Reviews in Fish Biology and Fisheries

, Volume 23, Issue 2, pp 175–194 | Cite as

Molecular cloning and gene expression analysis in aquaculture science: a review focusing on respiration and immune responses in European sea bass (Dicentrarchus labrax)

  • Genciana Terova
  • Simona Rimoldi
  • Giuliana Parisi
  • Laura Gasco
  • Antonio Pais
  • Giovanni Bernardini
Reviews
  • 1.1k Downloads

Abstract

Although fish farming has been practiced for 4,000 years, aquaculture research dates back only to about 1,870, whereas molecular techniques, in addition to the more traditional methods of biotechnology, were introduced only recently. Contemporary genomic approaches (often adapted from human or medical research) such as cDNA cloning and sequencing, cDNA microarray/expression analysis, and functional genomics, combined with improvements in transgenic technologies, have enhanced possibilities for aquacultural biotechnologists for improving fish growth rates and increasing resistance to pathogens and stressors. Although genomic technologies in fish have been applied primarily to model organisms, such as zebrafish (Danio rerio), fugu or pufferfish (Tetraodon nigroviridis), and medaka (Oryzias latipes), many teleosts of interest for biological research and with potential application in aquaculture have unique physiological characteristics that cannot be directly investigated from the study of small laboratory fish models. As a consequence, large-scale genomic research studies are increasingly being applied to farmed species of economic relevance, such as farmed rainbow trout, Atlantic salmon, tilapia, catfish, and sea bass. Accordingly, we describe the utilization of molecular cloning and gene expression analysis in cultured European sea bass (Dicentrarchus labrax) to generate “transcriptome-focused” information which may enable a better understanding of the transcriptional programs that underlie fish respiratory physiology and immune response pathways.

Keywords

Aquaculture biotechnology Functional genomics Hypoxic stress biomarkers Hypercapnia Molecular cloning Gene expression Fish innate immune system 

References

  1. Adams A, Thompson KD (2006) Biotechnology offers revolution to fish health management. Trends Biotechnol 24(5):201–205PubMedGoogle Scholar
  2. Adermann K, Raida M, Paul Y, Abu-Raya S, Bloch-Shilderman E, Lazarovici P, Hochman J, Wellhoner H (1998) Isolation, characterization and synthesis of a novel paradaxin isoform. FEBS Lett 435:173–177PubMedGoogle Scholar
  3. Baltimore D (1970) RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226:1209–1221PubMedGoogle Scholar
  4. Bogut I, Milakovic Z, Pavlicevic J, Petrovic D (2006) Effect of Bio-Mos® on performance and health of European Catfish. In: Nutrition and biotechnology in the feed and food industries, Alltech’s 22nd annual symposium, suppl. 1-abstracts of posters, Lexington KY, USAGoogle Scholar
  5. Boman HG (1995) Peptide antibiotics and their role in innate immunity. Ann Rev Immunol 13:61–92Google Scholar
  6. Borgese F, Sardet C, Cappadoro M, Pouysségur J, Motais R (1992) Cloning and expression of a cAMP-activated Na+/H+ exchanger, evidence that the cytoplasmic domain mediates hormone regulation. Proc Nat Acad Sci USA 89:6765–6769PubMedGoogle Scholar
  7. Bosch TJ, Maslam S, Roberts BL (2001) Fos-like immunohistochemical identification of neurons active during the startle response of the rainbow trout. J Comp Neurol 439:306–314PubMedGoogle Scholar
