Estrogen-responsive genes in macrophages of the bony fish gilthead seabream: A transcriptomic approach

Developmental and Comparative Immunology

Volumn 35, Issue 8, 2011, Pages 840-849

  Liarte, S ^a   Chaves Pozo, E ^b   Abellan E ^b   Meseguer, J ^a   Mulero, V ^a   Canario, A V M ^c   Garcia Ayala A ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b Instituto Español de Oceanografía   (Spain)

^c UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Estrogens; Gilthead seabream; Macrophages; Transcriptomic

Indexed keywords

26S PROTEASOME REGULATORY SUBUNIT 8; ACTIN RELATED PROTEIN 2-3 COMPLEX; ACTIN RELATED PROTEIN 2-3 COMPLEX SUBUNIT 3; ACTIN RELATED PROTEIN 2-3 COMPLEX SUBUNIT 4; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; BETA ACTIN; CELL RECEPTOR; COLLAGENASE 3; COMPLEMENTARY DNA; DNA FRAGMENT; DOLICHYLDIPHOSPHOOLIGOSACCHARIDE PROTEIN GLYCOSYLTRANSFERASE SUBUNIT DAD1; ESTRADIOL; ESTROGEN; GENE PRODUCT; GLYCOSYLTRANSFERASE; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE SUBUNIT BETA; MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR 2; MACROPHAGE RECEPTOR WITH COLLAGENOUS STRUCTURE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1 ALPHA; NOD LIKE RECEPTOR C3; PEROXIREDOXIN 1; TRANSCRIPTOME; UNCLASSIFIED DRUG; WD REPEAT CONTAINING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GILTHEAD SEABREAM; HORMONE RESPONSE; HOUSEKEEPING GENE; IMMUNE RESPONSE; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TELEOST; UNINDEXED SEQUENCE; UPREGULATION;

OSTEICHTHYES; SPARUS AURATA;

EID: 79957990866     PISSN: 0145305X     EISSN: 0145305X     Source Type: Journal    
DOI: 10.1016/j.dci.2011.03.015     Document Type: Article

