Effects of dietary inulin, Bacillus subtilis and microalgae on intestinal gene expression in gilthead seabream (Sparus aurata L.)

Fish and Shellfish Immunology

Volumn 34, Issue 3, 2013, Pages 843-848

  Cerezuela, Rebeca ^a   Meseguer, José ^a   Esteban, M Ángeles ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

Bacillus subtilis; Gilthead seabream (Sparus aurata L.); Intestine; Inulin; Microalgae

Indexed keywords

EID: 85016401456     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2012.12.026     Document Type: Article

References (55)

1. [1] Dimitroglou, A., Merrifield, D.L., Carnevali, O., Picchietti, S., Avella, M., Daniels, C., et al. Microbial manipulations to improve fish health and production – a Mediterranean perspective. Fish Shellfish Immunol 30 (2011), 1–16.
2. [2] Nayak, S.K., Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29 (2010), 2–14.
3. [3] Ring⊘, E., Olsen, R.E., Gifstad, T.Ø., Dalmo, R.A., Amlund, H., Hemre, G.-I., et al. Prebiotics in aquaculture: a review. Aquacult Nutr 16 (2010), 117–136.
4. [4] Harikrishnan, R., Kim, M.-C., Kim, J.-S., Balasundaram, C., Heo, M.-S., Protective effect of herbal and probiotics enriched diet on haematological and immunity status of Oplegnathus fasciatus (Temminck & Schlegel) against Edwardsiella tarda. Fish Shellfish Immunol 30 (2011), 886–893.
5. [5] Jovanović, B., Baran, E., Goetz, F.W., Palić, D., Effects of different lipopolysaccharide preparations on neutrophil function in the fathead minnow, Pimephales promelas Rafinesque. J Fish Dis 34 (2011), 877–880.
6. [6] Nya, E.J., Austin, B., Use of bacterial lipopolysaccharide (LPS) as an immunostimulant for the control of Aeromonas hydrophila infections in rainbow trout Oncorhynchus mykiss (Walbaum). J Appl Microbiol 108 (2010), 686–694.
7. [7] Falco, A., Frost, P., Miest, J., Pionnier, N., Irnazarow, I., Hoole, D., Reduced inflammatory response to Aeromonas salmonicida infection in common carp (Cyprinus carpio L.) fed with β-glucan supplements. Fish Shellfish Immunol 32 (2012), 1051–1057.
8. [8] Fredriksen, B.N., Sævareid, K., McAuley, L., Lane, M.E., B⊘gwald, J., Dalmo, R.A., Early immune responses in Atlantic salmon (Salmo salar L.) after immunization with PLGA nanoparticles loaded with a model antigen and β-glucan. Vaccine 29 (2011), 8338–8349.
9. [9] Pratheepa, V., Sukumaran, N., Enzymatic and protective effect analysis on pathogen infected Cyprinus carpio using Euphorbia hirta included medicated feed. Pharmacologia 3 (2012), 52–56.
10. [10] Galina, J., Yin, G., Ardó, L., Jeney, Z., The use of immunostimulating herbs in fish. An overview of research. Fish Physiol Biochem 35 (2009), 669–676.
11. [11] Kumar, R., Mukherjee, S.C., Ranjan, R., Nayak, S.K., Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish Shellfish Immunol 24 (2008), 168–172.
12. [12] Aly, S.M., Abdel-Galil Ahmed, Y., Abdel-Aziz Ghareeb, A., Mohamed, M.F., Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25 (2008), 128–136.
13. [13] Bakke-McKellep, A.M., Penn, M., Salas, P., Refstie, S., Sperstad, S., Landsverk, T., et al. Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97 (2007), 699–713.
14. [14] Ibrahem, M.D., Fathi, M., Mesalhy, S., Abd El-Aty, A.M., Effect of dietary supplementation of inulin and vitamin C on the growth, hematology, innate immunity, and resistance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 29 (2010), 241–246.
15. [15] Atalah, E., Cruz, C.M.H., Izquierdo, M.S., Rosenlund, G., Caballero, M.J., Valencia, A., et al. Two microalgae Crypthecodinium cohnii and Phaeodactylum tricornutum as alternative source of essential fatty acids in starter feeds for seabream (Sparus aurata). Aquaculture 270 (2007), 178–185.
