Gene Expression Profiles of the Spleen, Liver, and Head Kidney in Turbot (Scophthalmus maximus) Along the Infection Process with Aeromonas salmonicida Using an Immune-Enriched Oligo-microarray

Marine Biotechnology

Volumn 13, Issue 6, 2011, Pages 1099-1114

  Millán, Adrián ^a   Gómez Tato, Antonio ^a   Pardo, Belén G ^a   Fernández, Carlos ^a   Bouza, Carmen ^a   Vera, Manuel ^a   Alvarez Dios, J Antonio ^a   Cabaleiro, Santiago ^b   Lamas, Jesús ^a   Lemos, Manuel L ^c   Martínez, Paulino ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b Cluster de la Acuicultura de Galicia CETGA   (Spain)

^c Santiago de Compostela Spain   (Spain)

Author keywords

Aeromonas salmonicida; Functional classification; Immune response; Oligo microarray; Scophthalmus maximus; Turbot

Indexed keywords

BIOLOGICAL ORGANS; GENES; IMMUNE SYSTEM;

AEROMONAS SALMONICIDA; FUNCTIONAL CLASSIFICATION; IMMUNE RESPONSE; SCOPHTHALMUS MAXIMUS; TURBOT;

GENE EXPRESSION;

ARRAY; BACTERIAL DISEASE; BACTERIUM; CLUSTER ANALYSIS; DATABASE; FLATFISH; FUNCTIONAL MORPHOLOGY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNE SYSTEM; INFECTIVITY; PATHOGENICITY; PHYSIOLOGICAL RESPONSE;

AEROMONAS SALMONICIDA; SCOPHTHALMIDAE; SCOPHTHALMUS MAXIMUS;

EID: 85027907831     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-011-9374-7     Document Type: Article

References (73)