References (82)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
2. Anckar J., Sistonen L. SUMO: getting it on. Biochem. Soc. Trans. 2007, 35:1409-1413.
3. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., Sherlock G. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat. Genet. 2000, 25:25-29.
4. Bayne C.J., Gerwick L., Fujiki K., Nakao M., Yano T. Immune-relevant (including acute phase) genes identified in the livers of rainbow trout. Oncorhynchus mykiss, by means of suppression subtractive hybridization. Dev. Comp. Immunol. 2001, 25:205-217.
5. Bertram C., Hass R. Cellular responses to reactive oxygen species-induced DNA damage and aging. Biol. Chem. 2008, 389:211-220.
6. Bouwmeester T., Bauch A., Ruffner H., Angrand P.O., Bergamini G., Croughton K., Cruciat C., Eberhard D., Gagneur J., Ghidelli S., Hopf C., Huhse B., Mangano R., Michon A.M., Schirle M., Schlegl J., Schwab M., Stein M.A., Bauer A., Casari G., Drewes G., Gavin A.C., Jackson D.B., Joberty G., Neubauer G., Rick J., Kuster B., Superti-Furga G. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 2004, 6:97-105.
7. Brown M., Davies I.M., Moffat C.F., Robinson C., Redshaw J., Craft J.A. Identification of transcriptional effects of ethynyl oestradiol in male plaice (Pleuronectes platessa) by suppression subtractive hybridisation and a nylon maroarray. Mar. Environ. Res. 2004, 58:559-563.
8. Carmona-Saez P., Chagoyen M., Tirado F., Carazo J.M., Pascual-Montano A. GENECODIS: a web-based tool for finding significant concurrent annotations in gene lists. Genome Biol. 2007, 8:R3.
9. Castillo-Briceño P., Sepulcre M.P., Chaves-Pozo E., Meseguer J., García-Ayala A., Mulero V. Collagen regulates the activation of professional phagocytes of the teleost fish gilthead seabream. Mol. Immunol. 2009, 46:1409-1415.
10. Chang C.I., Pleguezuelos O., Zhang Y.A., Zou J., Secombes C.J. Identification of a novel cathelicidin gene in the rainbow trout, Oncorhynchus mykiss. Infect. Immun. 2005, 73:5053-5064.
11. Chang T.H., Kubota T., Matsuoka M., Jones S., Bradfute S.B., Bray M., Ozato K. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog. 2009, 5:e1000493.
12. Chapman L.M., Roling J.A., Bingham L.K., Herald M.R., Baldwin W.S. Construction of a subtractive library from hexavalent chromium treated winter flounder (Pseudopleuronectes americanus) reveals alterations in non-selenium glutathione peroxidases. Aquat. Toxicol. 2004, 67:181-194.
13. Chaves-Pozo E., Pelegrín P., Mulero V., Meseguer J., García Ayala A. A role for acidophilic granulocytes in the testis of the gilthead seabream (Sparus aurata L., Teleostei). J. Endocrinol. 2003, 179:1651-1674.
14. Chaves-Pozo E., Mulero V., Meseguer J., García Ayala A. An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L.). Biol. Reprod. 2005, 72:593-601.
15. Chaves-Pozo E., Mulero V., Meseguer J., García Ayala A. Professional phagocytic granulocytes of the bony fish gilthead seabream display functional adaptation to testicular microenvironment. J. Leukoc. Biol. 2005, 78:345-351.
16. Chaves-Pozo E., Liarte S., Vargas-Chacoff L., García-López A., Mulero V., Meseguer J., Mancera J.M., García-Ayala A. 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol. Reprod. 2007, 76:142-148.
17. Chaves-Pozo E., Liarte S., Fernández-Alacid L., Abellán E., Meseguer J., Mulero V., García-Ayala A. Pattern of expression of immune-relevant genes in the gonad of a teleost, the gilthead seabream (Sparus aurata L.). Mol. Immunol. 2008, 45:2998-3011.
18. Chaves-Pozo E., Arjona F.J., García-López A., García-Alcázar A., Meseguer J., García-Ayala A. Sex steroids and metabolic parameter levels in a seasonal breeding fish (Sparus aurata L.). Gen. Comp. Endocrinol. 2008, 156:531-536.
19. Chaves-Pozo E., Castillo-Briceño P., García-Alcázar A., Meseguer J., Mulero V., García-Ayala A. A role for matrix metalloproteinases in granulocyte infiltration and testicular remodelation in a seasonal breeding teleost. Mol. Immunol. 2008, 45:2820-2830.
20. Chen G., Shaw M.H., Kim Y.G., Nuñez G. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 2009, 4:365-398.
