Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Cloning, expression, and activity of type IV antifreeze protein from cultured subtropical olive flounder (Paralichthys olivaceus)

  • Lee, Jong Kyu (Department of Microbiology, College of Natural Sciences, Pukyong National University) ;
  • Kim, Hak Jun (Department of Chemistry, College of Natural Sciences, Pukyong National University)
  • Received : 2016.09.24
  • Accepted : 2016.10.07
  • Published : 2016.10.31
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Abstract

Antifreeze proteins (AFPs) lower the freezing point but not the melting point of aqueous solutions by inhibiting the growth of ice crystals via an adsorption-inhibition mechanism. However, the function of type IV AFP (AFP IV) is questionable, as its antifreeze activity is on the verge of detectable limits, its physiological concentration in adult fish blood is too low to function as a biological antifreeze, and its homologues are present even in fish from tropic oceans as well as freshwater. Therefore, we speculated that AFP IV may have gained antifreeze activity not by selective pressure but by chance. To test this hypothesis, we cloned, expressed, and assayed AFP IV from cultured subtropical olive flounder (Paralichthys olivaceus), which do not require antifreeze protein for survival. Among the identified expressed sequence tags of the flounder liver sample, a 5'-deleted complementary DNA (cDNA) sequence similar to the afp4 gene of the longhorn sculpin was identified, and its full-length cDNA and genome structure were examined. The deduced amino acid sequence of flounder AFP IV shared 55, 53, 52, and 49 % identity with those of Pleuragramma antarcticum, Myoxocephalus octodecemspinosus, Myoxocephalus scorpius, and Notothenia coriiceps, respectively. Furthermore, the genomic structure of this gene was conserved with those of other known AFP IVs. Notably, the recombinant AFP IV showed a weak but distinct thermal hysteresis of $0.07{\pm}0.01^{\circ}C$ at the concentration of 0.5 mg/mL, and ice crystals in an AFP IV solution grew star-shaped, which are very similar to those obtained from other polar AFP IVs. Taken together, our results do not support the hypothesis of evolution of AFP IV by selective pressure, suggesting that the antifreeze activity of AFP IV may have been gained by chance.

