Effect of different diets on proteolytic enzyme activity, trypsinogen gene expression and dietary carbon assimilation in Senegalese sole (Solea senegalensis) larvae

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 158, Issue 4, 2011, Pages 251-258

  Gamboa Delgado, Julián ^a   Le Vay, Lewis ^a   Fernández Díaz, Catalina ^b   Cañavate, Pedro ^b   Ponce, Marian ^b   Zerolo, Ricardo ^b   Manchado, Manuel ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b JUNTA DE ANDALUCÍA   (Spain)

Author keywords

Assimilation; Enzyme activity; Gene expression; Larval nutrition; Solea senegalensis; Stable isotopes; Trypsinogen

Indexed keywords

CARBON 13; CHYMOTRYPSIN; STABLE ISOTOPE; TRYPSIN; TRYPSINOGEN;

ARTEMIA; ARTICLE; CARBON FIXATION; CONTROLLED STUDY; DIET; ENZYME ACTIVITY; FISH; GENE EXPRESSION; HATCHING; LARVA; LARVAL DEVELOPMENT; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; ROTIFERA; SOLEA SENEGALENSIS; SURVIVAL RATE;

ARTEMIA; ARTEMIA SP.; ROTIFERA; SOLEA SENEGALENSIS;

EID: 79951773389     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.11.012     Document Type: Article

References (56)