21. Chen Y., Wermeling F., Sundqvist J., Jonsson A.B., Tryggvason K., Pikkarainen T., Karlsson M.C. A regulatory role for macrophage class A scavenger receptors in TLR4-mediated LPS responses. Eur. J. Immunol. 2010, 40:1451-1460.
22. Chiu H., Ring B.C., Sorrentino R.P., Kalamarz M., Garza D., Govind S. dUbc9 negatively regulates the toll-NF-kappa B pathways in larval hematopoiesis and drosomycin activation in Drosophila. Dev. Biol. 2005, 288:60-72.
23. Colombo G., Gatti S., Turcatti F., Lonati C., Sordi A., Rossi G., Bonino F., Catania A. Alteration in the transcriptional profile of livers from brain-dead organ donors. Transplantation 2006, 82:69-79.
24. Conti B.J., Davis B.K., Zhang J., O'connor W., Williams K.L., Ting J.P. CATERPILLER 16.2 (CLR16.2), a novel NBD/LRR family member that negatively regulates T cell function. J. Biol. Chem. 2005, 280:18375-18385.
25. Dios S., Poisa-Beiro L., Figueras A., Novoa B. Suppression subtraction hybridization (SSH) and macroarray techniques reveal differential gene expression profiles in brain of sea bream infected with nodavirus. Mol. Immunol. 2007, 44:2195-2204.
26. Douin-Echinard V., Laffont S., Seillet C., Delpy L., Krust A., Chambon P., Gourdy P., Arnal J.F., Guéry J.C. Estrogen receptor alpha, but not beta, is required for optimal dendritic cell differentiation and CD40-induced cytokine production. J. Immunol. 2008, 180:3661-3669. Erratum in: J. Immunol. 180, 7047.
27. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 262:460-2461.
28. Eisenberg E., Levanon E.Y. Human housekeeping genes are compact. Trends Genet. 2003, 19:362-365.
29. Feng C.Y., Johnson S.C., Hori T.S., Rise M., Hall J.R., Gamperl A.K., Hubert S., Kimball J., Bowman S., Rise M.L. Identification and analysis of differentially expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonas salmonicida. Physiol. Genomics 2009, 37:149-163.
30. Fiol D.F., Kültz D. Osmotic stress sensing and signaling in fishes. FEBS J. 2007, 274:5790-5798.
31. Fu J., Xiong Y., Xu Y., Cheng G., Tang H. MDA5 is SUMOylated by PIAS2β in the upregulation of type I interferon signaling. Mol. Immunol. 2011, 48:415-422.
32. Gill G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15:536-541.
33. Goetz F.W., Iliev D.B., McCauley L.A., Liarte C.Q., Tort L.B., Planas J.V., Mackenzie S. Analysis of genes isolated from lipopolysaccharide-stimulated rainbow trout (Oncorhynchus mykiss) macrophages. Mol. Immunol. 2004, 41:1199-1210.
34. Granucci F., Petralia F., Urbano M., Citterio S., Di Tota F., Santambrogio L., Ricciardi-Castagnoli P. The scavenger receptor MARCO mediates cytoskeleton rearrangements in dendritic cells and microglia. Blood 2003, 102:2940-2947.
35. Härkönen P.L., Väänänen H.K. Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann. N. Y. Acad. Sci. 2006, 1089:218-227.
36. Hsiao L.L., Dangond F., Yoshida T., Hong R., Jensen R.V., Misra J., Dillon W., Lee K.F., Clark K.E., Haverty P., Weng Z., Mutter G.L., Frosch M.P., MacDonald M.E., Milford E.L., Crum C.P., Bueno R., Pratt R.E., Mahadevappa M., Warrington J.A., Stephanopoulos G., Stephanopoulos G., Gullans S.R. A compendium of gene expression in normal human tissues. Physiol. Genomics 2001, 7:97-104.
37. Huang X., Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999, 9:868-877.
38. Huang C.C., Duffy K.E., San Mateo L.R., Amegadzie B.Y., Sarisky R.T., Mbow M.L. A pathway analysis of poly(I:C)-induced global gene expression change in human peripheral blood mononuclear cells. Physiol. Genomics 2006, 26:125-133.
39. Iwanowicz L.R., Ottinger C.A. Estrogens, estrogen receptors and their role as immunoregulators in fish. Fish Defenses, vol. 1 2009, 277-322. Science Publisher, Enfield. G. Zaccone, J. Meseguer, A. García-Ayala, B.G. Kapoor (Eds.).
40. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K.F., Itoh M., Kawashima S., Katayama T., Araki M., Hirakawa M. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 2006, 34:D354-357.
41. Kloetzel P.M. The proteasome and MHC class I antigen processing. Biochim. Biophys. Acta 2004, 1695:225-233.