  8. Burant CF, Sivitz WI, Fukumoto H, Kayano T, Nagamatsu S, Seino S, Pessin JE, Bell GI (1991) Mammalian glucose transporters, structure and molecular regulation. Recent Prog Horm Res 47:349–388PubMedGoogle Scholar
  9. Cameron JN (1985) The bone compartment in a teleost fish, Ictalurus punctatus, size, composition and acid-base response to hypercapnia. J Exp Biol 117:307–318PubMedGoogle Scholar
  10. Capilla E, Diaz M, Gutierrez J, Planas JV (2002) Physiological regulation of the expression of a GLUT4 homolog in fish skeletal muscle. Am J Physiol Endocrinol Metab 283:E44–E49PubMedGoogle Scholar
  11. Carninci P (2007) Constructing the landscape of the mammalian transcriptome. J Exp Biol 210:1497–1506PubMedGoogle Scholar
  12. Chini V, Rimoldi S, Terova G, Saroglia M, Rossi F, Bernardini G, Gornati R (2006) EST-based identification of genes expressed in the liver of adult seabass Dicentrarchus labrax, L. Gene 376:102–106PubMedGoogle Scholar
  13. Chini V, Cattaneo AG, Rossi F, Bernardini G, Terova G, Saroglia M, Gornati R (2008) Genes expressed in blue fin tuna Thunnus thynnus liver and gonads. Gene 410:207–213PubMedGoogle Scholar
  14. Claiborne JB, Blackston CR, Choe KP, Dawson DC, Harris SP, MacKenzie LA, Morrison-Shetler AI (1999) A mechanism for branchial acid excretion in marine fish, identification of multiple Na+/H+ antiporter isoforms NHE in gills of two seawater teleosts. J Exp Biol 202:315–324PubMedGoogle Scholar
  15. Cole AM, Weis P, Diamond G (1997) Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J Exp Biol 272:12008–12013Google Scholar
  16. Culjak V, Bogut G, Has-Schon E, Milakovic Z, Canecki K (2006) Effect of Bio-Mos® on performance and health of juvenile carp. In: Nutrition and biotechnology in the feed and food industries, Alltech’s 22nd annual symposium. Suppl. 1—abstracts of posters, Lexington KY, USAGoogle Scholar
  17. Dawson KA, Pirvulescu M (1999) In: Alltech’s Asia Pacific Lecture Tour, Alltech, Sydney, pp 75–83. Home page address: http://www.alltech.com/about/events/asia-pacific-lecture-tour
  18. Douglas SE, Gallant JW, Liebscher RS, Dacanay A, Tsoi SCM (2003) Identification and expression analysis of hepcidin-like antimicrobial peptides in bony fish. Dev Comp Immunol 27:589–601PubMedGoogle Scholar
  19. Ebert BL, Firth JD, Ratcliff PJ (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences. J Biol Chem 270:29083–29089PubMedGoogle Scholar
  20. Edwards SL, Claiborne JB, Morrison-Shetlar AI, Toop T (2001) NHE mRNA expression in the gill of the Atlantic hagfish Myxine glutinosa in response to metabolic acidosis. Comp Biochem Physiol A 130:81–91Google Scholar
  21. Edwards SL, Wall BP, Morrison-Shetlar A, Sligh S, Weakley JC, Claiborne JB (2005) The effect of environmental hypercapnia and salinity on the expression of NHE-like isoforms in the gills of a euryhaline fish Fundulus heteroclitus. J Exp Zool A 303:464–475Google Scholar
  22. Elgar G, Sandford R, Aparicio S, Macrae A, Venkatesh B, Brenner S (1996) Small is beautiful, comparative genomics with the pufferfish Fugu rubripes. Trends Genet 12:145–150PubMedGoogle Scholar
  23. Evans HD, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177PubMedGoogle Scholar
  24. FAO (2009) The State of World Fisheries and Aquaculture 2008. FAO, Rome. Home page address: http://www.fao.org/docrep/011/i0250e/i0250e00.htm
