Skip to main content
SpringerLink
Log in

Sequence analysis and expression regulation of rbp4 by 9-cis-RA in Megalobrama amblycephala

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Retinol-binding protein 4 (rbp4) is mainly synthesized in the liver, where it binds retinol and then enters the bloodstream, delivering retinol to cells. The full-length cDNA coding rbp4 was cloned from Megalobrama amblycephala. The amino acid sequence showed strong homology with the homologues of other vertebrates, and all structural and functional domains were highly conserved. The mRNA levels in different tissues and development stages detected by quantitative real-time PCR revealed that M. amblycephala rbp4 was highly expressed in liver (P < 0.001), but the lower levels were also detected in eyes, kidney, intestine, and spleen. During the different development stages, the rbp4 mRNA appeared until 28 hours post-fertilization (hpf), underwent a slight drop, and then gradually increased after 50 hpf. In addition, the promoter sequence of M. amblycephala rbp4 was obtained using thermal asymmetric interlaced PCR. Two single nucleotide polymorphism sites (-385A>G and -329C>T) were found in the promoter. Transfection with recombinant plasmids of two different haplotypes (GT, AC) showed that 9-cis-retinoic acid (RA) increased the promoter activity, but the AC haplotype was more sensitive to RA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bellovino D, Morimoto T, Mengheri E, Perozzi G, Garaguso I, Nobili F, Gaetani S (2001) Unique biochemical nature of carp retinol-binding protein. N-linked glycosylation and uncleavable NH2-terminal signal peptide. J Biol Chem 276:13949–13956

    CAS  PubMed  Google Scholar 

  • Bellovino D, Apreda M, Gragnoli S, Massimi M, Gaetani S (2003) Vitamin A transport: in vitro models for the study of RBP secretion. Mol Aspects Med 24:411–420

    Article  CAS  PubMed  Google Scholar 

  • Benkoussa M, Brand C, Delmotte MH, Formstecher P, Lefebvre P (2002) Retinoic acid receptors inhibit AP1 activation by regulating extracellular signal-regulated kinase and CBP recruitment to an AP1-responsive promoter. Mol Cell Biol 22:4522–4534

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blomhoff R, Blomhoff HK (2006) Overview of retinoid metabolism and function. J Neurobiol 66:606–630

    Article  CAS  PubMed  Google Scholar 

  • Chu J, Sadler KC (2009) New school in liver development: lessons from zebrafish. Hepatology 50(5):1656–1663

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clagett-Dame M, DeLuca HF (2002) The role of vitamin A in mammalian reproduction and embryonic development. Annu Rev Nutr 22:347–381

    Article  CAS  PubMed  Google Scholar 

  • Dedieu S, Lefebvre P (2006) Retinoids interfere with the AP1 signalling pathway in human breast cancer cells. Cell Signal 18:889–898

    Article  CAS  PubMed  Google Scholar 

  • Devirgiliis C, Gaetani S, Apreda M, Bellovino D (2005) Glycosylation is essential for translocation of carp retinol-binding protein across the endoplasmic reticulum membrane. Biochem Biophys Res Commun 332:504–511

    Article  CAS  PubMed  Google Scholar 

  • Duester G (2000) Families of retinoid dehydrogenases regulating vitamin A function; production of visual pigment and retinoid acid. Eur J Biochem 267:4315–4324

    Article  CAS  PubMed  Google Scholar 

  • Duester G (2008) Retinoic acid synthesis and signaling during early organogenesis. Cell 134:921–931

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, Evans RM, Thaller C (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 66:397–406

    Article  Google Scholar 

  • Hyung SJ, Deroo S, Robinson CV (2010) Retinol and retinol-binding protein stabilize transthyretin via formation of retinol transport complex. ACS Chem Biol 5(12):1137–1146

    Article  CAS  PubMed  Google Scholar 

  • Kam RK, Deng Y, Chen Y, Zhao H (2012) Retinoic acid synthesis and functions in early embryonic development. Cell Biosci 2:11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kato S, Matsukawa T, Koriyama Y, Sugitani K, Ogai K (2013) A molecular mechanism of optic nerve regeneration in fish: the retinoid signaling pathway. Prog Retin Eye Res 37:13–30

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi R, Yu J, Honda J, Hu J, Whitelegge J, Ping P, Wiita P, Bok D, Sun H (2007) A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315:820–825

    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 Endocrinol Metab 302(6):626–644

    Article  Google Scholar 

  • Levin AA, Sturzenbecker LJ, Kazmer S, Bosakowski T, Huselton C et al (1992) 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355:359–361

    Article  CAS  PubMed  Google Scholar 

  • Li S, Gul Y, Wang W, Qian X, Zhao Y (2013) PPARγ, an important gene related to lipid metabolism and immunity in Megalobrama amblycephala: cloning, characterization and transcription analysis by GeNorm. Gene 512:321–330

    Article  CAS  PubMed  Google Scholar 

  • Liu YG, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674–681

    Article  CAS  PubMed  Google Scholar 

  • Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  CAS  PubMed  Google Scholar 

  • Mangelsdorf DJ (1994) Vitamin A receptors. Nutr Rev 52:32–44

    Article  Google Scholar 

  • Monaco HL, Rizzi M, Coda A (1995) Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science 268:1039–1041

    Article  CAS  PubMed  Google Scholar 

  • Monzon RI, LaPres JJ, Hudson LG (1996) Regulation of involucrin gene expression by retinoic acid and glucocorticoids. Cell Growth Differ 7:1751–1759

