Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Expression of c-Type Lysozyme from the Fleshy Shrimp Fenneropenaeus chinensis Is Upregulated Following Vibrio anguillarum and Lipopolysaccharide Injection

  • Qiao, Guo (West Sea Fisheries Research Institute, National Fisheries Research & Development Institute) ;
  • Kim, Su-Kyoung (West Sea Fisheries Research Institute, National Fisheries Research & Development Institute) ;
  • Cho, Yeong-Rok (West Sea Fisheries Research Institute, National Fisheries Research & Development Institute) ;
  • Kim, Sukyoung (West Sea Fisheries Research Institute, National Fisheries Research & Development Institute) ;
  • Jang, In-Kwon (West Sea Fisheries Research Institute, National Fisheries Research & Development Institute)
  • Received : 2012.12.24
  • Accepted : 2013.08.01
  • Published : 2013.12.30
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Abstract

Chicken-type lysozyme (c-lysozyme) is present in shrimp and is active against some bacteria. To further understand the regulation of c-lysozyme in the fleshy shrimp Fenneropenaeus chinensis, we determined the tissue-specific gene expression of c-lysozyme and the time-course of mRNA expression in response to Vibrio anguillarum and lipopolysaccharide (LPS) injection by quantitative reverse real-time polymerase chain reaction. The results showed that c-lysozyme was expressed in all tissues tested, including gill, eyestalk, eye, hemocytes, hepatopancreas, intestine, heart, and pleopod. It was most highly expressed in the intestine followed by the eyestalk, gill, hemocytes and hepatopancreas. The mRNA expression level began to decline in a short time after V. anguillarum challenge and was then upregulated by two fold or more at 24 h post injection (hpi) compared to that at 0 h. Expression was suppressed shortly after LPS injection and began to increase with higher levels of 5.8-, 5.2- and 8.4-fold at 24, 48, and 72 hpi, respectively. Higher expression was sustained and showed a gradual increasing trend until the end of the experiment (72 hpi). These results increase our understanding of the regulation of defense mechanisms and facilitate an evaluation of the effects of probiotics or immunostimulants in shrimp culture.