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References

  1. Bendtsen JD, Nielsen H, Heijne GV, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783-95. https://doi.org/10.1016/j.jmb.2004.05.028
  2. Breton TS, Anderson JL, Goetz FW, Berlinsky DL. Identification of ovarian gene expression patterns during vitellogenesis in Atlantic cod (Gadus morhua). Gen Comp Endocrinol. 2012;179:296-304. https://doi.org/10.1016/j.ygcen.2012.09.003
  3. Cheng CH. Evolution of the diverse antifreeze proteins. Curr Opin Genet Dev. 1998;8:715-20. https://doi.org/10.1016/S0959-437X(98)80042-7
  4. Cheng CC. Freezing avoidance in polar fishes. In: Gerday C, editor. Encyclopedia of life support systems (EOLSS)-theme 6.73 extremophiles, developed under the auspices of the UNESCO. Oxford: Eolss Publishers; 2003. http://www.eolss.net.
  5. Cheng CH, Chen L. Evolution of an antifreeze glycoprotein. Nature. 1999;401:443-4. https://doi.org/10.1038/46721
  6. Cheng CH, Chen L, Near TJ, Jin Y. Functional antifreeze glycoprotein genes in temperate-water New Zealand notothenioid fish infer an Antarctic evolutionary origin. Mol Biol Evol. 2003;20:1897-908. https://doi.org/10.1093/molbev/msg208
  7. Choudhury M, Yamada S, Komatsu M, Kishimura H, Ando S. Homologue of mammalian apolipoprotein A-II in non-mammalian vertebrates. Acta Biochim Biophys Sin (Shanghai). 2009;41:370-8. https://doi.org/10.1093/abbs/gmp015
  8. Davies PL, Hew CL. Biochemistry of fish antifreeze proteins. FSSEB J. 1990;4:2460-8.
  9. Deng G, Laursen RA. Isolation and characterization of an antifreeze protein from the longhorn sculpin, Myoxocephalus octodecimspinosis. Biochim Biophys Acta. 1998;1388:305-14. https://doi.org/10.1016/S0167-4838(98)00180-0
  10. Deng G, Andrews DW, Laursen RA. Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin Myoxocephalus octodecimspinosis. FEBS Lett. 1997;402:17-20. https://doi.org/10.1016/S0014-5793(96)01466-4
  11. DeVries AL. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science. 1971;172:1152-5. https://doi.org/10.1126/science.172.3988.1152
  12. DeVries AL, Wohlschlag DE. Freezing resistance in some Antarctic fishes. Science. 1969;163:1073-5. https://doi.org/10.1126/science.163.3871.1073
  13. Fletcher GL, Hew CL, Davies PL. Antifreeze proteins of teleost fishes. Annu Rev Physiol. 2001;63:359-90. https://doi.org/10.1146/annurev.physiol.63.1.359
  14. Gauthier SY, Scotter AJ, Lin FH, Baardsnes J, Fletcher GL, Davies PL. A re-evaluation of the role of type IV antifreeze protein. Cryobiology. 2008;57:292-6. https://doi.org/10.1016/j.cryobiol.2008.10.122
  15. Goetz FW, McCauley L, Goetz GW, Norberg B. Using global genome approaches to address problems in cod mariculture. ICES J Marine Sci. 2006;63:393-9. https://doi.org/10.1016/j.icesjms.2005.10.006
  16. Graham LA, Lougheed SC, Ewart KV, Davies PL. Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS One. 2008;3:e2616. https://doi.org/10.1371/journal.pone.0002616
  17. Graham LA, Hobbs RS, Fletcher GL, Davies PL. Helical antifreeze proteins have independently evolved in fishes on four occasions. PLoS One. 2013;8:e81285. https://doi.org/10.1371/journal.pone.0081285
  18. Jia Z, Davies PL. Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem Sci. 2002;27:101-6. https://doi.org/10.1016/S0968-0004(01)02028-X
  19. Kim HJ. Antifreeze activity in temperate fish from the East Sea, Korea. Fisheries Aquatic Sci. 2015;18:137-42. https://doi.org/10.5657/FAS.2015.0137
  20. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. ClustalW and ClustalX version 2. Bioinformatics. 2007;23:2947-8. https://doi.org/10.1093/bioinformatics/btm404
  21. Lee JK, Kim YJ, Park KS, Shin SC, Kim HJ, Song YH, et al. Molecular and comparative analyses of type IV antifreeze proteins (AFPIVs) from two Antarctic fishes, Pleuragramma antarcticum and Notothenia coriiceps. Comp Biochem Physiol B Biochem Mol Biol. 2011;159:197-205. https://doi.org/10.1016/j.cbpb.2011.04.006
  22. Liu JX, Zhai YH, Gui JF. Molecular characterization and expression pattern of AFPIV during embryogenesis in gibel carp (Carassiu auratus gibelio). Mol Biol Rep. 2009;36:2011-8. https://doi.org/10.1007/s11033-008-9412-3
  23. Nishimiya Y, Yasuhiro M, Hirano Y, Kondo H, Miura A, Tsuda S. Mass preparation and technological development of an antifreeze protein. Synthesiology (Engl ed). 2008;1:7-14. https://doi.org/10.5571/syntheng.1.7
  24. Raymond JA, DeVries AL. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci U S A. 1977;74:2589-93. https://doi.org/10.1073/pnas.74.6.2589
  25. Wang Y, Zhou L, Li Z, Li W, Gui J. Apolipoprotein C1 regulates epiboly during gastrulation in zebrafish. Sci China Life Sci. 2013;56:975-84. https://doi.org/10.1007/s11427-013-4563-4
  26. Xia JH, Liu JX, Zhou L, Li Z, Gui JF. Apo-14 is required for digestive system organogenesis during fish embryogenesis and larval development. Int J Devel Biol. 2008;52:1089-98. https://doi.org/10.1387/ijdb.072519jx
  27. Xiao Q, Xia JH, Zhang XJ, Li Z, Wang Y, Zhou L, et al. Type-IV antifreeze proteins are essential for epiboly and convergence in gastrulation of zebrafish embryos. Int J Biol Sci. 2014;10:715-32. https://doi.org/10.7150/ijbs.9126
  28. Zhang T, Yao S, Wang P, Yin C, Xiao C, Qian M, et al. ApoA-II directs morphogenetic movements of zebrafish embryo by preventing chromosome fusion during nuclear division in yolk syncytial layer. J Biol Chem. 2011;286: 9514-25. https://doi.org/10.1074/jbc.M110.134908
  29. Zhao Z, Deng G, Lui Q, Laursen RA. Cloning and sequencing of cDNA encoding the LS-12 antifreeze protein in the longhorn sculpin, Myoxocephalus octodecimspinosis. Biochim Biophys Acta. 1998;1382:177-80. https://doi.org/10.1016/S0167-4838(97)00197-0

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