  25. FAO (Food and Agriculture Organization of the United Nations) (1996) Fisheries Circular No. 914 FIRI/C914, FAO, RomeGoogle Scholar
  26. Fivelstad S, Olsen AB, Asgard T, Baeverfjord G, Rasmussen T, Vindheim T, Stefansson S (2003) Long-term sublethal effects of carbon dioxide on Atlantic salmon smolts Salmo salar L., ion regulation, haematology, element composition, nephrocalcinosis and growth parameters. Aquaculture 215:301–319Google Scholar
  27. Galas DJ, McCormack SJ (2003) An historical perspective on genomic technologies. Curr Issues Mol Biol 5:123–128PubMedGoogle Scholar
  28. Grøttum JA, Sigholt T (1996) Acute toxicity of carbon dioxide on European sea bass Dicentrarchus labrax, mortality and effects on plasma ions. Comp Biochem Physiol A 115:323–327Google Scholar
  29. Hall JR, MacCormack TJ, Barry CA, Driezic WR (2004) Sequence and expression of a constitutive, facilitated glucose transporter GLUT1 in Atlantic cod Gadus morhua. J Exp Biol 207:4697–4706PubMedGoogle Scholar
  30. Hall JR, Short CE, Driezic WR (2006) Sequence of Atlantic cod Gadus morhua GLUT4, GLUT2 and GPDH, developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose. J Exp Biol 209:4490–4502PubMedGoogle Scholar
  31. Hancock RE, Scott MG (2000) The role of antimicrobial peptides in animal defences. Proc Nat Acad Sci USA 97:8856–8861PubMedGoogle Scholar
  32. Harbers M (2008) The current status of cDNA cloning. Genomics 91:232–242PubMedGoogle Scholar
  33. Heisler N (1984) Acid-base regulation in fishes. Fish Physiology 10A:315–401Google Scholar
  34. Heisler N (1986) Buffering and transmembrane ion transfer processes. In: Heisler N (ed) Acid-base regulation in animals. Elsevier, Amsterdam, pp 3–47. Available from URL: http://www.aquafeed.com/docs/papers/McLean.pdf
  35. Hirata T, Kaneko T, Ono Y, Nakazato T, Furukawa N, Hasegawa S, Wakabayashi S, Shigekawa M, Chang MH, Romero MF, Hirose S (2003) Mechanism of acid adaptation of a fish living in a pH 3.5 lake. Am J Physiol 284:R1199–R1212Google Scholar
  36. Iji PA, Saki AA, Tivey DR (2001) Intestinal structure and function of broiler chickens on diets supplemented with a mannan oligosaccharide. J Sci Food Agric 81:1186–1192Google Scholar
  37. Jobling M (1994) Fish bioenergetics. Chapman Hall, LondonGoogle Scholar
  38. Joost HG, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, Doege H, James DE, Lodish H, Moley KH, Moley JF, Mueckler M, Rogers S, Schurmann A, Seino S, Thorens B (2002) Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrinol Metab 282:E974–E976PubMedGoogle Scholar
  39. Kanaan A, Douglas RM, Alper SL, Boron WF, Haddad GG (2007) Effects of chronic elevated carbon dioxide on the expression of acid-base transporters in neonatal and adult mouse. Am J Physiol Regul Integr Comp Physiol 293:1294–1302Google Scholar
  40. Katsumata M, Burton KA, Li J, Dauncey MJ (1999) Suboptimal energy balance selectively up-regulates muscle GLUT gene expression but reduces insulin-dependent glucose uptake during postnatal development. FASEB J 13:1405–1413PubMedGoogle Scholar
  41. Krasnov A, Teerijoki H, Molsa H (2001) Rainbow trout Oncorhynchus mykiss hepatic glucose transporter. Biochim Biophys Acta 1520:174–178PubMedGoogle Scholar
  42. Kuhl H, Beck A, Wozniak G, Canario AVM, Volckaert FAM, Reinhardt R (2010) The European sea bass Dicentrarchus labrax genome puzzle, comparative BAC-mapping and low coverage shotgun sequencing. BMC Genomics 11:68PubMedGoogle Scholar
