Marine Biotechnology

, Volume 10, Issue 4, pp 438–446 | Cite as

The Encysted Dormant Embryo Proteome of Artemia sinica

  • Qian Zhou
  • Changgong Wu
  • Bo Dong
  • Fengqi Liu
  • Jianhai Xiang
Original Article

Abstract

The possibility of the brine shrimp Artemia to produce dormant embryo (cysts) in diapause is a key feature in its life history. In the present study, we obtained a proteomic reference map for the diapause embryo of Artemia sinica using two-dimensional gel electrophoresis with a pH range of 4–7 and a molecular weight range of 10–100 kDa. Approximately 233 proteins were detected, and 60 of them were analyzed by capillary liquid chromatography tandem mass spectrometry (LC–MS/MS). Of these, 39 spots representing 33 unique proteins were identified, which are categorized into functional groups, including cell defense, cell structure, metabolism, protein synthesis, proteolysis, and other processes. This reference map will contribute toward understanding the state of the diapause embryo and lay the basis and serve as a useful tool for further profound studies in the proteomics of Artemia at different developmental stages and physiological conditions.

Keywords

Proteome Diapause embryo 2D-E Mass spectrometry Artemia sinica 

Notes

Acknowledgments

This research was supported by the program of National Natural Science Foundation of China (20060109Z4016) and Natural Science Foundation of Shandong Province for the excellent young researcher (2006BSA02004).

