Specific and non-overlapping functions of testosterone and 11-ketotestosterone in the regulation of professional phagocyte responses in the teleost fish gilthead seabream

Molecular Immunology

Volumn 53, Issue 3, 2013, Pages 218-226

  Aguila S ^a   Castillo Briceno P ^a   Sanchez M ^b   Cabas, I ^a   Garcia Alcazar A ^b   Meseguer, J ^a   Mulero, V ^a   Garcia Ayala A ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b Instituto Español de Oceanografía   (Spain)

Author keywords

11 Ketotestosterone; Acidophilic granulocytes; Immunity; Macrophages; Teleost fish; Testosterone

Indexed keywords

11 OXOTESTOSTERONE; ANDROGEN RECEPTOR; TESTOSTERONE; TOLL LIKE RECEPTOR;

ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL SPECIFICITY; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GRANULOCYTE; HORMONAL REGULATION; IMMUNITY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INFLAMMATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; RESPIRATORY BURST; SEA BREAM; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; GENE EXPRESSION; GRANULOCYTES; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; LEUKOCYTES; MACROPHAGES; MALE; PHAGOCYTES; PHAGOCYTOSIS; REACTIVE OXYGEN SPECIES; RECEPTORS, ANDROGEN; RESPIRATORY BURST; SEA BREAM; TESTOSTERONE;

MAMMALIA; SPARUS AURATA; TELEOSTEI;

EID: 84865807696     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.08.002     Document Type: Article

References (46)

