA, Zeinstra L, Davis AM, Wright CVE, Korving JPWFM, Hogan BLM (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ledda S, Bogliolo L, Bebbere D, Ariu F, Pirino S (2010) Characterization, isolation and culture of primordial germ cells in domestic animals: recente progress and insights from the ovine species. Theriogenology 74:534–543

    CAS  PubMed  Google Scholar 

  • Li M, Hong N, Xu H, Yi M, Li C, Gui J, Hong Y (2009) Medaka vasa is required for migration but not survival of primordial germ cells. Mech Dev 126:366–381

    CAS  PubMed  Google Scholar 

  • Mazzoni TS, Quagio-Grassiotto I (2020) In totum immunostaining: a histological analysis tool for small dimensions biological samples. Int J Biol Med Res 11(1):6938–6943

    Google Scholar 

  • Mazzoni TS, Grier HJ, Quagio-Grassiotto I (2010) Germline cysts and the formation of the germinal epithelium during the female gonadal morphogenesis in Cyprinus carpio (Teleostei: Ostariophysi). Anat Rec 293:1581–1606

    Google Scholar 

  • Mazzoni TS, Grier HJ, Quagio-Grassiotto I (2014) Male gonadal differentiation and the paedomorphic evolution of the testis in Teleostei. Anat Rec 297:1137–1162

    Google Scholar 

  • Mazzoni TS, Lo Nostro FL, Antoneli FN, Quagio-Grassiotto I (2018) Action of the metalloproteinases in gonadal remodeling during sex reversal in the sequential hermaphroditism of the teleostei fish Synbranchus marmoratus (Synbranchiformes: Synbranchidae). Cells 7:34–60

    PubMed Central  Google Scholar 

  • Molyneaux K, Wylie C (2004) Primordial germ cell migration. Int J Dev Biol 48:537–544

    CAS  PubMed  Google Scholar 

  • Nakamura M, Takahashi H, Hiroi O (1974) Sex differentiation in the masu salmon (Oncorhynchus masou). Sci Rep Hokkaido Salmon Hatchery 28:1–8

    Google Scholar 

  • Nakamura M, Kobayashi T, Chang XT, Nagahama Y (1998) Gonadal sex differentiation in teleost fish. J Exp Zool 281:362–372

    Google Scholar 

  • Otani S, Kitauchi T, Saito T, Sakao S, Maegawa S, Inoue K, Yamaha E (2005) The formation of primordial germ cells from germline cells in spherical embryos derived from the blastodisc of 2-cell embryos in goldfish, Carassius auratus. Int J Dev Biol 49:843–850

    PubMed  Google Scholar 

  • Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8:221–233

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paluch EK, Raz E (2013) The role and regulation of blebs in cell migration. Curr Opin Cell Biol 25:582–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patiño R, Takashima F (1995) Gonads. In: Takashima F, Hibiya T (eds) An atlas of fish histology: normal and pathological features, 2nd edn. Gustav Fisher, Tokyo Kodansha Stuttgart, pp 128–153

    Google Scholar 

  • Quintero-Hunter I, Grier H, Muscato M (1991) Enhancement of histological detail using metanil yellow as counterstain in periodic acid/Schiff’s hematoxylin staining of glycol methacrylate tissue sections. Biotech Histochem 66:169–172

    CAS  PubMed  Google Scholar 

  • Reichman-Fried M, Minina S, Raz E (2004) Autonomous modes of behavior in primordial germ cell migration. Dev Cell 6:589–596

    CAS  PubMed  Google Scholar 

  • Ricci JM, Martinez ER, Butzge AJ, Doretto LB, Oliveira MA, Bombardelli RA, Bogerd J, Nóbrega RH (2018) Characterization of vasa homolog in a neotropical catfish, Jundiá (Rhamdia quelen): molecular cloning and expression analysis during embryonic and larval development. Gene 654:116–126

    CAS  PubMed  Google Scholar 

  • Richardson E, Lehmann R (2010) Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11:37–49

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santana JCO, Quagio-Grassiotto I (2014) Extracellular matrix remodeling of the testes through the male reproductive cycle in Teleostei fish. Fish Physiol Biochem 40:1863–1875

    CAS  PubMed  Google Scholar 

  • Schoenwolf GC, Bleyl SB, Brauer PR, Francis-West PH (2014) Larsen’s human embryology, 5th, Elsevier edn, Churchill Livingstone

  • Solnica-Krezel L (2005) Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15:R213–R228

    CAS  PubMed  Google Scholar 

  • Starz-Gaiano M, Lehmann R (2001) Moving towards the next generation. Mech Dev 105:5–18

    CAS  PubMed  Google Scholar 

  • Uchida D, Yamashita M, Kitano T, Iguchi T (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205:711–718

    PubMed  Google Scholar 

  • Warga RM, Kimmel CB (1990) Cell movements during epiboly and gastrulation in zebrafish. Development 108:569–580

    CAS  PubMed  Google Scholar 

  • Weidinger G, Wolke U, Köprunner M, Thisse C, Thisse B, Raz E (2002) Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target. Development 129:25–36

    CAS  PubMed  Google Scholar 

  • Wolpert L, Tickle C, Arias AM (2015) Principles of development. Oxford University Press, USA

    Google Scholar 

  • Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, Saitou M (2006) Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol Reprod 75:705–716

    CAS  PubMed  Google Scholar 

  • Yamamoto K (1982) Periblast in the egg of the eel, Anguilla japonica. Japan J Ichthyol 28:423–430

    Google Scholar 

  • Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3166

    CAS  PubMed  Google Scholar 

Download references

Funding

This study was funded by the Brazilian Agency FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo—process number: 2014/00868-3 and 2015/16358-7).

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  1. Department of Cell and Development Biology, Institute of Biomedical Sciences, Federal University of Alfenas (UNIFAL-MG), Gabriel Monteiro da Silva 700, Alfenas, MG, 37130-001, Brazil

    Talita Sarah Mazzoni

  2. Department of Morphology, Botucatu Biosciences Institute, State University of São Paulo (UNESP), Prof. Dr. Antonio Celso Wagner Zanin 250, Botucatu, SP, 18618-689, Brazil

    Talita Sarah Mazzoni & Irani Quagio-Grassiotto

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  1. Talita Sarah Mazzoni
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Correspondence to Irani Quagio-Grassiotto.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Ethics Committee on Animal Experimentation of the Institute of Biosciences of Botucatu—number 580-IBB-UNESP.

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Mazzoni, T.S., Quagio-Grassiotto, I. Presence of the matrix metalloproteinases during the migration of the primordial germ cells in zebrafish gonadal ridge. Cell Tissue Res 383, 707–722 (2021). https://doi.org/10.1007/s00441-020-03288-5

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