1. Adzhubei AA, Vlasova AV, Hagen-Larsen H, Ruden TA, Laerdahl JK, Hoyheim B (2007) Annotated expressed sequence tags (ESTs) from pre-smolt Atlantic salmon (Salmo salar) in a searchable data resource. BMC Genomics 8: 209.
2. Allison DB, Cui XQ, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet 7: 55-65.
3. Austin B, Austin DA (1999) Bacterial fish pathogens. Diseases of farmed and wild fish. Springer, Heidelberg.
4. Brattgjerd S, Evensen O (1996) A sequential light microscopic and ultrastructural study on the uptake and handling of Vibrio salmonicida in the head kidney phagocytes of experimentally infected Atlantic salmon, Salmo salar L. Vet Pathol 33: 55-65.
5. Brown SJ, Kuhn D, Wisser R, Power E, Schnell R (2004) Quantification of sources of variation and accuracy of sequence discrimination in a replicated microarray experiment. Biotechniques 36: 324-332.
6. Cerdà J, Mercadé J, Lozano JJ, Manchado M, Tingaud-Sequeira A, Astola A, Infante C, Halm S, Viñas J, Castellana B, Asensio E, Cañavate P, Martínez-Rodríguez G, Piferrer F, Planas J, Prat F, Yúfera M, Durany O, Subirada F, Rosell E, Maes T (2008) Genomic resources for a commercial flatfish, the Senegalese sole (Solea senegalensis): EST sequencing, oligo microarray design, and development of the Soleamold bioinformatic platform. BMC Genomics 9: 508.
7. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354: 610-621.
8. Croisetiére S, Tarte PD, Bernatchez L, Belhumeur P (2008) Identification of MHC class II beta resistance/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis). Mol Immunol 45: 11.
9. Dacanay A, Knickle L, Solanky KS, Boyd JM, Walter JA, Brown LL, Johnson SC, Reith M (2006) Contribution of the type III secretion system (TTSS) to virulence of Aeromonas salmonicida subsp. salmonicida. Microbiology 152: 1847-1856.
10. Danneving BH, Lauve A, Press C, Landsverk T (1994) Receptor-mediated endocytosis and phagocytosis by rainbow trout head kidney sinusoidal cells. Fish Shellfish Immunol 4: 3-18.
11. Dinarello CA (2000) Proinflammatory cytokines. Chest 118: 503-508.
12. Dopazo J, Carazo JM (1997) Phylogenetic reconstruction using a growing neural network that adopts the topology of a phylogenetic tree. J Mol Evol 44: 226-233.
13. Draghici S, Khatri P, Eklund AC, Szallasi Z (2006) Reliability and reproducibility issues in DNA microarray measurements. Trends Genet 22: 101-109.
14. Ebanks RO, Knickle LC, Goguen M, Boyd JM, Pinto DM, Reith M, Ross NW (2006) Expression of and secretion through the Aeromonas salmonicida type III secretion system. Microbiology 152: 1275-1286.
15. Ellis AE (1997) Immunization with bacterial antigens: furunculosis. In: Gudding R, Lillehaug A, Midtlyng PJ, Brown PR (eds) Fish Vaccinology. Karger, Basel, pp 107-116.
16. Ewart KV, Belanger JC, Williams J, Karakach T, Penny S, Tsoi SC, Richards RC, Douglas SE (2005) Identification of genes differentially expressed in Atlantic salmon (Salmo salar) in response to infection by Aeromonas salmonicida using cDNA microarray technology. Dev Comp Immunol 29: 333-347.
17. Ewart KV, Williams J, Richards RC, Gallant JW, Melville K, Douglas SE (2008) The early response of Atlantic salmon (Salmo salar) macrophages exposed in vitro to Aeromonas salmonicida cultured in broth and in fish. Dev Comp Immunol 32: 380-390.
18. Fast MD, Tse B, Boyd JM, Johnson SC (2009) Mutations in the Aeromonas salmonicida subsp. salmonicida type III secretion system affect Atlantic salmon leucocyte activation and downstream immune responses. Fish Shellfish Immunol 27: 721-728.
19. Feng CY, Rise ML (2010) Characterization and expression analyses of anti-apoptotic Bcl-2-like genes NIZ-13, Mcl-1, Bcl-X1, and Bcl-X2 in Atlantic cod (Gadus morhua). Mol Immunol 47: 763-784.
20. Feng CY, Johnson SC, Hori TS, Rise M, Hall JR, Gamperl AK, Hubert S, Kimball J, Bowman S, Rise ML (2009) Identification and analysis of differentially expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonas salmonicida. Physiol Genomics 37: 149-163.
21. Ferraresso S, Vitulo N, Mininni AN, Romualdi C, Cardazzo B, Negrisolo E, Reinhardt R, Canario AVM, Patarnello T, Bargelloni L (2008) Development and validation of a gene expression oligo microarray for the gilthead sea bream (Sparus aurata). BMC Genomics 9: 580.
22. Ferraresso S, Milan M, Pellizzari C, Vitulo N, Reinhardt R, Canario AVM, Patarnello T, Bargelloni L (2010) Development of an oligo DNA microarray for the European sea bass and its application to expression profiling of jaw deformity. BMC Genomics 11: 354.
23. FEAP. 2010. Production and Price reports of member associations of the FEAP. Federation of European Aquaculture Producers. May 2010 http://www. aquamedia. org/home/default2_en. asp.
24. Filby AL, Tyler CR (2007) Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol 8: 10.
