Fish Physiology and Biochemistry

, Volume 43, Issue 5, pp 1289–1298 | Cite as

Characterization of a low-density lipoprotein receptor, Lrp13, in Chinese tongue sole (Cynoglossus semilaevis) and medaka (Oryzias latipes)

  • Na WangEmail author
  • Ruoqing Wang
  • Qiaomu Hu
  • Wenteng Xu
  • Ying Zhu
  • Fang Yan
  • Songlin ChenEmail author


As an important economic marine species cultured in China, Chinese tongue sole (Cynoglossus semilaevis) has interested us due to its sexual dimorphism and ZW/ZZ sex determination system. In a previous study, dmrt1 was identified as a dosage-dependent male-determining gene. In the present study, a female-specific expressed gene, cse0440, initially annotated as lrp1b-like, was identified from chromosome W of C. semilaevis. In view of the differences between cse0440 and lrp1b in terms of expression pattern, a phylogenetic analysis containing 85 LRP proteins was constructed and provided an evidence to re-annotate cse0440 as cseLRP13. In addition, two orthologues of cseLRP13 were separately identified from W and Z chromosomes: cseLRP13-W and cseLRP13-Z. The subsequent multiple sequence alignment and syntenic arrangements of LRP13 in C. semilaevis, Japanese medaka (Oryzias latipes), large yellow croaker (Larimichthys crocea), striped bass (Morone saxatilis), white perch (Morone americana) and Fugu rubripes (Takifugu rubripes) further supported this re-annotation. RT-PCR and in situ hybridization revealed that cselrp13 was exclusively expressed in the oocytes and follicles of ovaries. These results suggested that lrp13 may play important roles in female reproduction. In future, with the advancement of micromanipulation in flatfish, the detailed function of two lrp13 orthologues in C. semilaevis will be elucidated.


Chinese tongue sole (Cynoglossus semilaeviscse0440 Low-density lipoprotein receptor-related protein 13 (LRP13) Medaka (Oryzias latipes



This work was supported by grants from the Central Public-interest Scientific Institution Basal Research Fund CAFS (NO. 2016GH03), Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (NO. 20603022016004), the National Natural Science Foundation of China (31530078, 31472273) and the Taishan Scholar Project of Shandong Province.

Author contributions

NW and SLC conceived and designed the experiments, while NW and QMH verified the sequences of cseLRP13 and olaLRP13 by PCR experiments. RQW conducted RT-PCR. YZ and FY participated in the experiment of in situ hybridization. NW and RQW analysed the data and wrote the paper. WTX provided valuable suggestions regarding paper organization and language fluency. All authors read and approved the final manuscript.

Compliance with ethical standards

The collection and handling of the animals used in this study were approved by the Animal Care and Use Committee at the Chinese Academy of Fishery Sciences, and all the experimental procedures were performed in accordance with the guidelines for the Care and Use of Laboratory Animals at the Chinese Academy of Fishery Sciences.

Competing interest

The authors declare that they have no competing interests.

Supplementary material

10695_2017_372_MOESM1_ESM.docx (16 kb)
ESM 1 (DOCX 16 kb)


