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Cloning, characterization and expression of the pepsinogen C from the golden mandarin fish Siniperca scherzeri (Teleostei: Perciformes)

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Abstract

Pepsinogens are precursors of pepsins, which are gastric digestive proteinases that degrade food proteins into peptides. In the study reported here, the cDNA and its corresponding genomic DNA of the golden mandarin fish (Siniperca scherzeri, Perciformes) pepsinogen C (PGC) were cloned and sequenced. The golden mandarin fish PGC gene was deduced to have nine exons and eight introns, a structure similar to the PGCs of other vertebrates. The full-length cDNA was found to contain a 37-bp 5′-untranslated region, a 1,164-bp open reading frame, and a 304-bp 3′-untranslated region and the PGC protein to consist of a signal peptide, an activation segment, and a pepsin moiety. A sequence analysis revealed that pairwise sequence similarities of PGC proteins are around 70% between golden mandarin fish and other vertebrate groups, and around 90% within the fish group. A comparison of vertebrate PGC protein sequences revealed two motifs. One was in the activation segment that occurred only in the mammal and avian PGCs, suggesting that PGCs active in homeotherms (mammal and avian) have different activation mechanisms than those in poikilotherms (amphibian and fish). The second was in the pepsin moiety that occurred only in fish, suggesting the primitive position of fish among vertebrates. PGC mRNA is mainly expressed in the stomach and esophagus and at much lower levels in the skin and muscle. Taken together with results reported from other studies, the results reported here will lead to a better understanding of the molecular mechanisms of fish digestive physiology and the evolution of fish pepsinogen genes.

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References

  1. Kageyama T (2002) Pepsinogens, progastricsins and prochymosins: structure, function, evolution and development. Cell Mol Life Sci 59:288–306

    Article  CAS  PubMed  Google Scholar 

  2. Taylor WH (1968) Biochemistry of pepsins. In: Code CF, Heide W (eds) Handbook of physiology—alimentary canal, vol 5. Williams and Wilkins, Baltimore, pp 2567–2587

    Google Scholar 

  3. Foltmann B (1981) Gastric proteinases-structure, function, evolution and mechanism of action. Essays Biochem 17:52–84

    CAS  PubMed  Google Scholar 

  4. Gildberg A (1988) Aspartic proteinases in fishes and aquatic invertebrates. Comp Biochem Physiol B 91:425–435

    Article  CAS  PubMed  Google Scholar 

  5. Yin MC (1995) Fish ecology. Agricultural Press of China, Beijing

    Google Scholar 

  6. Bobe J, Goetz FW (2001) An ovarian progastricsin is present in the trout coelomic fluid after ovulation. Biol Reprod 64:1048–1055

    Article  CAS  PubMed  Google Scholar 

  7. Carginale V, Trinchella F, Capasso C, Scudiero R, Parisi E (2004) Gene amplification and cold adaptation of pepsin in Antarctic fish. A possible strategy for food digestion at low temperature. Gene 336:195–205

    Article  CAS  PubMed  Google Scholar 

  8. Terova G, Rimoldi S, Larghi S, Bernardini G, Gornati R, Saroglia M (2007) Regulation of progastricsin mRNA levels in sea bass (Dicentrarchus labrax) in response to fluctuations in food availability. Biochem Biophys Res Commun 363:591–596

    Article  CAS  PubMed  Google Scholar 

  9. Feng SZ, Li WS, Lin HR (2008) Characterization and expression of the pepsinogen C gene and determination of pepsin-like enzyme activity from orange-spotted grouper (Epinephelus coioides). Comp Biochem Physiol B 149:275–284

    Article  PubMed  Google Scholar 

  10. Tanji M, Yakabe E, Kubota K, Kageyama T, Ichinose M, Miki K, Ito H, Takahashi K (2009) Structural and phylogenetic comparison of three pepsinogens from Pacific bluefin tuna: molecular evolution of fish pepsinogens. Comp Biochem Physiol B 152:9–19

    Article  PubMed  Google Scholar 

  11. Zhou CW, Yang Q, Cai DL (1988) On the classification and distribution of the Sinipercinae fishes (Family Serranidae). Zool Res 9:113–125

    Google Scholar 

  12. Wu XF, Zhao JL, Qian YZ, Wu C (2007) Histological study on the digestive system organogenesis for the mandarin fish, Siniperca chuatsi. Zool Res 28:511–518