16. [16] Ring⊘, E., Myklebust, R., Mayhew, T., Olsen, R., Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268 (2007), 251–264.
17. [17] Birkbeck, T., Ring⊘, E., Pathogenesis and the gastrointestinal tract of growing fish. Holzapfel, W., Naughton, P., (eds.) Microbial ecology in growing animals, 2005, Elsevier, Edinburgh, UK, 208–234.
18. [18] Cerezuela, R., Fumanal, M., Tapia-Paniagua, S.T., Meseguer, J., Moriñigo, M.A., Esteban, M.Á., Changes in intestinal morphology and microbiota caused by dietary administration of inulin and Bacillus subtilis in gilthead sea bream (Sparus aurata L.) specimens. 2012.
19. [19] Cerezuela, R., Guardiola, F.A., Meseguer, J., Esteban, M.A., Increases in immune parameters by inulin and Bacillus subtilis dietary administration to gilthead seabream (Sparus aurata L.) did not correlate with disease resistance to Photobacterium damselae. Fish Shellfish Immunol 32 (2012), 1032–1040.
20. [20] Cerezuela, R., Guardiola, F.A., Meseguer, J., Esteban, M.A., Enrichment of gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the immune system. Fish Physiol Biochem 38 (2012), 1729–1739.
21. [21] Cerezuela, R., Fumanal, M., Tapia-Paniagua, S.T., Meseguer, J., Moriñigo, M.A., Esteban, M.Á., Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae. Cell Tissue Res 350 (2012), 477–489.
22. [22] Salinas, I., Cuesta, A., Esteban, M.A., Meseguer, J., Dietary administration of Lactobacillus delbrüeckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish Shellfish Immunol 19 (2005), 67–77.
23. [23] Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001), 402–408.
24. [24] Alvarez-Pellitero, P., Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet Immunol Immunopathol 126 (2008), 171–198.
25. [25] Secombes, C.J., Wang, T., Hong, S., Peddie, S., Crampe, M., Laing, K.J., et al. Cytokines and innate immunity of fish. Dev Comp Immunol 25 (2001), 713–723.
26. [26] López-Castejón, G., Sepulcre, M.P., Mulero, I., Pelegrín, P., Meseguer, J., Mulero, V., Molecular and functional characterization of gilthead seabream Sparus aurata caspase-1: the first identification of an inflammatory caspase in fish. Mol Immunol 45 (2008), 49–57.
27. [27] Mohammad, M.G., Raftos, D.A., Joss, J., Cytoskeletal proteins in thymic epithelial cells of the Australian lungfish Neoceratodus forsteri. J Anat 214 (2009), 140–152.
28. [28] Kiener, T.K., Sleptsova-Friedrich, I., Hunziker, W., Identification, tissue distribution and developmental expression of tjp1/zo-1, tjp2/zo-2 and tjp3/zo-3 in the zebrafish, Danio rerio. Gene Expr Patterns 7 (2007), 767–776.
29. [29] 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 19 (1998), 145–152.
30. [30] Bates, J.M., Akerlund, J., Mittge, E., Guillemin, K., Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2 (2007), 371–382.
31. [31] Chen, K.T., Malo, M.S., Beasley-Topliffe, L.K., Poelstra, K., Millan, J.L., Mostafa, G., et al. A role for intestinal alkaline phosphatase in the maintenance of local gut immunity. Dig Dis Sci 56 (2011), 1020–1027.
32. [32] Kim, D.-H., Austin, B., Cytokine expression in leucocytes and gut cells of rainbow trout, Oncorhynchus mykiss Walbaum, induced by probiotics. Vet Immunol Immunopathol 114 (2006), 297–304.
33. [33] Pérez-Sánchez, T., Balcázar, J.L., Merrifield, D.L., Carnevali, O., Gioacchini, G., de Blas, I., et al. Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immunol 31 (2011), 196–201.
34. [34] Mulder, I.E., Wadsworth, S., Secombes, C.J., Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida. Fish Shellfish Immunol 23 (2007), 747–759.
35. [35] Angosto, D., López-Castejón, G., López-Muñoz, A., Sepulcre, M.P., Arizcun, M., Meseguer, J., et al. Evolution of inflammasome functions in vertebrates: inflammasome and caspase-1 trigger fish macrophage cell death but are dispensable for the processing of IL-1β. Innate Immun 18 (2012), 815–824.