  43. Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM, Van Olst JC, Nized V, Taylor SW, Shimizu C, Bulet P (2002) Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J Biol Chem 277:5030–5039PubMedGoogle Scholar
  44. Lee KS, Kita J, Ishimatsu A (2003) Effects of lethal levels of environmental hypercapnia on cardiovascular and blood-gas status in yellowtail, Seriola quinqueradiata. Zoolog Sci 20:417–422PubMedGoogle Scholar
  45. Leturque A, Brot-Laroche E, Le Gall M, Stolarczyk E, Tobin V (2005) The role of GLUT2 in dietary sugar handling. J Physiol Biochem 61:529–538PubMedGoogle Scholar
  46. Li Y, Kim I, Kim YJ, Kim MK, Yoon YD, Lee Y, Lee J (2004) Cloning and sequence analysis of the self-fertilizing fish Rivulus marmoratus immediate early gene c-fos. Marine Environ Res 58:681–685Google Scholar
  47. Lin Z, Weinberg JM, Malhotra R, Merritt SE, Holzman LB, Brosius FC III (2000) GLUT-1 reduces hypoxia-induced apoptosis and JNK pathway activation. Am J Physiol Endocrinol Metab 278:E958–E966PubMedGoogle Scholar
  48. Matsuoka I, Fuyuki K, Shoji T, Kurihara K (1998) Identification of c-fos related genes and their induction by neural activation in rainbow trout brain. Biochim Biophys Acta 1395:220–227PubMedGoogle Scholar
  49. McGowan KM, Long SD, Pekala PH (1995) Glucose transporter gene expression, regulation of transcription and mRNA stability. Pharmacol Ther 66:465–505PubMedGoogle Scholar
  50. McLean E, Craig SR (2006) Nutrigenomics in aquaculture research, a key in the ‘Aquanomic’ revolution. In: Nutritional biotechnology in the feed and food industries: Proceedings of Alltech’s 22nd annual symposium, Lexington, Kentucky, USA, 23–26 April 2006,pp 433–444. Available from URL: http://www.cabdirect.org/abstracts/20063209187.html;jsessionid=D41BC1BB6DA94929ECEA6CCF14C17B55
  51. Melamed P, Gong Z, Fletcher G, Hew CL (2002) The potential impact of modern biotechnology on fish aquaculture. Aquaculture 204:255–269Google Scholar
  52. Miguel JC, Rodriguez-Zas SL, Pettigrew JE (2002) Practical effects of Bio-Mos® in nursery pig diets, a meta-analysis. In: Lyons TP, Jacques KA (eds) Nutritional biotechnology in the feed and food industries, from niche markets to mainstream. Proceedings of Alltech’s 18th annual symposium. Nottingham University Press, Nottingham, pp 425–433Google Scholar
  53. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I, Allard WJ, Lienhard GE, Lodish HF (1985) Sequence and structure of a human glucose transporter. Science 229:941–945PubMedGoogle Scholar
  54. Mullis KB (1990) The unusual origin of the polymerase chain reaction. Sci Am 262:56–61PubMedGoogle Scholar
  55. Oleksiak MF (2010) Genomic approaches with natural fish populations. J Fish Biol 76:1067–1093PubMedGoogle Scholar
  56. Oren Z, Shai YA (1996) Class of highly potent antibacterial peptides derived from pardaxin, a pore-forming peptide isolated from Moses sole fish Pardachirus marmoratus. Eur J Biochem 237:303–310PubMedGoogle Scholar
  57. Overturf K (2010) Convergence of aquaculture and molecular biology. In: Overturf K (ed) Molecular research in aquaculture. Wiley-Blackwell, Ames, pp 1–15Google Scholar
  58. Park CB, Lee JH, Park IY, Kim SC (1997) A novel antimicrobial peptide from the loach, Misgurnus anguillicaudatus. FEBS Lett 411:173–178PubMedGoogle Scholar