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References

  1. Bae S and Kim Y. 2003. Lysozyme of the beet armyworm, Spodoptera exigua: activity induction and cDNA structure. Comp Biochem Physiol B Biochem Mol Biol 135, 511-519. http://dx.doi.org/10.1016/S1096-4959(03)00119-2.
  2. Beintema JJ and Terwisscha van Scheltinga AC. 1996. Plant lysozymes. In: Lysozymes: Model Enzymes in Biochemistry and Biology. Jolles P, ed. Birkhauser Verlag, Basel, pp. 75-86.
  3. Bu X, Du X, Zhou W, Zhao X and Wang J. 2008. Molecular cloning, recombinant expression, and characterization of lysozyme from Chinese shrimp Fenneropenaeus chinensis. Chin J Biotechnol 24, 723-732. http://dx.doi.org/10.1016/S1872-2075(08)60037-0.
  4. Burge EJ, Madigan DJ, Burnett LE and Burnett KG. 2007. Lysozyme gene expression by haemocytes of Pacific white shrimp, Litopenaeus vannamei, after injection with Vibrio. Fish Shellfish Immunol 22, 327-339. http://dx.doi.org/10.1016/j.fsi.2006.06.004.
  5. De Lorgeril J, Saulnier D, Janech MG, Gueguen Y and Bachere E. 2005. Identification of genes that are differentially expressed in haemocytes of the Pacific blue shrimp (Litopenaeus stylirostris) surviving an infection with Vibrio penaeicida. Physiol Genomics 21, 174-183. http://dx.doi.org/10.1152/physiolgenomics.00281.2004.
  6. De-la-Re-Vega E, Garcia-Galaz A, Diaz-Cinco ME and Sotelo-Mundo RR. 2006. White shrimp (Litopenaeus vannamei) recombinant lysozyme has antibacterial activity against Gram negative bacteria: Vibrio alginolyticus, Vibrio parahemolyticus and Vibrio cholerae. Fish Shellfish Immunol 20, 405-408. http://dx.doi.org/10.1016/j.fsi.2005.06.005.
  7. Dobson DE, Prager EM and Wilson AC. 1984. Stomach lysozymes of ruminants: I. distribution and catalytic properties. J Biol Chem 259, 11607-11616.
  8. Fastrez J. 1996. Phage lysozymes. In: Lysozymes: Model Enzymes in Biochemistry and Biology. Jolles P, ed. Birkhauser Verlag, Basel, pp. 35-64.
  9. Hikima S, Hikima J, Rojtinnakorn J, Hirono I and Aoki T. 2003. Characterization and function of Kuruma shrimp lysozyme possessing lytic activity against Vibrio species. Gene 316, 187-195. http://dx.doi.org/10.1016/S0378-1119(03)00761-3.
  10. Holtje JV. 1996. Bacterial lysozymes. In: Lysozymes: Model Enzymes in Biochemistry and Biology. Jolles P, ed. Birkhauser Verlag, Basel, pp. 65-74.
  11. Hultmark D. 1996. Insect lysozymes. In: Lysozymes: Model Enzymes in Biochemistry and Biology. Jolles P, ed. Basel: Birkhauser Verlag. pp. 87-102.
  12. Jang IK, Pang Z, Yu J, Kim SK, Seo HC and Cho YR. 2011. Selectively enhanced expression of prophenoloxidase activating enzyme 1 (PPAE1) at a bacteria clearance site in the white shrimp, Litopenaeus vannamei. BMC Immunology 12, 70. https://doi.org/10.1186/1471-2172-12-70
  13. Ji PF, Yao CL and Wang ZY. 2009. Immune response and gene expression in shrimp (Litopenaeus vannamei) haemocytes and hepatopancreas against some pathogen-associated molecular patterns. Fish Shellfish Immunol 27, 563-570. http://dx.doi.org/10.1016/j.fsi.2009.08.001.
  14. Jolles J and Jolles P. 1975. The lysozyme from Asterias rubens. Eur J Biochem 54, 19-23. http://dx.doi.org/10.1111/j.1432-1033.1975.tb04108.x.
  15. Jolles P and Jolles J. 1984. What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem 63, 165-189.
  16. Livak KJ and Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-{\Delta\Delta}Ct}$ method. Methods 25, 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
  17. Mai WJ and Hu CQ. 2009. Molecular cloning, characterization, expression and antibacterial analysis of a lysozyme homologue from Fenneropenaeus merguiensis. Mol Biol Rep 36, 1587-1595. http://dx.doi.org/10.1007/s11033-008-9355-8.
  18. McHenery JG, Birkbeck TH and Allen JA. 1979. The occurrence of lysozyme in marine bivalves. Comp Biochem Physiol 63, 25-28. http://dx.doi.org/10.1016/0305-0491(79)90228-1.
  19. Pan L, Yue F, Miao J, Zhang L and Li J. 2010. Molecular cloning and characterization of a novel c-type lysozyme gene in swimming crab Portunus trituberculatus. Fish Shellfish Immunol 29, 286-292. http://dx.doi.org/10.1016/j.fsi.2010.04.011.