1. Ahsan M.N., Watabe S. Kinetic and structural properties of two isoforms of trypsin isolated from the viscera of Japanese anchovy, Engraulis japonicus. J. Protein Chem. 2001, 20:49-58.
2. Applebaum S.L., Holt G.J. The digestive protease, chymotrypsin, as an indicator of nutritional condition in larval red drum (Sciaenops ocellatus). Mar. Biol. 2003, 142:1159-1167.
3. Asgeirsson B., Fox J.W., Bjarnason J.B. Purification and characterization of trypsin from the poikilotherm Gadus morhua. Eur. J. Biochem. 1989, 180:85-94.
4. Bolasina S., Pérez A., Yamashita Y. Digestive enzymes activity during ontogenetic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture 2006, 252:503-515.
5. Bosley K.L., Witting D.A., Chambers R.C., Wainright S.C. Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Mar. Ecol. Prog. Ser. 2002, 236:233-240.
6. Bradford M.A. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye binding. Anal. Biochem. 1976, 72:248-254.
7. Buchheister A., Latour R.J. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can. J. Fish. Aquat. Sci. 2010, 67:445-461.
8. Cahu C., Zambonino-Infante J. Substitution of live food by formulated diets in marine fish larvae. Aquaculture 2001, 200:161-180.
9. Cahu C., Zambonino-Infante J., Takeuchi T. Nutritional components affecting skeletal development in fish larvae. Aquaculture 2003, 227:245-258.
10. Cañavate J.P., Fernández-Diaz C. Influence of co-feeding larvae with live and inert diets on weaning the sole Solea senegalensis onto commercial dry feeds. Aquaculture 1999, 174:255-263.
11. Carleton S.A., Martinez Del Rio C. Growth and catabolism in isotopic incorporation: a new formulation and experimental data. Funct. Ecol. 2010, 24:805-812.
12. Chen J.M., Kukor Z., Le Marechal C., Toth M., Tsakiris L., Raguenes O., Ferec C., Sahin-Toth M. Evolution of trypsinogen activation peptides. Mol. Biol. Evol. 2003, 20:1767-1777.
13. Cunha I., Planas M. Optimal prey size for early turbot larvae (Scophthalmus maximus L.) based on mouth and ingested prey size. Aquaculture 1999, 175:103-110.
14. Engrola S., Conceição L.E.C., Dias L., Pereira R., Ribeiro L., Dinis M.T. Improving weaning strategies for Senegalese sole: effects of body weight and digestive capacity. Aquac. Res. 2007, 38:696-707.
15. Engrola S., Mai M.G., Dinis M.T., Conceição L.E.C. Co-feeding of inert diet from mouth opening does not impair protein utilization by Senegalese sole (Solea senegalensis) larvae. Aquaculture 2009, 287:185-190.
16. Engrola S., Figueira L., Conceição L.E.C., Gavaia P.J., Ribeiro L., Dinis M.T. Co-feeding in Senegalese sole larvae with inert diet from mouth opening promotes growth at weaning. Aquaculture 2009, 288:264-272.
17. Fernández-Díaz C., Yúfera M., Cañavate J.P., Moyano F.J., Alarcón F.J., Diaz M. Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J. Fish Biol. 2001, 58:1086-1097.
18. Fisk A., Sash K., Maerz J., Palmer W., Carroll J.P., MacNeil M.A. Metabolic turnover rates of carbon and nitrogen stable isotopes in captive juvenile snakes. Rapid Commun. Mass Spectrom. 2009, 23:319-326.
19. Fletcher T.S., Alhadeff M., Craik C.S., Largman C. Isolation and characterization of a cDNA encoding rat cationic trypsinogen. Biochemistry 1987, 26:3081-3086.
20. Gamboa-Delgado J., Cañavate J.P., Zerolo R., Le Vay L. Natural carbon stable isotope ratios as indicators of the relative contribution of live and inert diets to growth in larval Senegalese sole (Solea senegalensis). Aquaculture 2008, 280:190-197.
21. Gawlicka A.K., Horn M.H. Trypsin gene expression by quantitative in situ hybridization in carnivorous and herbivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol. Biochem. Zool. 2006, 79:120-132.
22. Gawlicka A., Parent B., Horn M.H., Ross N., Opstad I., Torrissen O.J. Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 2000, 184:303-314.
23. German D.P., Miles R.D. Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environ. Biol. Fish. 2010, 89:117-133.
24. Gudmundsdottir A., Palsdottir H.M. Atlantic cod trypsins: from basic research to practical applications. Mar. Biotechnol. 2005, 7:77-88.
25. 15N. Can. J. Fish. Aquat. Sci. 1993, 50:2071-2076.
26. Infante C., Matsuoka M.P., Asensio E., Cañavate J.P., Reith M., Manchado M. Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol. Biol. 2008, 9:28.
27. 15N) isotopes as natural indicators of live and dry food in Piaractus mesopotamicus (Holmberg, 1887) larval tissue. Aquac. Res. 2008, 39:370-381.
28. Kaufman M.R., Gradinger R.R., Bluhm B.A., O'Brien D.M. Using stable isotopes to assess carbon and nitrogen turnover in the Arctic sympagic amphipod (Onisimus litoralis). Oecologia 2008, 158:11-22.
29. Kolkovski S. Digestive enzymes in fish larvae and juveniles - implications and applications to formulated diets. Aquaculture 2001, 200:181-201.
30. Kolkovski S., Tandler A., Kissil G.W., Gertler A. The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream (Sparus aurata, Sparidae, Linnaeus) larvae. Fish Physiol. Biochem. 1993, 12:203-209.
