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Molecular cloning, characterization and evolutionary analysis of vitellogenin in Chinese giant salamander Andrias davidianus

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Abstract

Vitellogenin (VTG) is the major precursor of yolk proteins and could transport many components into oocytes, and hence it was thought to be a potential marker of reproduction of oviparious animal. Andrias davidianus is a critically endangered amphibian species, of which the wild population decreased dramatically and the artificial breeding has been successfully established. In this study, a full-length VTG cDNA was cloned and characterized from A. davidianus (designated as AdVTG) using 5′ and 3′ rapid amplification cDNA ends and RT-PCR. The AdVTG cDNA is 5,418 base pair in length and it encodes 1,805 amino acid long protein with typical quadripartite domains and several conserved cleavage sites. The tissue expression pattern indicated that AdVTG is mainly expressed in liver in one-year old individual. The three-dimensional model of AdVTG constructed by homology modelling revealed the presence of conserved N-terminal β-sheet and lipid-binding cavity. Moreover, the phylogenetic analysis of VTG in metazoa was carried out, which revealed that Anura-specific gene duplication occurred after the divergence of Caudata. All these results would improve the understanding of the physiological roles of AdVTG in A. davidianus and contribute to elucidating the evolution of VTG in vertebrates.

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Abbreviations

MCMCMC:

Metropolis-coupled Markov chain Monte Carlo

PDB:

Protein Data Bank

RACE:

rapid amplification cDNA ends

SDS-PAGE:

sodium dodecyl sulfate polyacrylamide gel electrophoresis

VTG:

vitellogenin

VWD:

von Willebrand factor type D domain

WGD:

whole genome duplication

References

  • Almenara D.P., de Moura J.P., Scarabotto C.P., Zingali R.B. & Winter C.E. 2013. The molecular and structural characterization of two vitellogenins from the free-living nematode Oscheius tipulae. PLoS One 8: e53460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W. & Lipman D.J. 1997. Nucleic Acids Res. 25: 3389–3402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babin P.J. 2008. Conservation of a vitellogenin gene cluster in oviparous vertebrates and identification of its traces in the platypus genome. Gene 413: 76–82.

    Article  CAS  PubMed  Google Scholar 

  • Beiko R.G. 2011. Telling the whole story in a 10,000-genome world. Biol. Direct. 6: 34.

    Article  PubMed  PubMed Central  Google Scholar 

  • Biasini M., Bienert S., Waterhouse A., Arnold K., Studer G., Schmidt T., Kiefer F., Cassarino T.G., Bertoni M., Bordoli L. & Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42(Web Server Issue): W252–W258.

    Google Scholar 

  • Benson D.A., Clark K., Karsch-Mizrachi I., Lipman D.J., Ostell J. & Sayers E.W. 2014. GenBank. Nucleic Acids Res. 42: D32–D37.

    Article  CAS  PubMed  Google Scholar 

  • Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N. & Bourne P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canapa A., Olmo E., Forconi M., Pallavicini A., Makapedua M.D., Biscotti M.A. & Barucca M. 2012. Composition and phylogenetic analysis of vitellogenin coding sequences in the Indonesian coelacanth Latimeria menadoensis. J. Exp. Zool. (Mol. Dev. Evol.) 318B: 404–416.

    Article  CAS  Google Scholar 

  • Cayrol C. & Deparis P. 1986. Identification of the vitellogenin proteins in the newt Pleurodeles waltl (Urodele amphibian). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 83: 135–142.

    Article  CAS  Google Scholar 

  • Cerda J., Fabra M. & Raldua D. 2007. Physiological and molecular basis of fish oocyte hydration, pp. 349–396. In: Babin P.J., Cerda J. & Lubzens E. (eds) The Fish Oocyte, Springer, Netherlands.

  • Currylow A.F., Tift M.S., Meyer J.L., Crocker D.E. & Williams R.N. 2013. Seasonal variations in plasma vitellogenin and sex steroids in male and female Eastern Box Turtles, Terrapene carolina carolina. Gen. Comp. Endocrinol. 180: 48–55.

    Article  CAS  PubMed  Google Scholar 

  • Davis L.K., Hiramatsu N., Hiramatsu K., Reading B.J., Matsub-ara T., Hara A., Sullivan C.V., Pierce A.L., Hirano T. & Grau E.G. 2007. Induction of three vitellogenins by 17β-estradiol with concurrent inhibition of the growth hormone-insulin-like growth factor 1 axis in a euryhaline teleost, the tilapia (Oreochromis mossambicus). Biol. Reprod. 77: 614–625.

    Article  CAS  PubMed  Google Scholar 

  • Evans M.I., Silva R. & Burch J.B. 1988. Isolation of chicken vitel-logenin I and III cDNAs and the developmental regulation of five estrogen-responsive genes in the embryonic liver. Genes Dev. 2: 116–124.