  20. Paskewitz SM, Li B and Kajla MK. 2008. Cloning and molecular characterization of two invertebrate-type lysozymes from Anopheles gambiae. Insect Mol Biol 17, 217-225. http://dx.doi.org/10.1111/j.1365-2583.2008.00797.x.
  21. Peregrino-Uriarte AB, Muhlia-Almazan AT, Arvizu-Flores AA, Gomez-Anduro G, Gollas-Galvan T, Yepiz-Plascencia G and Sotelo-Mundo R. 2012. Shrimp invertebrate lysozyme i-lyz: gene structure, molecular model and response of c and i lysozymes to lipopolysaccharide (LPS). Fish Shellfish Immunol 32, 230-236. http://dx.doi.org/10.1016/j.fsi.2011.10.026.
  22. Prager EM and Jolles P. 1996. Animal lysozymes c and g: an overview. In: Lysozymes: Model Enzymes in Biochemistry and Biology. Jolles P, ed. Birkhauser Verlag, Basel, pp. 9-31.
  23. Qasba PK and Kumar S. 1997. Molecular divergence of lysozymes and alpha-lactalbumin. Crit Rev Biochem Mol Biol 32, 255-306. http://dx.doi.org/10.3109/10409239709082574.
  24. Qiao G, Lee DC, Woo SH, Li H, Xu DH and Park SI. 2012. Microbiological characteristics of Vibrio scophthalmi isolates from diseased olive flounder Paralichthys olivaceus. Fish Sci 78, 853-863. http://dx.doi.org/10.1007/s12562-012-0502-8.
  25. Ratcliffe NA, Rowley AF, Fitzgerald SW and Rhodes CP. 1985. Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol 97, 183-350. http://dx.doi.org/10.1016/S0074-7696(08)62351-7.
  26. Rodriguez-Ramos T, Espinosa G, Hernandez-Lopez J, Gollas-Galvan T, Marrero J, Borrell Y, Alonso Ma, Becquer U and Alonso M. 2008. Effects of Escherichia coli lipopolysaccharides and dissolved ammonia on immune response in southern white shrimp Litopenaeus schmitti. Aquaculture 274, 118-125. http://dx.doi.org/10.1016/j.aquaculture.2007.10.049.
  27. Sotelo-Mundo RR, Islas-Osuna MA, de-la-Re-Vega E, Hernandez-Lopez J, Vargas-Albores F and Yepiz-Plascencia G. 2003. cDNA cloning of the lysozyme of the white shrimp Penaeus vannamei. Fish Shellfish Immunol 15, 325-331. http://dx.doi.org/10.1016/S1050-4648(02)00176-6.
  28. Sung HH and Sun R. 1999. Intrahaemolytic activity of lysosomal enzymes in Penaeus monodon and Macrobrachium rosenbergii. Fish Shellfish Immunol 9, 505-508. https://doi.org/10.1006/fsim.1999.0209
  29. Supungul P, Klinbunga S, Pichyangkura R, Jitrapakdee S, Hirono I, Aoki T and Tassanakajon A. 2002. Identification of immune-related genes in haemocytes of black tiger shrimp (Penaeus monodon). Mar Biotechnol 4, 487-494. http://dx.doi.org/10.1007/s10126-002-0043-8.
  30. Supungul P, Rimphanitchayakit V, Aoki T, Hirono I and Tassanakajon A. 2010. Molecular characterization and expression analysis of a c-type and two novel muramidase-deficient i-type lysozymes from Penaeus monodon. Fish Shellfish Immunol 28, 490-498. http://dx.doi.org/10.1016/j.fsi.2010.01.003.
  31. Tyagi A, Khushiramani R, Karunasagar I and Karunasagar I. 2007. Antivibrio activity of recombinant lysozyme expressed from black tiger shrimp, Penaeus monodon. Aquaculture 272, 246-253. http://dx.doi.org/10.1016/j.aquaculture.2007.08.055.
  32. Xue Q, Hellberg ME, Schey KL, Itoh N, Eytan RI, Cooper RK and La Peyre JF. 2010. A new lysozyme from the eastern oyster Crassostrea virginica, and a possible evolutionary pathway for i-type lysozymes in bivalves from host defence to digestion. BMC Evol Biol 10, 213. http://dx.doi.org/10.1186/1471-2148-10-213.
  33. Yao CL, Wu CG, Xiang JH, Li F, Wang ZY and Han X. 2008. The lysozyme and lysozyme response in Chinese shrimp Fenneropenaeus chinensis to Vibrio anguillarum and laminarin stimulation. J Exp Mar Biol Ecol 363, 124-129. http://dx.doi.org/10.1016/j.jembe.2008.06.035.
  34. Zasloff M. 2002. Innate immunity, antimicrobial peptides, and protection of the oral cavity. The Lancet 360, 1116-1117. http://dx.doi.org/10.1016/S0140-6736(02)11239-6.
  35. Zhang HW, Sun C, Sun SS, Zhao XF and Wang JX. 2010. Functional analysis of two invertebrate-type lysozymes from red swamp crayfish Procambarus clarkii. Fish Shellfish Immunol 29, 1066-1072. http://dx.doi.org/10.1016/j.fsi.2010.08.023.
  36. Zhao J, Song L, Li C, Zou H, Ni D, Wang W and Xu W. 2007. Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol Immunol 44, 1198-1208. http://dx.doi.org/10.1016/j.molimm.2006.06.008.

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