25. Fleury E, Moal J, Boulo V, Daniel JY, Mazurais D, Hénaut A, Corporeau C, Boudry P, Favrel P, Huvet A (2010) Microarray-based identification of gonad transcripts differentially expressed between lines of Pacific oyster selected to be resistant or susceptible to summer mortality. Mar Biotechnol 12: 326-339.
26. Freedman SJ (1991) The role of α2-macroglobulin in furunculosis: a comparison of rainbow trout and brook trout. Comp Biochem Physiol 98B: 549-553.
27. Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saebø S, Stet RJ (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55: 210-219.
28. Heeley DH, Hong C (1994) Isolation and characterization of tropomyosin from fish muscle. Comp Biochem Physiol Biochem Mol Biol 108: 95-106.
29. Infante C, Matsuoka MP, Asensio E, Cañavate JP, Reith M, Manchado M (2008) Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol Biol 9: 28.
30. Jorgensen SM, Afanasyev S, Krasnov A (2008) Gene expression analyses in Atlantic salmon challenged with infectious salmon anemia virus reveal differences between individuals with early, intermediate and late mortality. BMC Genomics 9: 179.
31. Kjøglum S, Larsen S, Bakke HG, Grimholt U (2008) The effect of specific MHC class I and class II combinations on resistance to furunculosis in Atlantic salmon (Salmo salar). Scand J Immunol 67: 160-168.
32. Kojima M, Kangawa K (2005) Ghrelin: structure and function. Physiol Rev 85: 495-522.
33. Komatsu K, Tsutsui S, Hino K, Araki K, Yoshiura Y, Yamamoto A, Nakamura O, Watanabe T (2009) Expression profiles of cytokines released in intestinal epithelial cells of the rainbow trout, Oncorhynchus mykiss, in response to bacterial infection. Dev Comp Immunol 33: 499-506.
34. Kumari J, Larsen AN, Bogwald J, Dalmo RA (2009a) Interleukin-17D in Atlantic salmon (Salmo salar): molecular characterization, 3D modelling and promoter analysis. Fish Shellfish Immunol 27: 647-659.
35. Kumari J, Bogwald J, Dalmo RA (2009b) Transcription factor GATA-3 in Atlantic salmon (Salmo salar): molecular characterization, promoter activity and expression analysis. Mol Immnunol 46: 3099-3107.
36. Lamas J, Ellis A (1994) Atlantic salmon (Salmo salar) neutrophil responses to Aeromonas salmonicida. Fish Shellfish Immunol 4: 201-219.
37. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
38. Lee KK, Ellis AE (1990) Glycerophospholipid: cholesterol acyltransferase complexed with LPS is a major lethal exotoxin and cytolysin of Aeromonas salmonicida: LPS stabilises and enhances toxicity of the enzyme. J Bacteriol 172: 5382-5393.
39. Lee KK, Ellis AE (1991) The role of extracellular lethal cytolysin of Aeromonas salmonicida in the pathology of furunculosis. J Fish Dis 14: 453-460.
40. Lin B, Chen S, Cao Z, Lin Y, Mo D, Zhang H, Gu J, Dong M, Liu Z, Xu A (2007) Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol Immunol 44: 295-301.
41. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
42. Lo J, Lee S, Xu M, Liu F, Ruan H, Eun A, He Y, Ma W, Wang W, Wen Z, Peng J (2005) 15, 000 Unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis. Genome Res 13: 455-466.
43. Mahlmann S, Meyerhof W, Hausmann H, Heierhorst J, Schonrock C, Zwiers H, Lederis K, Richter D (1994) Structure, function, and phylogeny of [Arg8]vasotocin receptors from teleost fish and toad. Proc Natl Acad Sci USA 91: 1342-1345.
44. Martin SA, Blaney SC, Houlihan DF, Secombes CJ (2006) Transcriptome response following administration of a live bacterial vaccine in Atlantic salmon (Salmo salar). Mol Immunol 43: 1900-1911.
45. Millán, A. (2010). Desarrollo de un microarray para la identificación de genes de resistencia a patógenos de interés industrial en rodaballo (Scophthalmus maximus). Ph. D. thesis, Universidade de Santiago de Compostela, Lugo. pp 354.
46. Millán A, Gómez-Tato A, Fernández C, Pardo BG, Álvarez-Dios JA, Calaza M, Bouza C, Vázquez M, Cabaleiro S, Martínez P (2010) Design and performance of a turbot (Scophthalmus maximus) oligo-microarray based on ESTs from immune tissues. Mar Biotechnol 12: 452-465.
47. Miron M, Woody OZ, Marcil A, Murie C, Sladek R, Nadon R (2006) A methodology for global validation of microarray experiment. BMC Bioinform 7: 333.
48. Morey JS, Ryan JC, VanDolah FM (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8: 175-193.
49. Mulder IE, Wadsworth S, Secombes CJ (2007) Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida. Fish Shellfish Immunol 23: 747-759.
50. Overturf K, LaPatra S (2006) Quantitative expression (Walbaum) of immunological factors in rainbow trout, Oncorhynchus mykiss (Walbaum), after infection with either Flavobacterium psychrophilum, Aeromonas salmonicida, or infectious haematopoietic necrosis virus. J Fish Dis 29: 215-224.
51. Pardo BG, Fernández C, Millán A, Bouza C, Vázquez-López A, Vera M, Alvarez-Dios JA, Calaza M, Gómez-Tato A, Vázquez M, Cabaleiro S, Magariños B, Lemos ML, Leiro JM, Martínez P (2008) Expressed sequence tags (ESTs) from immune tissues of turbot (Scophthalmus maximus) challenged with pathogens. BMC Vet Res 4: 37.