31. Koven W., Kolkovski S., Hadas E., Gamsiz K., Tandler A. Advances in the development of microdiets for gilthead seabream, Sparus aurata: a review. Aquaculture 2001, 194:107-121.
32. Lauff M., Hofer R. Proteolytic enzymes in fish developed and the importance of dietary enzymes. Aquaculture 1984, 37:335-346.
33. Le Vay L., Gamboa-Delgado J. Naturally-occurring stable isotopes as direct measures of larval feeding efficiency, nutrient incorporation and turnover. Aquaculture 2010, 10.1016/j.aquaculture.2010.03.033.
34. Lemieux H., Blier P., Dutil J.D. Do digestive enzymes set a physiological limit on growth rate and food conversion efficiency in the Atlantic cod (Gadus morhua)?. Fish Physiol. Biochem. 1999, 2014:293-303.
35. -ΔΔCt method. Methods 2001, 25:402-408.
36. MacAvoy S.E., Macko S.A., Arneson L.S. Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can. J. Zool. 2005, 83:631-641.
37. Manchado M., Infante C., Asensio E., Cañavate J.P. Differential gene expression and dependence on thyroid hormones of two glyceraldehyde-3-phosphate dehydrogenases in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 2007, 400:1-8.
38. Manchado M., Infante C., Asensio E., Cañavate J.P., Douglas S.E. Comparative sequence analysis of the complete set of 40S ribosomal proteins in the Senegalese sole (Solea senegalensis Kaup) and Atlantic halibut (Hippoglossus hippoglossus L.) (Teleostei: Pleuronectiformes): phylogeny and tissue- and development-specific expression. BMC Evol. Biol. 2007, 7:107.
39. Manchado M., Infante C., Asensio E., Crespo A., Zuasti E., Cañavate J.P. Molecular characterization and gene expression of six trypsinogens in the flatfish Senegalese sole (Solea senegalensis Kaup) during larval development and in tissues. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 149:334-344.
40. Martínez del Rio C., Wolf N., Carleton S., Gannes L.Z. Isotopic ecology ten years after a call for more laboratory experiments. Biol. Rev. 2008, 84:91-111.
41. Moyano F.J., Diaz M., Alarcon F.J., Sarasquete M.C. Characterization of digestive enzyme activity during larval development of gilthead sea bream (Sparus aurata). Fish Physiol. Biochem. 1996, 15:121-130.
42. Moyano F.J., Barros A.M., Prieto A., Cañavate J.P., Cárdenas S. Evaluación de la ontogenia de enzimas digestivas en larvas de hurta, Pagrus auriga (Pisces: Sparidae). Rev. AquaTIC 2005, 22:39-47.
43. Murashita K., Fukada H., Hosokawa H., Masumoto T. Changes in cholecystokinin and peptide Y gene expression with feeding in yellowtail (Seriola quinqueradiata): relation to pancreatic exocrine regulation. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 146:318-325.
44. Nolting B., Ueberschär B., Rosenthal H. Trypsin activity and physiological aspects in larval rearing of European seabass (Dicentrarchus labrax) using live prey and compound diets. J. Appl. Ichthyol. 1999, 15:138-142.
45. Pedersen B.H., Hjelmeland K. Fate of trypsin and assimilation efficiency in larval herring Clupea harengus following digestion of copepods. Mar. Biol. 1988, 97:467-476.
46. Pedersen B.H., Nilssen E.M., Hjelmeland K. Variations in the content of trypsin and trysinogen in larval herring (Clupea harengus) digesting copepod naupli. Mar. Biol. 1987, 94:171-181.
47. Péres A., Zambonino Infante J.L., Cahu C. Dietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol. Biochem. 1998, 19:145-152.
48. Perez-Casanova J.C., Murray H.M., Gallant J.W., Ross N.W., Douglas S.E., Johnson S.C. Development of the digestive capacity in larvae of haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua). Aquaculture 2006, 251:337-401.
49. Phillips D.L., Gregg J.W. Uncertainty in source partitioning using stable isotopes. Oecologia 2001, 127:171-179. (see also erratum, Oecologia 128, 204).
50. Ribeiro L., Zambonino-Infante J.L., Cahu C., Dinis M.T. Development of digestive enzymes in larvae of Solea senegalensis, Kaup 1858. Aquaculture 1999, 179:465-473.
51. Ribeiro L., Zambonino-Infante J.L., Cahu C., Dinis M.T. Digestive enzymes profile of Solea senegalensis post larvae fed Artemia and a compound diet. Fish Physiol. Biochem. 2002, 27:61-69.
52. Rosenlund G., Stoss J., Talbot C. Co-feeding marine fish larvae with inert and live diets. Aquaculture 1997, 155:183-191.
53. Schlechtriem C., Focken U., Becker K. Stable isotopes as a tool for nutrient assimilation studies in larval fish feeding on live food. Aquat. Ecol. 2004, 38:93-100.
54. Suzuki K.W., Kasai A., Nakayama K., Tanaka M. Differential isotopic enrichment and half life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can. J. Fish. Aquat. Sci. 2005, 62:671-678.
55. Teshima S., Ishikawa M., Koshio S. Nutritional assessment and feed intake of microparticulate diets in crustacean and fish. Aquac. Res. 2000, 31:691-702.
56. Wang C., Xie S., Zhu X., Lei W., Yang Y., Liu J. Effects of age and dietary protein level on digestive enzyme activity and gene expression of Pelteobagrus fulvidraco larvae. Aquaculture 2006, 254:554-562.