    Article  CAS  PubMed  Google Scholar 

  • Finn R.D., Bateman A., Clements J., Coggill P., Eberhardt R.Y., Eddy S.R., Heger A., Hetherington K., Holm L., Mistry J., Sonnhammer E.L., Tate J. & Punta M. 2014. Pfam: the protein families database. Nucleic Acids Res. 42: D222–D230.

    Article  CAS  PubMed  Google Scholar 

  • Finn R.N. 2007. Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitel-logenins. Biol. Reprod. 76: 926–935.

    Article  CAS  PubMed  Google Scholar 

  • Finn R.N., Kolarevic J., Kongshaug H. & Nilsen F. 2009. Evolution and differential expression of a vertebrate vitellogenin gene cluster. BMC Evol. Biol. 9: 2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Finn R.N. & Kristoffersen B.A. 2007. Vertebrate vitellogenin gene duplication in relation to the “3R hypothesis”: correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2: e169.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia J., Munro E.S., Monte M.M., Fourrier M.C., Whitelaw J., Smail D.A. & Ellis A.E. 2010. Atlantic salmon (Salmo salar L.) serum vitellogenin neutralises infectivity of infectious pancreatic necrosis virus (IPNV). Fish Shellfish Immunol. 29: 293–297.

    Article  CAS  PubMed  Google Scholar 

  • Guex N. & Peitsch M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714–2723.

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa H., Andoh T. & Watanabe T. 2006. Precursor structure of egg proteins in the coral Galaxea fascicularis. Biochem. Biophys. Res. Commun. 344: 173–180.

    Article  CAS  PubMed  Google Scholar 

  • Hayward A., Takahashi T., Bendena W.G., Tobe S.S. & Hui J.H. 2010. Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in meta-zoans. FEBS Lett. 584: 1273–1278.

    Article  CAS  PubMed  Google Scholar 

  • Irie T. & Seki T. 2002. Retinoid composition and retinal localization in the eggs of teleost fishes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131: 209–219.

    Article  PubMed  Google Scholar 

  • Jia X., Chen Y., Zou Z., Lin P., Wang Y. & Zhang Z. 2013. Characterization and expression profile of vitellogenin gene from Scylla paramamosain. Gene 520: 119–30.

    Article  CAS  PubMed  Google Scholar 

  • Kohn Y.Y., Lokman P.M., Kilimnik A. & Symonds J.E. 2013. Sex identification in captive hapuku (Polyprion oxygeneios) using ultrasound imagery and plasma levels of vitellogenin and sex steroids. Aquaculture 384: 87–93.

    Article  CAS  Google Scholar 

  • Kung S.Y., Chan S.M., Hui J.H.L., Tsang W.S., Mak A. & He J.G. 2004. Vitellogenesis in the sand shrimp, Metapenaeus ensis: the contribution from the hepatopancreas-specific vitel-logenin gene (MeVg2). Biol. Reprod. 71: 863–870.

    Article  CAS  PubMed  Google Scholar 

  • Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R. & Thornton J.M. 1996. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8: 477–486.

    Article  CAS  PubMed  Google Scholar 

  • Levi L., Ziv T., Admon A., Levavi-Sivan B. & Lubzens E. 2012. Insight into molecular pathways of retinal metabolism, associated with vitellogenesis in zebrafish. Am. J. Physiol. En-docrinol. Metab. 302: E626–E644.

    CAS  Google Scholar 

  • Li A., Sadasivam M., & Ding J.L. 2003. Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E. The first three ligand-binding repeats of VtgR interact with the amino-terminal region of Vtg. J. Biol. Chem. 278: 2799–2806.

    Article  CAS  PubMed  Google Scholar 

  • Liu Q.H., Zhang S.C., Li Z.J. & Gao C.R. 2009. Characterization of a pattern recognition molecule vitellogenin from carp (Cyprinus carpio). Immunobiology 214: 257–267.

    Article  CAS  PubMed  Google Scholar 

  • Lu X. & Rasco B.A. 2013. Sturgeon (Acipenser transmontanus) sexual maturation and caviar quality. Aquaculture 6: 89–99.

    Article  Google Scholar 

  • Matsubara T., Nagae M., Ohkubo N., Andoh T., Sawaguchi S., Hiramatsu N., Sullivan C.V. & Hara A. 2003. Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol. Biochem. 28: 295–299.

    Article  CAS  Google Scholar 

  • Nakamura A., Yasuda K., Adachi H., Sakurai Y., Ishii N. & Goto S. 1999. Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 264: 580–583.

    Article  CAS  PubMed  Google Scholar 

  • Nelson C., Ihle K., Fondrk M., Page R.J. & Amdam G. 2007. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5: e62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olmstead A.W., Korte J.J., Woodis K.K., Bennett B.A., Ostazeski S. & Degitz S.J. 2009. Reproductive maturation of the tropical clawed frog: Xenopus tropicalis. Gen. Comp. Endocrinol. 160: 117–123.