  59. Park IY, Park CB, Kim MS (1998) Parasin I, an antimicrobial peptide derived from histone H2A in the catfish, Parasilurus asotus. FEBS Lett 437:258–262PubMedGoogle Scholar
  60. Perry SF, Gilmour KM (2006) Acid-base balance and CO2 excretion in fish, unanswered questions and emerging models. Respir Physiol Neurobiol 154:199–215PubMedGoogle Scholar
  61. Peruzzi S, Chatain B, Menu B (2005) Flow cytometric determination of genome size in European seabass Dicentrarchus labrax, gilthead seabream Sparus aurata, thinlip mullet Liza ramada, and European eel Anguilla anguilla. Aquat Living Resour 18:77–81Google Scholar
  62. Pessin JE, Bell GI (1992) Mammalian facilitative glucose transporter family, structure and molecular regulation. Ann Rev Physiol 54:911–930Google Scholar
  63. Pete G, Mack SO, Haxhiu MA, Walbaum S, Gauda EB (2002) CO2-induced c-Fos expression in brainstem preprotachynin mRNA-containing neurons. Respir Physiol Neurobiol 130:265–274PubMedGoogle Scholar
  64. Planas JV, Capilla E, Gutierrez J (2000) Molecular identification of a glucose transporter from fish muscle. FEBS Lett 481:266–270PubMedGoogle Scholar
  65. Rimoldi S, Terova G, Brambilla F, Bernardini G, Gornati R, Saroglia M (2009) Molecular characterizaton and expression analysis of Na+/H+ exchanger NHE-1 and c-Fos genes in sea bass Dicentrarchus labrax, L. exposed to acute and chronic hypercapnia. J Exp Mar Biol Ecol 375:32–40Google Scholar
  66. Rinaldi L, Basso P, Tettamanti G, Grimaldi A, Terova G, Saroglia M, DeEguileor M (2005) Oxygen availability causes morphological changes and a different VEGF/Flk-1/HIF-2 expression pattern in sea bass gills. Italian J Zool 72:103–111Google Scholar
  67. Robert E, Hancock W, Chapple DS (1999) Peptide antibiotics. Antimicrob Agents Chemother 43:1317–1323Google Scholar
  68. Rossi F, Chini V, Cattaneo AG, Bernardini G, Terova G, Saroglia M, Gornati R (2007) EST-based identification of genes expressed in perch Perca fluviatilis, L. Gene Expr 14:117–127PubMedGoogle Scholar
  69. Salerno G, Parriello N, Roch P, Cammarata M (2007) cDNA sequence and tissue expression of an antimicrobial peptide, dicentracin, a new component of the moronecidin family isolated from head kidney leukocytes of sea bass, Dicentrarchus labrax. Comp Biochem Physiol B 146:521–529PubMedGoogle Scholar
  70. Salierno JD, Snyder NS, Murphy AZ, Poli M, Hall S, Baden D, Kane AS (2006) Harmful algal bloom toxins alter c-fos protein expression in the brain of killifish, Fundulus heteroclitus. Aquat Toxicol 78:350–357PubMedGoogle Scholar
  71. Sangaletti R, Terova G, Peres A, Bossi E, Corà S, Saroglia M (2009) Functional expression of the oligopeptide transporter PepT1 from the sea bass (Dicentrarchus labrax). Pflugers Arch-Eur J Physiol 459:47–54Google Scholar
  72. Sarmento A, Marques F, Ellis AE, Afonso A (2004) Modulation of the activity of sea bass Dicentrarchus labrax head-kidney macrophages by macrophage activating factors and lipopolysaccharide. Fish Shellfish Immunol 16:79–92PubMedGoogle Scholar
  73. Sato M, Mueckler M (1999) A conserved amino acid motif RXGRR in the GLUT1 glucose transporter is an important determinant of membrane topology. J Biol Chem 274:24721–24725PubMedGoogle Scholar
  74. Sato M, Severinghaus JW, Basbaum AI (1992) Medullary CO2 chemoreceptor neuron identification by c-fos immunocytochemistry. J Appl Physiol 73:96–100PubMedGoogle Scholar