52. Park KC, Osborne JA, Montes A, Dios S, Nerland AH, Novoa B, Figueras A, Brown LL, Johnson SC (2009) Immunological responses of turbot (Psetta maxima) to nodavirus infection or polyriboinosinic polyribocytidylic acid (pIC) stimulation, using expressed sequence tags (ESTs) analysis and cDNA microarrays. Fish Shellfish Immunol 26: 91-108.
53. Patterson TA, Lobenhofer EK, Fulmer-Smentek SB, Collins PJ, Chu TM, Bao W, Fang H, Kawasaki ES, Hager J, Tikhonova IR, Walker SJ, Zhang L, Hurban P, de Longueville F, Fuscoe JC, Tong W, Shi L, Wolfinger RD (2006) Performance comparison of one-color and two-color platforms within the MicroArray Quality Control (MAQC) project. Nat Biotechnol 24: 1140-1150.
54. Press CM, Evensen O (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9: 309-318.
55. Rainger GE, Rowley AF (1993) Antibacterial activity in the serum and mucus of rainbow trout, Oncorhynchus mykiss, following immunisation with Aeromonas salmonicida. Fish Shellfish Immunol 3: 475-482.
56. Ramachandra L, Simmons D, Harding CV (2009) MHC molecules and microbial antigen processing in phagosomes. Curr Opin Immunol 21: 98-104.
57. Rebl A, Siegl E, Kollner B, Fischer U, Seyfert HM (2007) Characterization of twin toll-like receptors from rainbow trout (Oncorhynchus mykiss): evolutionary relationship and induced expression by Aeromonas salmonicida salmonicida. Dev Comp Immunol 31: 499-510.
58. Reith ME, Singh RK, Curtis B, Boyd JM, Bouevitch A, Kimball J, Munholland J, Murphy C, Sarty D, Williams J, Nash JH, Johnson SC, Brown LL (2008) The genome of Aeromonas salmonicida subsp. salmonicida A449: insights into the evolution of a fish pathogen. BMC Genomics 9: 427.
59. Rise ML, Jones SRM, Brown GD, von Schalburg KR, Davidson WS, Koop BF (2004) Microarray analyses identify molecular biomarkers of Atlantic salmon macrophage and hematopoietic kidney response to Piscirickettsia salmonis infection. Physiol Genomics 20: 21-35.
60. Roed KH, Fevolden SE, Fjalestad KT (2002) Disease resistance and immune characteristics in rainbow trout (Oncorhynchus mykiss) selected for lysozyme activity. Aquaculture 209: 91-101.
61. Russell S, Hayes MA, Simko E, Lumsden JS (2006) Plasma proteomic analysis of the acute phase response of rainbow trout (Oncorhynchus mykiss) to intraperitoneal inflammation and LPS injection. Dev Comp Immunol 30: 393-406.
62. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
63. Sakai DK, Kimura T (1985) Relationship between agglutinative properties of Aeromonas salmonicida strains isolated from fish in Japan and their resistance tomechanisms of host defense. Fish Pathol 20: 9-21.
64. Secombes CJ, Olivier G (1997) Host-pathogen interaction in salmonids. In: Bernorth EM, Ellis AE, Midtlyng PJ, Olivier G, Smith P (eds) Forunculosis: multidisciplinary fish disease research. Academic, San Diego, pp 269-296.
65. Skugor S, Jørgensen SM, Gjerde B, Krasnov A (2009) Hepatic gene expression profiling reveals protective responses in Atlantic salmon vaccinated against furunculosis. BMC Genomics 10: 503.
66. Sundvold H, Ruyter B, Ostbye TK, Moen T (2010) Identification of a novel allele of peroxisome proliferator-activated receptor gamma (PPARG) and its association with resistance to Aeromonas salmonicida in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 28: 394-400.
67. Tingaud-Sequeira A, Chauvigne F, Lozano J, Agulleiro MJ, Asensio E, Cerda J (2009) New insights into molecular pathways associated with flatfish ovarian development and atresia revealed by transcriptional analysis. BMC Genomics 10: 434.
68. Toranzo AE, Barja JL (1992) First report of furunculosis in turbot reared in floating cages in northwest of Spain. Bull Eur Assoc Fish Pathol 12: 147-149.
69. Toranzo AE, Santos Y, Barja JL (1997) Immunization with bacterial antigens: Vibrio infections. In: Gudding R, Lillehaug A, Midtlyng PJ, Brown F (eds) Fish Vaccinology. Karger, Basel, pp 93-105.
70. Tsoi SC, Ewart KV, Penny S, Melville K, Liebscher RS, Brown LL, Douglas SE (2004) Identification of immune-relevant genes from Atlantic salmon using suppression subtractive hybridization. Mar Biotechnol 6: 199-214.
71. Wynne JW, O'Sullivan MG, Cook MT, Stone G, Nowak BF, Lovell DR, Elliott NG (2008) Transcriptome analyses of amoebic gill disease-affected Atlantic salmon (Salmo salar) tissues reveal localized host gene suppression. Mar Biotechnol 10: 388-403.
72. Zapata AG, Chibá A, Varas A (1996) Cells and tissues of the immune system of fish. In: Iwama G, Nakanishi T (eds) The fish immune system. Organism, pathogen and environment. Academic, San Diego, pp 1-62.
73. Zapata A, Diez B, Cejalvo T, Gutiérrez-de FC, Cortés A (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20: 126-136.