    Article  CAS  PubMed  Google Scholar 

  • Price M.N., Dehal P.S. & Arkin A.P. 2010. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prowse T. A. & Byrne M. 2012. Evolution of yolk protein genes in the Echinodermata. Evol. Dev. 14: 139–151.

    Article  CAS  PubMed  Google Scholar 

  • Ren J., Wen L., Gao X., Jin C., Xue Y. & Yao X. 2009. DOG 1.0: illustrator of protein domain structures. Cell Res. 19: 271–273.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: bayesian phy-logenetic inference under mixed models. Bioinformatics 19: 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Roure B., Rodriguez-Ezpeleta N. & Philippe H. 2007. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol. 7 (Suppl. 1): S2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seehuus S.C., Norberg K., Gimsa U., Krekling T. & Amdam G.V. 2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA 103: 962–967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X.D., Zhang S.C. & Pang Q.X. 2006. Vitellogenin is a novel player in defense reactions. Fish Shellfish Immunol. 20: 769–772.

    Article  CAS  PubMed  Google Scholar 

  • Singh N.K., Pakkianathan B.C., Kumar M., Prasad T., Kannan M., Konig S. & Krishnan M. 2013 Vitellogenin from the silkworm, Bombyx mori: an effective anti-bacterial agent. PLoS One 8: e73005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun C., Hu L., Liu S., Hu G. & Zhang S. 2013. Antiviral activity of phosvitin from zebrafish Danio rerio. Dev. Comp. Immunol. 40: 28–34.

    Article  CAS  PubMed  Google Scholar 

  • Thompson J.R. & Banaszak L.J. 2002. Lipid-protein interactions in lipovitellin. Biochemistry 41: 9398–9409.

    Article  CAS  PubMed  Google Scholar 

  • Tingaud-Sequeira A., Knoll-Gellida A., Andre M. & Babin P.J. 2012. Vitellogenin expression in white adipose tissue in female teleost fish. Biol. Reprod. 86: 38.

    Article  PubMed  CAS  Google Scholar 

  • Tong Z., Li L., Pawar R. & Zhang S.C. 2010. Vitellogenin is an acute phase protein with bacterial-binding and inhibiting activities. Immunobiology 215: 898–902.

    Article  CAS  PubMed  Google Scholar 

  • Wahli W., Dawid I.B., Ryffel G.U. & Weber R. 1981. Vitellogen-esis and the vitellogenin gene family. Science 212: 298–304.

    Article  CAS  PubMed  Google Scholar 

  • Wang H., Tan J.T., Emelyanov A., Korzh V. & Gong Z. 2005. Hepatic and extrahepatic expression of vitellogenin genes in the zebrafish. Danio rerio. Gene 356: 91–100.

    Article  CAS  PubMed  Google Scholar 

  • Wu L.T., Hui J.H. & Chu K.H. 2013. Origin and evolution of yolk proteins: expansion and functional diversification of large lipid transfer protein superfamily. Biol. Reprod. 88: 102.

    PubMed  Google Scholar 

  • Xiao H.B., Liu J.Y., Yang Y.Q. & Lin X.Z. 2006. Artificial propagation of tank-cultured chinese giant salamander (Andrias davidianus). Acta Hydrobiologica Sinica 30: 530–534. (In Chinese)

    Google Scholar 

  • Zhang K.J., Wang X.M., Wu W., Wang Z.H. & Huang S. 2002. Advances in conservation biology of Chinese giant salamander. Biodiversity Science 10: 291–297. (In Chinese)

    Google Scholar 

  • Zhang P., Chen Y.Q., Liu Y.F., Zhou H. & Qu L.H. 2003. The complete mitochondrial genome of the Chinese giant salamander, Andrias davidianus (Amphibia: Caudata). Gene 311: 93–98.

    Article  CAS  PubMed  Google Scholar 

  • Ziv T., Gattegno T., Chapovetsky V., Wolf H., Barnea E., Lubzens E. & Admon A. 2008. Comparative proteomics of the developing fish (zebrafish and gilthead seabream) oocytes. Comp. Biochem. Physiol. D Genomics Proteomics 3: 12–35.

    Article  PubMed  CAS  Google Scholar 

  • Zmora N., Trant J., Chan S.M. & Chung J.S. 2007. Vitellogenin and its messenger RNA during ovarian development in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biol. Reprod. 77: 138–146.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work is supported by the Special Fund for Agroscientific Research in the Public Interest (201203086), the foundation of Director of Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences (SZ2012-02), and the National Nonprofit Institute Research Grant of Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences (2015JBFM40). We also thank the constructive comments and suggestions of the anonymous referees that improved this manuscript.

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Correspondence to Han-bing Xiao.

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Tian, Hf., Meng, Y., Hu, Qm. et al. Molecular cloning, characterization and evolutionary analysis of vitellogenin in Chinese giant salamander Andrias davidianus. Biologia 70, 1254–1262 (2015). https://doi.org/10.1515/biolog-2015-0143

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