  75. Scott MG, Rosenberger CM, Gold MR, Finlay B, Hancock REW (2000) An a-helical cationic antimicrobial peptide selectively modulates macrophage responses to lipopolysaccharide and directly alters macrophage gene expression. J Immunol 165:3358–3365PubMedGoogle Scholar
  76. Shimokawa N, Dikic I, Sugama S, Koibuchi N (2005) Molecular responses to acidosis of central chemosensitive neurons in brain. Cellular Signaling 17:799–808Google Scholar
  77. Smith VJ, Fernandes JMO, Jones SJ, Kemp GD, Tatner MF (2000) Antibacterial proteins in rainbow trout, Oncorhynchus mykiss. Fish Shellfish Immunol 10:243–260PubMedGoogle Scholar
  78. Söderström V, Nilsson GE (2000) Brain blood flow during hypercapnia in fish, no role of nitric oxide. Brain Res 857:207–211PubMedGoogle Scholar
  79. Soleimani M, Bookstein C, Singh G, Rao MC, Chang EB, Bastini B (1995) Differential regulation of Na+/H+ exchange and H+-ATPase by pH and HCO3 in the kidney proximal tubules. J Membr Biol 144:209–216PubMedGoogle Scholar
  80. Soncini R, Glass ML (2000) Oxygen and acid-base status related drives to gill ventilation in carp. J Fish Biol 56:528–541Google Scholar
  81. Sonmez G, Eren M (1999) Effect of supplementation of zinc bacitracin, mannan oligosaccharides, and probiotic into the broiler feeds on morphology of the small intestine. Veteriner Facultesi Dergisi Uludag Univ 18:125–138Google Scholar
  82. Staykov Y, Denev S, Spring P (2005) Influence of dietary mannan oligosaccharides Bio-Mos® on growth rate and immune function of common carp Cyprinus carpio L. In: Howell B, Flos R (eds) Lessons from the past to optimise the future. European Aquaculture Society, Special Publication No 35, pp 431–432. Available from: http://en.engormix.com/MA-aquaculture/articles/improving-growth-performance-health-t606/p0.htm
  83. Staykov Y, Spring P, Denev S, Sweetman J (2007) Effect of mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquacult Int 15:153–161Google Scholar
  84. Tankersley CG, Haxhiu MA, Gauda EB (2002) Differential CO2-induced c-fos gene expression in the nucleus tractus solitarii of inbred mouse strains. J Appl Physiol 92:1277–1284PubMedGoogle Scholar
  85. Teerijoki H, Krasnov A, Pitkanen TI, Molsa H (2000) Cloning and characterization of glucose transporter in teleost fish rainbow trout Oncorhynchus mykiss. Biochim Biophys Acta 1494:290–294PubMedGoogle Scholar
  86. Temin HM, Mizutani S (1970) RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:1209–1211Google Scholar
  87. Terova G, Gornati R, Rimoldi S, Bernardini G, Saroglia M (2005) Quantification of a glucocorticoid receptor in sea bass Dicentrarchus labrax, L. reared at high stocking densities. Gene 357:144–151PubMedGoogle Scholar
  88. 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 363:591–596PubMedGoogle Scholar
  89. Terova G, Rimoldi S, Corà S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass Dicentrarchus labrax. Aquaculture 279:150–159Google Scholar
  90. Terova G, Forchino A, Rimoldi S, Brambilla F, Antonini M, Saroglia M (2009a). Bio-Mos®: an effective inducer of dicentracin gene expression in European sea bass (Dicentrarchus labrax). Comp Biochem Physiol B 153/4:372–377Google Scholar
  91. Terova G, Rimoldi S, Brambilla F, Gornati R, Bernardini G, Saroglia M (2009b) In vivo regulation of GLUT2 mRNA in sea bass Dicentrarchus labrax in response to acute and chronic hypoxia. Comp Biochem Physiol B 152:306–316PubMedGoogle Scholar