  1. Bajari TM, Strasser V, Nimpf J, Schneider WJ (2005) LDL receptor family: isolation, production, and ligand binding analysis. Methods 36(2):109–116CrossRefPubMedGoogle Scholar
  2. Battle MA, Maher VM, McCormick JJ (2003) ST7 is a novel low-density lipoprotein receptor-related protein (LRP) with a cytoplasmic tail that interacts with proteins related to signal transduction pathways. Biochemistry 42(24):7270–7282CrossRefPubMedGoogle Scholar
  3. Cam JA, Zerbinatti CV, Knisely JM, Hecimovic S, Li Y, Bu G (2004) The low density lipoprotein receptor-related protein 1B retains beta-amyloid precursor protein at the cell surface and reduces amyloid-beta peptide production. J Biol Chem 279(28):29639–29646CrossRefPubMedGoogle Scholar
  4. Chen SL, Li J, Deng SP, Tian YS, Wang QY, Zhuang ZM, Sha ZX, Xu JY (2007) Isolation of female-specific AFLP markers and molecular identification of genetic sex in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol (NY) 9(2):273–280CrossRefGoogle Scholar
  5. Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff JN, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Q, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46(3):253–260CrossRefPubMedGoogle Scholar
  6. Chue J, Smith CA (2011) Sex determination and sexual differentiation in the avian model. FEBS J 278(7):1027–1034CrossRefPubMedGoogle Scholar
  7. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA (2012) A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 109(8):2955–2959CrossRefPubMedPubMedCentralGoogle Scholar
  8. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  9. Li Y, Knisely JM, Lu W, McCormick LM, Wang J, Henkin J, Schwartz AL, Bu G (2002) Low density lipoprotein (LDL) receptor-related protein 1B impairs urokinase receptor regeneration on the cell surface and inhibits cell migration. J Biol Chem 277(44):42366–42371CrossRefPubMedGoogle Scholar
  10. Li Y, Lu W, Bu G (2005) Striking differences of LDL receptor-related protein 1B expression in mouse and human. Biochem Biophys Res Commun 333(3):868–873CrossRefPubMedGoogle Scholar
  11. Liu CX, Li Y, Obermoeller-McCormick LM, Schwartz AL, Bu G (2001) The putative tumor suppressor LRP1B, a novel member of the low density lipoprotein (LDL) receptor family, exhibits both overlapping and distinct properties with the LDL receptor-related protein. J Biol Chem 276(31):28889–28896CrossRefPubMedGoogle Scholar
  12. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563CrossRefPubMedGoogle Scholar
  13. Mushirobira Y, Mizuta H, Luo W, Todo T, Hara A, Reading BJ, Sullivan CV, Hiramatsu N (2015) Molecular cloning and partial characterization of a low-density lipoprotein receptor-related protein 13 (Lrp13) involved in vitellogenin uptake in the cutthroat trout (Oncorhynchus clarki). Mol Reprod Dev 82(12):986–1000CrossRefPubMedGoogle Scholar
  14. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191(1):163–170CrossRefPubMedPubMedCentralGoogle Scholar
  15. Penman DJ, Piferrer F (2008) Fish gonadogenesis. Part I: genetic and environmental mechanisms of sex determination. Rev Fish Sci 16(S1):16–34CrossRefGoogle Scholar
  16. Piferrer F, Guiguen Y (2008) Fish gonadogenesis. Part II: molecular biology and genomics of sex differentiation. Rev Fish Sci 16(S1):35–55CrossRefGoogle Scholar
  17. Reading BJ, Hiramatsu N, Schilling J, Molloy KT, Glassbrook N, Mizuta H, Luo W, Baltzegar DA, Williams VN, Todo T, Hara A, Sullivan CV (2014) Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes. J Lipid Res 55(11):2287–2295CrossRefPubMedPubMedCentralGoogle Scholar
  18. Sha Z, Wang S, Zhuang Z, Wang Q, Wang Q, Li P, Ding H, Wang N, Liu Z, Chen S (2010) Generation and analysis of 10 000 ESTs from the half-smooth tongue sole Cynoglossus semilaevis and identification of microsatellite and SNP markers. J Fish Biol 76(5):1190–1204CrossRefPubMedGoogle Scholar
  19. Shao CW, Chen SL, Scheuring CF, Xu JY, Sha ZX, Dong XL, Zhang HB (2010) Construction of two BAC libraries from half-smooth tongue sole Cynoglossus semilaevis and identification of clones containing candidate sex-determination genes. Mar Biotechnol (NY) 12(5):558–568CrossRefGoogle Scholar
  20. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346(6281):240–244CrossRefPubMedGoogle Scholar
  21. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461(7261):267–271CrossRefPubMedGoogle Scholar
  22. Song W, Li Y, Zhao Y, Liu Y, Niu Y, Pang R, Miao G, Liao X, Shao C, Gao F, Chen S (2012) Construction of a high-density microsatellite genetic linkage map and mapping of sexual and growth-related traits in half-smooth tongue sole (Cynoglossus semilaevis). PLoS One 7(12):e52097CrossRefPubMedPubMedCentralGoogle Scholar
  23. Sonoda I, Imoto I, Inoue J, Shibata T, Shimada Y, Chin K, Imamura M, Amagasa T, Gray JW, Hirohashi S, Inazawa J (2004) Frequent silencing of low density lipoprotein receptor-related protein 1B (LRP1B) expression by genetic and epigenetic mechanisms in esophageal squamous cell carcinoma. Cancer Res 64(11):3741–3747CrossRefPubMedGoogle Scholar
  24. Strickland DK, Gonias SL, Argraves WS (2002) Diverse roles for the LDL receptor family. Trends Endocrinol Metab 13(2):66–74CrossRefPubMedGoogle Scholar
  25. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 105(7):2469–2474CrossRefPubMedPubMedCentralGoogle Scholar
  26. Zhou LQ, Yang AG, Liu XZ, Du W, Zhuang ZM (2005) The karyotype of the tongue fish Cynoglossus semilaevis. J Fish Sci China 3:417–419Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Key Laboratory for Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdaoChina
  2. 2.Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiChina
  4. 4.Yangtze River Fisheries Research InstituteChinese Academy of Fishery SciencesWuhanChina
  5. 5.Marine Biology Institute of Shandong ProvinceQingdaoChina

Personalised recommendations