42. Kloetzel P.M., Ossendorp F. Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 2004, 16:76-81.
43. Koskinen H., Krasnov A., Rexroad C., Gorodilov Y., Afanasyev S., Mölsä H. The 14-3-3 proteins in the teleost fish rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 2004, 207:3361-3368.
44. Kubota T., Matsuoka M., Chang T.H., Tailor P., Sasaki T., Tashiro M., Kato A., Ozato K. Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J. Biol. Chem. 2008, 283:25660-25670.
45. Kültz D., Chakravarty D., Adilakshmi T. A novel 14-3-3 gene is osmoregulated in gill epithelium of the euryhaline teleost Fundulus heteroclitus. J. Exp. Biol. 2001, 204:2975-2985.
46. Kratz E., Eimon P.M., Mukhyala K., Stern H., Zha J., Strasser A., Hart R., Ashkenazi A. Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ. 2006, 13:1631-1640.
47. Krüger E., Kuckelkorn U., Sijts A., Kloetzel P.M. The components of the proteasome system and their role in MHC class I antigen processing. Rev. Physiol. Biochem. Pharmacol. 2003, 148:81-104.
48. Larkin P., Knoebl I., Denslow N.D. Differential gene expression analysis in fish exposed to endocrine disrupting compounds. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2003, 136:149-161.
49. Li T., Brouwer M. Bioinformatic analysis of expressed sequence tags from grass shrimp Palaemonetes pugio exposed to environmental stressors. Comp. Biochem. Physiol. Part D: Genomics Proteomics 2009, 4:187-195.
50. Liarte S., Chaves-Pozo E., García-Alcazar A., Mulero V., Meseguer J., García-Ayala A. Testicular involution prior to sex change in gilthead seabream is characterized by a decrease in DMRT1 gene expression and by massive leukocyte infiltration. Reprod. Biol. Endocrinol. 2007, 4:5-20.
51. Liarte S., Chaves-Pozo E., Abellán E., Meseguer J., Mulero V., García-Ayala A. 17β-Estradiol regulates gilthead seabream professional phagocyte responses through macrophage activation. Dev. Comp. Immmunol. 2011, 35:19-27.
52. Lonard D.M., Nawaz Z., Smith C.L., O'Malley B.W. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol. Cell 2000, 5:939-948.
53. Maier V.H., Dorn K.V., Gudmundsdottir B.K., Gudmundsson G.H. Characterisation of cathelicidin gene family members in divergent fish species. Mol. Immunol. 2008, 45:3723-3730.
54. Medina A., Ghahary A. Transdifferentiated circulating monocytes release exosomes containing 14-3-3 proteins with matrix metalloproteinase-1 stimulating effect for dermal fibroblasts. Wound Repair Regen. 2010, 18:245-253.
55. Moens L.N., Soetaert A., van der Ven K., Del-Favero J., De Coen W.M. Use of suppression subtractive hybridization PCR for the development of cDNA arrays for the detection of endocrine disruption in carp (Cyprinus carpio). Comp. Biochem. Physiol. Part D: Genomics Proteomics 2007, 2:18-33.
56. Morton L.M., Purdue M.P., Zheng T., Wang S.S., Armstrong B., Zhang Y., Menashe I., Chatterjee N., Davis S., Lan Q., Vajdic C.M., Severson R.K., Holford T.R., Kricker A., Cerhan J.R., Leaderer B., Grulich A., Yeager M., Cozen W., Hoar Zahm S., Chanock S.J., Rothman N., Hartge P. Risk of non-Hodgkin lymphoma associated with germline variation in genes that regulate the cell cycle, apoptosis, and lymphocyte development. Cancer Epidemiol. Biomarkers Prev. 2009, 18:1259-1270.
57. Nalbandian G., Kovats S. Understanding sex biases in immunity: Effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol. Res. 2005, 31:91-106.
58. Nilsson B.O. Modulation of the inflammatory response by estrogens with focus on the endothelium and its interactions with leukocytes. Inflamm. Res. 2007, 56:269-273.
59. Nogales-Cadenas R., Carmona-Saez P., Vazquez M., Vicente C., Yang X., Tirado F., Carazo J.M., Pascual-Montano A. GeneCodis: interpreting gene lists through enrichment analysis and integration of diverse biological information. Nucleic Acids Res. 2009, 37:W317-W322.
60. Pedra J.H., Cassel S.L., Sutterwala F.S. Sensing pathogens and danger signals by the inflammasome. Curr. Opin. Immunol. 2009, 21:10-16.
61. Pinto P.I., Teodósio H.R., Galay-Burgos M., Power D.M., Sweeney G.E., Canário A.V. Identification of estrogen-responsive genes in the testis of sea bream (Sparus auratus) using suppression subtractive hybridization. Mol. Reprod. Dev. 2006, 73:318-329.