    Google Scholar 

  13. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor

    Google Scholar 

  14. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  Google Scholar 

  15. Liu XX, Liang XF, Wang L, Duan JX, Li GZ, Liao WQ (2009) Cloning and analysis of the full-length cDNA sequence and 5′-flanking region of Chinese perch Siniperca chuatsi β-actin gene. J Oceanol Limnol 40:102–108

    CAS  Google Scholar 

  16. Karlsen S, Hough E, Olsen RL (1998) Structure and proposed amino-acid sequence of a pepsin from Atlantic cod (Gadus morhua). Acta Crystallogr Sect D Biol Crystallogr 54:32–46

    Article  CAS  Google Scholar 

  17. Andreeva NS, James MN (1991) Why does pepsin have a negative charge at very low pH? An analysis of conserved charged residues in aspartic proteinases. Adv Exp Med Biol 306:39–45

    CAS  PubMed  Google Scholar 

  18. Hassan MI, Toor A, Ahmad F (2010) Progastriscin: structure, function, and its role in tumor progression. J Mol Cell Biol 2:118–127

    Article  CAS  PubMed  Google Scholar 

  19. Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Article  CAS  PubMed  Google Scholar 

  20. Evers MP, Zelle B, Bebelman JP, van Beusechem VV, Kraakman L, Hoffer MJ, Pronk JC, Mager WH, Planta RJ, Eriksson AW, Frants RR (1989) Nucleotide sequence comparison of five human pepsinogen A (PGA) genes: evolution of the PGA multigene family. Genomics 4:232–239

    Article  CAS  PubMed  Google Scholar 

  21. Tang J, Sepulveda P, Marciniszyn J, Chen KCS, Huang WY, Tao N, Liu D, Lanier JP (1973) Amino-acid sequence of porcine pepsin. Proc Natl Acad Sci USA 70:3437–3439

    Article  CAS  PubMed  Google Scholar 

  22. Kageyama T, Takahashi K (1978) Monkey pepsinogens and pepsins. III. Carbohydrate moiety of Japanese monkey pepsinogens and the amino acid sequence around the site of its attachment to protein. J Biochem 84:771–778

    CAS  PubMed  Google Scholar 

  23. Martin P, Trieu-Cuot P, Collin JC, Dumas BR (1982) Purification and characterization of bovine gastricsin. Eur J Biochem 122:31–39

    Article  CAS  PubMed  Google Scholar 

  24. Pals G, Azuma T, Mohandas TK, Bell GI, Bacon J, Samloff IM, Walz DA, Barr PJ, Taggart RT (1989) Human pepsinogen C (Progastricsin) polymorphism: evidence for a single locus located at 6p21.1-pter. Genomics 4:137–145

    Article  CAS  PubMed  Google Scholar 

  25. Yakabe E, Tanji M, Ichinose M, Goto S, Miki K, Kurokawa K, Ito H, Kageyama T, Takahashi K (1991) Purification, characterization and amino acid sequences of pepsinogens and pepsins from the esophageal mucosa of bullfrog (Rana catesbeiana). J Biol Chem 266:22436–22443

    CAS  PubMed  Google Scholar 

  26. Foltmann B, Jensen AL (1982) Human progastricsin. Analysis of intermediates during activation into gastricsin and determination of the amino acid sequence of the propart. Eur J Biochem 128:63–70

    Article  CAS  PubMed  Google Scholar 

  27. Zheng J, Chen JH (1998) General biochemistry, 3rd edn. Higher Education Press, Beijing

    Google Scholar 

  28. Tang J (1970) Gastricsin and pepsin. Methods Enzymol 19:406–421

    Article  Google Scholar 

  29. Szecsi PB (1992) The aspartic proteases. Scand J Clin Lab Invest 52:5–22

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Mary Christman, University of Nebraska at Omaha, for proof-reading this paper. This work was sponsored by Science and Technology Commission of Shanghai Municipality (09JC1406900), Shanghai Leading Academic Discipline Project (No. Y1101) and Shanghai Municipal Education Commission (05KZ02).

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Correspondence to Jinliang Zhao.

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Deng, Y., Zhao, J., Lu, G. et al. Cloning, characterization and expression of the pepsinogen C from the golden mandarin fish Siniperca scherzeri (Teleostei: Perciformes). Fish Sci 76, 819–826 (2010). https://doi.org/10.1007/s12562-010-0275-x

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