Abstract
Rare minnow (Gobiocypris rarus) is an emerging model fish in China, and the development of its gonads is still elusive. Germ cell-specific genes are conserved in animals. Dead end (Dnd) was first documented as a germ granule component in zebrafish. Here, we report the cloning and expression profile of dnd in rare minnow. RT-PCR results showed that dnd is expressed specifically in the gonads of both sexes, is maternal in origin and is expressed continuously during embryogenesis. Dnd mRNA could be detected exclusively in the germ cells of the testis and ovary. Temporal expression of dnd mRNA is similar to that of vasa and dnd in zebrafish during embryogenesis. Taken together, dnd mRNA is restricted to the germ cells of rare minnow.
Similar content being viewed by others
Abbreviations
- AA:
-
Amino acids
- BCIP:
-
5-bromo-4-chloro-3-indolyl phosphate
- bp:
-
Base pairs
- cDNA:
-
Complementary DNA
- DIG:
-
Digoxigenin
- dnd :
-
dead end
- DSRM:
-
Double-stranded RNA recognition motif
- hpf:
-
Hours post-fertilization
- LATS2:
-
Large tumor suppressor kinase 2
- NBT:
-
Nitroblue tetrazolium
- ORF:
-
Open reading frame
- PBS:
-
Phosphate buffered saline
- PCR:
-
Polymerase chain reaction
- PGC:
-
Primordial germ cell
- RACE:
-
Rapid amplification of cDNA ends
- RBD:
-
RNA-binding domain
- RNP:
-
Ribonucleoprotein domain
- RRM:
-
RNA recognition motifs
- RT-PCR:
-
Reverse transcription polymerase chain reaction
- UTR:
-
Untranslated region
References
Aramaki S, Kubota K, Soh T, Yamauchi N, Hattori MA (2009) Chicken dead end homologue protein is a nucleoprotein of germ cells including primordial germ cells. J Reprod Dev 55:214–218
Bhattacharya C, Aggarwal S, Zhu R, Kumar M, Zhao M, Meistrich ML, Matin A (2007) The mouse dead-end gene isoform alpha is necessary for germ cell and embryonic viability. Biochem Biophys Res Commun 355:194–199
Birney E, Kumar S, Krainer AR (1993) Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res 21:5803–5816
Braat AK, van de Water S, Goos H, Bogerd J, Zivkovic D (2000) Vasa protein expression and localization in the zebrafish. Mech Dev 95:271–274
Cao M, Yang Y, Xu H, Duan J, Cheng N, Wang J, Hu W, Zhao H (2012) Germ cell specific expression of Vasa in rare minnow, Gobiocypris rarus. Comp Biochem Physiol A Mol Integr Physiol 162:163–170
Chen S, Zeng M, Sun H, Deng W, Lu Y, Tao D, Liu Y, Zhang S, Ma Y (2010) Zebrafish Dnd protein binds to 3′UTR of geminin mRNA and regulates its expression. BMB Rep 43:438–444
Fujimoto T, Nishimura T, Goto-Kazeto R, Kawakami Y, Yamaha E, Arai K (2010) Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish. Proc Natl Acad Sci USA 107:17211–17216
Hashimoto Y, Maegawa S, Nagai T, Yamaha E, Suzuki H, Yasuda K, Inouea K (2004) Localized maternal factors are required for zebrafish germ cell formation. Dev Biol 268:152–161
Herpin A, Rohr S, Riedel D, Kluever N, Raz E, Schartl M (2007) Specification of primordial germ cells in medaka (Oryzias latipes). BMC Dev Biol 7:3
Horvay K, Claussen M, Katzer M, Landgrebe J, Pieler T (2006) Xenopus dead end mRNA is a localized maternal determinant that serves a conserved function in germ cell development. Dev Biol 291:1–11
Houston DW, King ML (2000) Germ plasm and molecular determinants of germ cell fate. Curr Top Dev Biol 50:155–181
Jiang W, Yang Y, Zhao D, Liu X, Duan J, Xie S, Zhao H (2011) Effects of sexual steroids on the expression of foxl2 in Gobiocypris rarus. Comp Biochem Physiol B Biochem Mol Biol 160:187–193
Kedde M, Strasser MJ, Boldajipour B, Vrielink JAO, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Ørom UA, Lund AH, Perrakis A, Raz E, Agami R (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131:1273–1286
Knaut H, Pelegri F, Bohmann K, Schwarz H, 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 149:875–888
Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, Korving JP, Hogan BL (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436
Liang L, Diehl-Jones W, Lasko PF (1994) Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120:1201–1211
Lin F, Zhao CY, Xu SH, Ma DY, Xiao ZZ, Xiao YS, Xu CA, Liu QH, Li J (2013) Germline-specific and sexually dimorphic expression of a dead end gene homologue in turbot (Scophthalmus maximus). Theriogenology 80:665–672
Liu W, Collodi P (2010) Zebrafish dead end possesses ATPase activity that is required for primordial germ cell development. FASEB J 24:2641–2650
Liu L, Hong N, Xu H, Li M, Yan Y, Purwanti Y, Yi M, Li Z, Wang L, Hong Y (2009) Medaka dead end encodes a cytoplasmic protein and identifies embryonic and adult germ cells. Gene Expr Patterns 9:541–548
Mei W, Jin Z, Lai F, Schwend T, Houston DW, King ML, Yang J (2013) Maternal Dead-End1 is required for vegetal cortical microtubule assembly during Xenopus axis specification. Development 140:2334–2344
Miyake A, Saito T, Kashiwagi T, Ando D, Yamamoto A, Suzuki T, Nakatsuji N, Nakatsuji T (2006) Cloning and pattern of expression of the shiro-uo vasa gene during embryogenesis and its roles in PGC development. Int J Dev Biol 50:619–625
Otani S, Maegawa S, Inoue K, Arai K, Yamaha E (2002) The germ cell lineage identified by vas-mRNA during the embryogenesis in goldfish. Zool Sci 19:519–526
Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55:1141–1163
Saito T, Otani S, Fujimoto T, Suzuki T, Nakatsuji T, Arai K, Yamaha E (2004) The germ line lineage in ukigori, Gymnogobius species (Teleostei: Gobiidae) during embryonic development. Int J Dev Biol 48:1079–1085
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Wang J, Liu X, Wang H, Wu T, Hu X, Qin F, Wang Z (2010) Expression of two cytochrome P450 aromatase genes is regulated by endocrine disrupting chemicals in rare minnow Gobiocypris rarus juveniles. Comp Biochem Physiol C Toxicol Pharmacol 152:313–320
Weidinger G, Stebler J, Slanchev K, Dumstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E (2003) dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429–1434
Wu WZ, Li W, Xu Y, Wang JW (2001) Long-term toxic impact of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the reproduction, sexual differentiation, and development of different life stages of Gobiocypris rarus and Daphnia magna. Ecotoxicol Environ Saf 48:293–300
Wylie C (1999) Germ cells. Cell 96:165–174
Ying Y, Qi X, Zhao GQ (2001) Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci U S A 98:7858–7862
Youngren KK, Coveney D, Peng X, Bhattacharya C, Schmidt LS, Nickerson ML, Lamb BT, Deng JM, Behringer RR, Capel B, Rubin EM, Nadeau JH, Matin A (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435:360–364
Zhao H, Guan G, Duan J, Cheng N, Wang J, Matsuda M, Paul-Prasanth B, Nagahama Y (2013) Ol4E-T, a eukaryotic translation initiation factor 4E- binding protein of Medaka fish (Oryzias latipes), can interact with Nanos3 and Vasa in vitro. J Exp Zool B Mol Dev Evol 320:10–21
Zhong X, Xu Y, Liang Y, Liao T, Wang J (2004) Vitellogenin in rare minnow (Gobiocypris rarus): identification and induction by waterborne diethylstilbestrol. Comp Biochem Physiol C Toxicol Pharmacol 137:291–298
Acknowledgments
This work was supported by Natural Science Foundation of China (Grant # 31272645 to HZ), the Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences (to HZ).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Duan, J., Feng, G., Chang, P. et al. Germ cell-specific expression of dead end (dnd) in rare minnow (Gobiocypris rarus). Fish Physiol Biochem 41, 561–571 (2015). https://doi.org/10.1007/s10695-015-0029-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-015-0029-x