62. Plouffe D.A., Hanington P.C., Walsh J.G., Wilson E.C., Belosevic M. Comparison of select innate immune mechanisms of fish and mammals. Xenotransplantation 2005, 12:266-277.
63. Potter N., Karakoula A., Phipps K.P., Harkness W., Hayward R., Thompson D.N., Jacques T.S., Harding B., Thomas D.G., Palmer R.W., Rees J., Darling J., Warr T.J. Genomic deletions correlate with underexpression of novel candidate genes at six loci in pediatric pilocytic astrocytoma. Neoplasia 2008, 10:757-772.
64. Prieto-Alamo M.J., Abril N., Osuna-Jiménez I., Pueyo C. Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges: large-scale identification by suppression subtractive hybridization and absolute quantification of transcriptional profiles by real-time RT-PCR. Aquat. Toxicol. 2009, 91:312-319.
65. Randelli E., Buonocore F., Scapigliati G. Cell markers and determinants in fish immunology. Fish Shellfish Immunol. 2008, 25:326-340.
66. Rise M.L., Hall J., Rise M., Hori T., Gamperl A.K., Kimball J., Hubert S., Bowman S., Johnson S.C. Functional genomic analysis of the response of Atlantic cod (Gadus morhua) spleen to the viral mimic polyriboinosinic polyribocytidylic acid (pIC). Dev. Comp. Immunol. 2008, 32:916-931.
67. Roca F.J., Sepulcre M.A., López-Castejón G., Meseguer J., Mulero V. The colony-stimulating factor-1 receptor is a specific marker of macrophages from the bony fish gilthead seabream. Mol. Immunol. 2006, 43:1418-1423.
68. Rytinki M.M., Palvimo J.J. SUMOylation modulates the transcription repressor function of RIP140. J. Biol. Chem. 2008, 283:11586-11595.
69. Saltzman A., Searfoss G., Marcireau C., Stone M., Ressner R., Munro R., Franks C., D'Alonzo J., Tocque B., Jaye M., Ivashchenko Y. hUBC9 associates with MEKK1 and type I TNF-alpha receptor and stimulates NFkappaB activity. FEBS Lett. 1998, 425:431-435.
70. Sentis S., Le Romancer M., Bianchin C., Rostan M.C., Corbo L. Sumoylation of the estrogen receptor alpha hinge region regulates its transcriptional activity. Mol. Endocrinol. 2005, 19:2671-2684.
71. Sha Z., Abernathy J.W., Wang S., Li P., Kucuktas H., Liu H., Peatman E., Liu Z. NOD-like subfamily of the nucleotide-binding domain and leucine-rich repeat containing family receptors and their expression in channel catfish. Dev. Comp. Immunol. 2009, 33:991-999.
72. Siracusa M.C., Overstreet M.G., Housseau F., Scott A.L., Klein S.L. 17Beta-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J. Immunol. 2008, 180:1423-1431.
73. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
74. Taherian A., Krone P.H., Ovsenek N. A comparison of Hsp90alpha and Hsp90beta interactions with cochaperones and substrates. Biochem. Cell Biol. 2008, 86:37-45.
75. Tang S., Zhang Z., Tan S.L., Tang M.H., Kumar A.P., Ramadoss S.K., Bajic V.B. KBERG: knowledgebase for estrogen responsive genes. Nucleic Acids Res. 2007, 35:D732-736.
76. Tashiro K., Pando M.P., Kanegae Y., Wamsley P.M., Inoue S., Verma I.M. Direct involvement of the ubiquitin-conjugating enzyme Ubc9/Hus5 in the degradation of IkappaBalpha. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:7862-7867.
77. Theil E.C. Ferritin: at the crossroads of iron and oxygen metabolism. J. Nutr. 2003, 133(Suppl 1):1549-1553.
78. Tsoi S.C., Ewart K.V., Penny S., Melville K., Liebscher R.S., Brown L.L., Douglas S.E. Identification of immune-relevant genes from Atlantic salmon using suppression subtractive hybridization. Mar. Biotechnol. 2004, 6:199-214.
79. Trinchieri G., Sher A. Cooperation of toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 2007, 7:179-190.
80. Tzivion G., Gupta V.S., Kaplun L., Balan V. 14-3-3 proteins as potential oncogenes. Semin. Cancer Biol. 2006, 16:203-213.
81. Wang L., Wu X. Identification of differentially expressed genes in lipopolysaccharide-stimulated yellow grouper Epinephelus awoara spleen. Fish Shellfish Immunol. 2007, 23:354-363.
82. Xia J.H., Yue G.H. Identification and analysis of immune-related transcriptome in Asian seabass Lates calcarifer. BMC Genomics 2010, 11:356.