  92. Ton C, Stamatiou D, Liew C (2003) Gene expression profile of zebrafish exposed to hypoxia during development. Physiol Genomics 13:97–106PubMedGoogle Scholar
  93. Torrecillas S, Makol A, Caballero MJ, Montero D, Robaina L, Real F, Sweetman J, Tort L, Izquierdo MS (2007) Immune stimulation and improved infection resistance in European sea bass Dicentrarchus labrax fed mannan oligosaccharides. Fish Shellfish Immunol 23:969–981PubMedGoogle Scholar
  94. Trower MK, Orton SM, Purvis IJ, Sanseau P, Riley J, Christodoulou C, Burt D, See CG, Elgar G, Sherrington R, Rogaev EI, St. George-Hyslop P, Brenner S, Dykes CW (1996) Conservation of synteny between the genome of the pufferfish Fugu rubripes and the region on human chromosome 14 14q24.3 associated with familial Alzheimer disease AD3 locus. Proc Nat Acad Sci USA 93:1366–1369PubMedGoogle Scholar
  95. Valasek MA, Repa JJ (2005) The power of real-time PCR. Adv Physiol Educ 29:151–159PubMedGoogle Scholar
  96. Vulsevic B, McNeill B, Perry SF (2006) Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J Exp Biol 209:1261–1273Google Scholar
  97. Wood IS, Trayhurn P (2003) Glucose transporters GLUT and SGLUT, expanded families of sugar transport proteins. Br J Nutr 89:3–9PubMedGoogle Scholar
  98. Wood IS, Wang B, Lorente-Cebrián S, Trayhurn P (2007) Hypoxia increases expression of selective facilitative glucose transporters GLUT and 2-deoxy-D glucose uptake in human adipocytes. Biochem Biophys Res Commun 361:468–473PubMedGoogle Scholar
  99. Wortheya EA, Myler PJ (2005) Protozoan genomes, gene identification and annotation. Int J Parasitol 35:495–512Google Scholar
  100. Wright JR Jr, O’Hali W, Yang H, Bonen A (1998) GLUT-4 deficiency and absolute peripheral resistance to insulin in the teleost fish tilapia. Gen Comp Endocrinol 111:20–27PubMedGoogle Scholar
  101. Yeku O, Scotto-Lavino E, Frohman MA (2009) Identification of alternative transcripts using rapid amplification of cDNA ends (RACE). Methods Mol Biol 590:279–294PubMedGoogle Scholar
  102. Yin ZX, He W, Chen WJ, Yan JH, Yang JN, Chan SM, He JG (2005) Cloning, expression and antimicrobial activity of antimicrobial peptide, epinecidin-1, from the orange-spotted grouper, Epinephelus coioides. Aquaculture 253:204–211Google Scholar
  103. Zhang Z, Wu RS, Mok HO, Wang Y, Poon WL, Cheng SH, Kong RY (2003) Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus. Eur J Biochem 270:3010–3017PubMedGoogle Scholar
  104. Zhang Y-A, Salinas I, Li J, Parra D, Bjork S, Xu Z, LaPatra SE, Bartholomew J, Sunyer JO (2010) IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 11(9):827–835PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Genciana Terova
    • 1
    • 2
  • Simona Rimoldi
    • 2
  • Giuliana Parisi
    • 1
    • 3
  • Laura Gasco
    • 1
    • 4
  • Antonio Pais
    • 1
    • 5
  • Giovanni Bernardini
    • 2
  1. 1.ASPA (Association for Science and Animal Production) Commission “Aquaculture”ViterboItaly
  2. 2.Department of Biotechnology and Life Sciences (DBSV)University of InsubriaVareseItaly
  3. 3.Department of Agricultural BiotechnologyUniversity of FlorenceFlorenceItaly
  4. 4.Department of Agricultural, Forestry, and Food SciencesUniversity of Studies of TurinGrugliasco (Turin)Italy
  5. 5.Section of Animal Science, Department of AgricultureUniversity of SassariSassariItaly

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