    CAS  PubMed  Google Scholar 

  • Munkhtulga L, Nagashima S, Nakayama K, Utsumi N, Yanagisawa Y et al (2010) Regulatory SNP in the RBP4 gene modified the expression in adipocytes and associated with BMI. Obesity 18:1006–1014

    Article  CAS  PubMed  Google Scholar 

  • Nagashima M, Sakurai H, Mawatari K, Koriyama Y, Matsukawa T, Kato S (2009) Involvement of retinoic acid signaling in goldfish optic nerve regeneration. Neurochem Int 54(3–4):229–236

    Article  CAS  PubMed  Google Scholar 

  • Napoli JL (1996) Biochemical pathways of retinoid transport, metabolism, and signal transduction. Clin Immunol Immunopathol 80:52–62

    Article  Google Scholar 

  • Naylor HM, Newcomer ME (1999) The structure of human retinol-binding protein (RBP) with its carrier protein transthyretin reveals an interaction with the carboxy terminus of RBP. Biochemistry 38:2647–2653

    Article  CAS  PubMed  Google Scholar 

  • Noy N (2000) Retinoid-binding proteins: mediators of retinoid action. Biochem J 348:481–495

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pemrick SM, Lucas DA, Grippo JF (1994) The retinoid receptors. Leukemia 8:1797–1806

    CAS  PubMed  Google Scholar 

  • Rhinn M, Dollé P (2012) Retinoic acid signalling during development. Development 139:843–858

    Article  CAS  PubMed  Google Scholar 

  • Richardson SJ, Cody V (2009) Recent advances in transthyretin evolution structure and biological functions. Springer, Berlin

    Book  Google Scholar 

  • Ross AC (2000) Addressing research questions with national survey data—the relation of vitamin A status to infection and inflammation. Am J Clin Nutr 72:1069–1070

    CAS  PubMed  Google Scholar 

  • Sammar M, Babin PJ, Durliat M, Meiri I, Zchori I, Elizur A, Lubzens E (2001) Retinol binding protein in Rainbow Trout: molecular properties and mRNA expression in tissues. Gen Comp Endocrinol 123:51–61

    Article  CAS  PubMed  Google Scholar 

  • Sammar M, Levi L, Hurvitz A, Lubzens E (2005) Studies on retinol-binding protein during vitellogenesis in the rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 141:141–151

    Article  CAS  PubMed  Google Scholar 

  • Soprano DR, Blaner WS (1994) The retinoids: biology, chemistry and medicine. Sporn MB., Roberts AB and Goodman DS., eds 2nd Ed. Raven Press, New York, pp 257–282

  • Stafford D, Prince VE (2002) Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr Biol 12:1215–1220

    Article  CAS  PubMed  Google Scholar 

  • Strausberg RL, Feingold EA, Grouse LH et al (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A 99:16899–16903

    Article  PubMed  Google Scholar 

  • Thanh T, Chi VT, Abdullah MP, Omar H, Napis S (2012) Efficiency of Ligation-Mediated PCR and TAIL-PCR methods for isolation of RbcS promoter sequences from green microalga Ankistrodesmus convolutus. Mol Biol 46:64–70

    Article  Google Scholar 

  • Wang M, Lai X, Yu H (2010) Two novel single nucleotide polymorphisms (SNPs) and 4-bp deletion mutation of rbp4 gene in Chinese cattle. J Genet 89:233–236

    Article  PubMed  Google Scholar 

  • Wolf G (2006) Is 9-cis-retinoic acid the endogenous ligand for the retinoic acid-X receptor? Nutr Rev 64:532–538

    Article  PubMed  Google Scholar 

  • Zanotti G, Marcello M, Malpeli G, Folli C, Sartori G, Berni R (1994) Crystallographic studies on complexes between retinoids and plasma retinol-binding protein. J Biol Chem 269:29613–29620

    CAS  PubMed  Google Scholar 

  • Zapponi MC, Zanotti G, Stoppini M, Berni R (1992) The primary structure of piscine (Oncorhynchus mykiss) retinol-binding protein and a comparison with the three-dimensional structure of mammalian retinol-binding protein. Eur J Biochem 210:937–943

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Wei XL, Chen LP, Chen N, Li YH, Wang WM, Wang HL (2013) Sequence analysis and expression differentiation of chemokine receptor CXCR4b among three populations of Megalobrama amblycephala. Dev Comp Immunol 40:195–201

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Fundamental Research Funds for the Central Universities (2013PY067), and Program for New Century Excellent Talents in University (NCET-10-0403).

Author information

Authors and Affiliations

  1. Key Lab of Freshwater Animal Breeding, Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Ministry of Education, College of Fishery, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Mengxia Xu, Chunxiao Huang, Nan Chen, Xinjie Wu, Kecheng Zhu, Weimin Wang & Huanling Wang

  2. Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan, 430070, People’s Republic of China

    Weimin Wang & Huanling Wang

Authors
  1. Mengxia Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunxiao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinjie Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kecheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weimin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huanling Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huanling Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, M., Huang, C., Chen, N. et al. Sequence analysis and expression regulation of rbp4 by 9-cis-RA in Megalobrama amblycephala . Fish Physiol Biochem 41, 437–447 (2015). https://doi.org/10.1007/s10695-014-9995-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-014-9995-7

Keywords

Search

Navigation