References

  1. Abatzopoulos TJ (2002) Artemia: basic and applied biology. Kluwer Academic Publishers, The NetherlandsGoogle Scholar
  2. Apraiz I, Mi J, Cristobal S (2006) Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol Cell Proteomics 5:1274–1285PubMedCrossRefGoogle Scholar
  3. Bowen ST (1962) The genetics of Artemia salina. I. The reproductive cycle. Biol Bull 122:25–32CrossRefGoogle Scholar
  4. Boyer PD (1997) The ATP synthase: a splendid molecular machine. Annu Rev Biochem 66:717–749PubMedCrossRefGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  6. Britton C, Murray L (2002) A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Mol Biochem Parasit 122:21–33CrossRefGoogle Scholar
  7. Browne RA, Trotman CNA, Sorgeloos P (1991) Artemia biology. CRC Press, Boca RatonGoogle Scholar
  8. Carballido-Lopez R, Errington J (2003) A dynamic bacterial cytoskeleton. Trends Cell Biol 13:577–583PubMedCrossRefGoogle Scholar
  9. Clegg JS (1964) The control of emergence and metabolism by external osmotic pressure and the role of free glycerol in developing cysts of Artemia salina. J Exp Biol 41:879–892PubMedGoogle Scholar
  10. Clegg JS (1997) Embryos of Artemia franciscana survive four years of continuous anoxia: The case for complete metabolic rate depression. J Exp Biol 200:467–475PubMedGoogle Scholar
  11. Clegg JS (2005) Desiccation tolerance in encysted embryos of the animal extremophile, Artemia. Integ Comp Biol 45:715–724CrossRefGoogle Scholar
  12. Clegg JS, Van Hoa N, Sorgeloos P (2001) Thermal tolerance and heat shock proteins in encysted embryos of Artemia from widely different thermal habitats. Hydrobiologia 466:221–229CrossRefGoogle Scholar
  13. Conte FP, Droukas PC, Ewing RD (1977) Development of sodium regulation and De Novo synthesis of NA + K-activated ATPase in larval brine shrimp, Artemia salina. J Exp Zool 202:339–362CrossRefGoogle Scholar
  14. Day RM, Gupta JS, MacRae TH (2003) A small heat shock/alpha-crystallin protein from encysted Artemia embryos suppresses tubulin denaturation. Cell Stress Chaperon 8:183–193CrossRefGoogle Scholar
  15. de Chaffoy de Courcelles D, Kondo M (1980) Lipovitellin from the crustacean, Artemia salina. Biochemical analysis of lipovitellin complex from the yolk granules. J Biol Chem 255:6727–6733PubMedGoogle Scholar
  16. Drinkwater LE, Crowe JH (1987) Regulation of embryonic diapause in Arternia: environmental and physiological signals. J Exp Zool 241:297–307CrossRefGoogle Scholar
  17. Dumas C (1993) Cloning and sequence analysis of the gene for arginine kinase of lobster muscle. J Biol Chem 268:21599–21605PubMedGoogle Scholar
  18. Ellington WR (1989) Phosphocreatine represents a thermodynamic and functional improvement over other muscle phosphagens. J Exp Biol 143:177–194PubMedGoogle Scholar
  19. Fagotto F (1990) Yolk degradation in tick eggs: II. Evidence that cathepsin L-like proteinase is stored as a latent, acid-activable proenzyme. Arch Insect Biochem Physiol 14:237–252PubMedCrossRefGoogle Scholar
  20. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45PubMedCrossRefGoogle Scholar
  21. Guiliano DB, Hong XQ, McKerrow JH, Blaxter ML, Oksov Y, Liu J, Ghedin E, Lustigman S (2004) A gene family of cathepsin L-like proteases of filarial nematodes are associated with larval molting and cuticle and eggshell remodeling. Mol Biochem Parasit 136:227–242CrossRefGoogle Scholar
  22. Hecker M, Engelmann S, Cordwell SJ (2003) Proteomics of Staphylococcus aureus—current state and future challenges. J Chromatogr B 787:179–195Google Scholar
  23. Herman IM (1993) Actin isoforms. Curr Opin Cell Biol 5:48–55PubMedCrossRefGoogle Scholar
  24. Howard J, Hyman AA (2003) Dynamics and mechanics of the microtubule plus end. Nature 422:753–758PubMedCrossRefGoogle Scholar
  25. Hu KJ, Leung PC (2004) Shrimp cathepsin L encoded by an intronless gene has predominant expression in hepatopancreas, and occurs in the nucleus of oocyte. Comp Biochem Phys B-Biochem Mol Biol 138:445CrossRefGoogle Scholar
  26. Huang C, Liu G, Zeng L, Wu M (2002) Influence of inducing conditions and specific diapause deactivation methods on hatchability of two species. Artemia cysts produced in lab. Fisheries Sci 21:1–4Google Scholar
  27. Kotlyar S, Weihrauch D, Paulsen RS, Towle DW (2000) Expression of arginine kinase enzymatic activity and mRNA in gills of the euryhaline crabs Carcinus maenas and Callinectes sapidus. J Exp Biol 203:2395–2404PubMedGoogle Scholar
  28. Langdon CM, Rafiee P, Macrae TH (1991) Synthesis of tubulin during early postgastrula development of Artemia - isotubulin generation and translational regulation. Dev Biol 148:138–146PubMedCrossRefGoogle Scholar
  29. Lavens P, Sorgeloos P (1987) The cryptobiotic state of Artemia cysts, its diapause deactivation and hatching: a review. In: Sorgeloos P et al (eds) Artemia research and its applications: 3. Ecology, culturing, use in aquaculture. In the Second International Symposium on the brine shrimp Artemia, pp 27–63Google Scholar
  30. Lavens P, Sorgeloos P (1996) Manual on the production and use of live food for aquaculture, vol 361. FAO Fisheries Technical Paper, RomeGoogle Scholar
  31. Lee J, Valkova N, White MP, Kultz D (2006) Proteomic identification of processes and pathways characteristic of osmoregulatory tissues in spiny dogfish shark (Squalus acanthias). Comp Biochem Phys D-Genom Proteom 1:328–343Google Scholar
  32. Liang P, MacRae TH (1999) The synthesis of a small heat shock/[alpha]-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445–456PubMedCrossRefGoogle Scholar
  33. Liu LQ, Warner AH (2006) Further characterization of the cathepsin L-associated protein and its gene in two species of the brine shrimp, Artemia. Comp Biochem Phys A-Mol Integ Phys 145:458–467Google Scholar
  34. MacRae TH (2003) Molecular chaperones, stress resistance and development in Artemia franciscana. Semin Cell Dev Biol 14:251–258PubMedCrossRefGoogle Scholar
  35. MacRae TH, Ludueña RF (1984) Developmental and comparative aspects of brine shrimp tubulin. Biochem J 219:137–148PubMedGoogle Scholar
  36. Miyata S, Kubo T (1997) Inhibition of gastrulation in Xenopus embryos by an antibody against a cathepsin L-like protease. Dev Growth Differ 39:111–115PubMedCrossRefGoogle Scholar
  37. O’Connell PA, Pinto DM, Chisholm KA, MacRae TH (2006) Characterization of the microtubule proteome during post-diapause development of Artemia franciscana. Biochim Biophys Acta (BBA) Proteins Proteom 1764:920–928CrossRefGoogle Scholar
  38. Olson CS, Clegg JS (1978) Cell division during the development of Artemia salina. Dev Genes Evol 184:1–13Google Scholar
  39. Pandey A, Mann M (2000) Proteomics to study genes and genomes. Nature 405:837–846PubMedCrossRefGoogle Scholar
  40. Qiu ZJ, Viner RI, MacRae TH, Willsie JK, Clegg JS (2004) A small heat shock protein from Artemia franciscana is phosphorylated at serine 50. Biochim Biophys Acta-Proteins Proteom 1700:75–83CrossRefGoogle Scholar
  41. Shevchenko A, Jensen, ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Shevchenko A, Boucherie H, Mann M (1996) Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Biochemistry 93:14440–14445Google Scholar
  42. Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233PubMedCrossRefGoogle Scholar
  43. Tyan Y-C, Guo H-R, Liu C-Y, Liao P-C (2006) Proteomic profiling of human urinary proteome using nano-high performance liquid chromatography/electrospray ionization tandem mass spectrometry. Anal Chim Acta 579:158–176PubMedCrossRefGoogle Scholar
  44. Wang H-C, Wang H-C, Leu J-H, Kou G-H, Wang AHJ, Lo C-F (2007) Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Dev Comp Immunol 31:672–686PubMedCrossRefGoogle Scholar
  45. Warner AH, Pert MJ, Osahan JK, Zielinski BS (1995) Potential role in development of the major cysteine protease in larvae of the brine shrimp Artemia franciscana. Cell Tissue Res 282:21–31PubMedGoogle Scholar
  46. Warner AH, Pullumbi E, Amons R, Liu LQ (2004) Characterization of a cathepsin L-associated protein in Artemia and its relationship to the FAS-I family of cell adhesion proteins. Eur J Biochem 271:4014–4025PubMedCrossRefGoogle Scholar
  47. Willsie JK, Clegg JS (2001) Nuclear p26, a small heat shock/alpha-crystallin protein, and its relationship to stress resistance in Artemia franciscana embryos. J Exp Biol 204:2339–2350PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Qian Zhou
    • 1
    • 2
  • Changgong Wu
    • 1
  • Bo Dong
    • 1
  • Fengqi Liu
    • 3
  • Jianhai Xiang
    • 1
  1. 1.Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoPeople’s Republic of China
  2. 2.Graduate SchoolChinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.College of Life SciencesNankai UniversityTianjinPeople’s Republic of China

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