36. [36] Koenen, T.B., Stienstra, R., van Tits, L.J., Joosten, L.A.B., van Velzen, J.F., Hijmans, A., et al. The inflammasome and caspase-1 activation: a new mechanism underlying increased inflammatory activity in human visceral adipose tissue. Endocrinology 152 (2011), 3769–3778.
37. [37] Ramsay, R.G., Ciznadija, D., Vanevski, M., Mantamadiotis, T., Transcriptional regulation of cyclo-oxygenase expression: three pillars of control. Int J Immunopath Pharmacol 16 (2003), 59–67.
38. [38] Martín Sanz, P., Hortelano, S., Bosca, L., Casado, M., Cyclooxygenase 2: understanding the pathophysiological role through genetically altered mouse models. Front Biosci 11 (2006), 2876–2888.
39. [39] Obi, S.K., Lecithinase and toxin production in Bacillus species. Zentralbl Bakteriol A 246 (1980), 415–422.
40. [40] Hong, H.A., Huang, J.-M., Khaneja, R., Hiep, L.V., Urdaci, M.C., Cutting, S.M., The safety of Bacillus subtilis and Bacillus indicus as food probiotics. J Appl Microbiol 105 (2008), 510–520.
41. [41] Dennis, E.A., Cao, J., Hsu, Y.-H., Magrioti, V., Kokotos, G., Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem Rev 111 (2011), 6130–6185.
42. 2): a review. Lipids Health Dis, 10, 2011, 170.
43. [43] Mancini, A.D., Di Battista, J.A., The cardinal role of the phospholipase A(2)/cyclooxygenase-2/prostaglandin E synthase/prostaglandin E(2) (PCPP) axis in inflammostasis. Inflamm Res 60 (2011), 1083–1092.
44. [44] Hennessey, E.S., Drummond, D.R., Sparrow, J.C., Molecular genetics of actin function. Biochem J 291 (1993), 657–671.
45. [45] Kimura, Y., Shiozaki, H., Hirao, M., Maeno, Y., Doki, Y., Inoue, M., et al. Expression of occludin, tight-junction-associated protein, in human digestive tract. Am J Pathol 151 (1997), 45–54.
46. [46] Cani, P.D., Possemiers, S., Van de Wiele, T., Guiot, Y., Everard, A., Rottier, O., et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58 (2009), 1091–1103.
47. [47] Mennigen, R., Nolte, K., Rijcken, E., Utech, M., Loeffler, B., Senninger, N., et al. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol 296 (2009), G1140–G1149.
48. [48] Huber, J.D., Witt, K.A., Hom, S., Egleton, R.D., Mark, K.S., Davis, T.P., Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression. Am J Physiol Heart C 280 (2001), H1241–H1248.
49. [49] Greenberg, S.A., Sanoudou, D., Haslett, J.N., Kohane, I.S., Kunkel, L.M., Beggs, A.H., et al. Molecular profiles of inflammatory myopathies. Neurology 59 (2002), 1170–1182.
50. [50] Stafford, J.L., Belosevic, M., Transferrin and the innate immune response of fish: identification of a novel mechanism of macrophage activation. Dev Comp Immunol 27 (2003), 539–554.
51. [51] Ong, S.T., Ho, J.Z.S., Ho, B., Ding, J.L., Iron-withholding strategy in innate immunity. Immunobiology 211 (2006), 295–314.
52. [52] García-Fernández, C., Sánchez, J.A., Blanco, G., Characterization of the gilthead seabream (Sparus aurata L.) transferrin gene: genomic structure, constitutive expression and SNP variation. Fish Shellfish Immunol 31 (2011), 548–556.
53. [53] Wang, Y., Zeng, T., Wang, S., Wang, W., Wang, Q., Yu, H.-X., Fructo-oligosaccharides enhance the mineral absorption and counteract the adverse effects of phytic acid in mice. Nutrition 26 (2010), 305–311.
54. [54] Tako, E., Glahn, R.P., Welch, R.M., Lei, X., Yasuda, K., Miller, D.D., Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Br J Nutr 99 (2008), 472–480.
55. [55] Liu, Y., Yu, S., Chai, Y., Zhu, Q., Transferrin gene expression in response to LPS challenge and heavy metal exposure in roughskin sculpin (Trachidermus fasciatus). Fish Shellfish Immunol 32 (2012), 223–229.