1. Adori M., Kiss E., Barad Z., Barabás K., Kiszely E., Schneider A., Kövesdi D., Sziksz E., Abrahám I.M., Matkó J., Sármay G. Estrogen augments the T cell-dependent but not the T-independent immune response. Cell Mol. Life Sci. 2010, 67:1661-1674.
2. Blázquez M., Piferrer F. Sea bass (Dicentrarchus labrax) androgen receptor: cDNA cloning, tissue-specific expression and mRNA levels during early development and sex differentiation. Mol. Cell. Endocrinol. 2005, 15:23737-23748.
3. Bouman A., Heineman M.J., Faas M.M. Sex hormones and the immune response in humans. Hum. Reprod. Update 2005, 11:411-423.
4. 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.
5. Castillo-Briceño P., Cabas I., Arizcun M., Meseguer J., Mulero V., García-Ayala A. Identification of a β1 integrin isoform with restricted tissue expression in a teleost fish. Reprod. Fertil. Dev. 2011, 23:654-664.
6. Castillo-Briceño, P., águila-Martínez, S., Liarte, S., García Alcázar, A., Meseguer, J., Mulero, V., García-Ayala, A., unpublished results. Testosterone modulates in vivo the immune response of the teleost fish gilthead seabream by in situ forming microparticle system.
7. Cavaco J.E.B., Bogerd J., Goos H., Schulz R.W. Testosterone inhibits 11-ketotestosterone-induced spermatogenesis in African catfish (Clarias gariepinus). Biol. Reprod. 2001, 65:1807-1812.
8. Chaves-Pozo E., Pelegrín P., Mulero V., Meseguer J., García Ayala A. A role for acidophilic granulocytes in the testis of gilthead seabream (Sparus aurata L. Teleost). J. Endocrinol. 2003, 179:165-174.
9. 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.
10. 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.
11. 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.
12. Cohn D.A. High sensitivity to androgen as a contributing factor in sex differences in the immune response. Arthritis Rheum. 1979, 22:1217-1233.
13. Cuesta A., Vargas-Chacoff L., García-López A., Arjona F.J., Martínez-Rodríguez G., Meseguer J., Mancera J.M., Esteban M.A. Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish Shellfish Immunol. 2007, 23:693-700.
14. de Waal P.P., Wang D.S., Nijenhuis W.A., Schulz R.W., Bogerd J. Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction 2008, 136:225-234.
15. Douard V., Brunet F., Boussau B., Ahrens-Fath I., Vlaeminck-Guillem V., Haendler B., Laudet V., Guiguen Y. The fate of the duplicated androgen receptor in fishes: a late neofunctionalization event?. BMC Evol. Biol. 2008, 8:336.
16. Esteban M.A., Mulero V., Muñoz J., Meseguer J. Methodological aspects of assessing phagocytosis of Vibrio anguillarum by leucocytes of gilthead seabream (Sparus aurata L.) by flow cytometry and electron microscopy. Cell Tissue Res. 1998, 293:133-141.
17. Fairweather D., Frisancho-Kiss S., Rose N.R. Sex differences in autoimmune disease from a pathological perspective. Am. J. Pathol. 2008, 173:600-609.
18. Filipin Mdel V., Caetano L.C., Brazão V., Santello F.H., Toldo M.P., do Prado J.C. DHEA and testosterone therapies in Trypanosoma cruzi-infected rats are associated with thymic changes. Res. Vet. Sci. 2010, 89:98-103.
19. Friedman A.E. Testosterone may speed up the growth of prostate cancer due to aromatase activity. BJU Int. 2010, 106:434.
20. Gillgrass A., Chege D., Bhavanam S., Kaushic C. Estradiol limits viral replication following intravaginal immunization leading to diminished mucosal IgG response and non-sterile protection against genital herpes challenge. Am. J. Reprod. Immunol. 2010, 63:299-309.
21. Greiner S., Stefanski V., Dehnhard M., Voigt C.C. Plasma testosterone levels decrease after activation of skin immune system in a free-ranging mammal. Gen. Comp. Endocrinol. 2010, 168:466-473.
22. Hoeger B., Hitzfeld B., Köllner B., Dietrich D.R., van den Heuvel M.R. Sex and low-level sampling stress modify the impacts of sewage effluent on the rainbow trout (Oncorhynchus mykiss) immune system. Aquatic Toxicol. 2005, 73:79-90.
23. Kurtz J., Kalbe M., Langefors A., Mayer I., Milinski M., Hasselquisti D. An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. Am. Nat. 2007, 170:509-519.
24. Lee T.P., Chiang B.L. Sex differences in spontaneous versus induced animal models of autoimmunity. Autoimmun. Rev. 2012, 11:422-429.
25. Lin Q., Li M., Fang D., Fang J., Su S.B. The essential roles of Toll-like receptor signaling pathways in sterile inflammatory diseases. Int. Immunopharmacol. 2011, 11:1422-1432.
26. Mulero V., Esteban M.A., Meseguer J. Effects of in vitro addition of exogenous vitamins C and E on gilthead seabream (Sparus aurata L.) phagocytes. Vet. Immunol. Immunopathol. 1998, 66:185-199.
27. Namazi M.R. The Th1-promoting effects of dehydroepiandrosterone can provide an explanation for the stronger Th1-immune response of women. Iran J. Allergy Asthma Immunol. 2009, 8:65-69.
28. Ogino Y., Katoh H., Kuraku S., Yamada G. Evolutionary history and functional characterization of androgen receptor genes in jawed vertebrates. Endocrinology 2009, 150:5415-5427.
29. Ogino Y., Miyagawa S., Katoh H., Prins G.S., Iguchi T., Yamada G. Essential functions of androgen signaling emerged through the developmental analysis of vertebrate sex characteristics. Evol. Dev. 2011, 13:315-325.
30. Posma E., Moes H., Heineman M.J., Faas M.M. The effect of testosterone on cytokine production in the specific and non-specific immune response. Am. J. Reprod. Immunol. 2004, 52:237-243.
31. Rahman F., Christian H.C. Non-classical actions of testosterone: an update. Trends Endocrinol. Metab. 2007, 18:371-378.
32. Rebl A., Goldammer T., Seyfert H.M. Toll-like receptor signaling in bony fish. Vet. Immunol. Immunopathol. 2010, 134:139-150.
33. Rettew J.A., Huet-Hudson Y.M., Marriott I. Testosterone reduces MØ expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod. 2008, 78:432-437.
34. Roca F.J., Sepulcre M.A., López-Castejón G., Meseguer J., Mulero V. The colony-stimulating factor-1 receptor is a specific marker of MØs from the bony fish gilthead seabream. Mol. Immunol. 2006, 43:1418-1423.
35. Romano A., Rubolini D., Caprioli M., Boncoraglio G., Ambrosini R., Saino N. Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings. PLoS ONE 2011, 6:e22805.
36. Sepulcre M.P., Pelegrín P., Mulero V., Meseguer J. Characterization of gilthead seabream acidophilic granulocytes by monoclonal antibody unequivocally points to their involvement in fish phagocytic response. Cell Tissue Res. 2002, 308:97-102.
37. Sepulcre M.P., López-Castejón G., Meseguer J., Mulero V. The activation of gilthead seabream professional phagocytes by different PAMPs underlines the behavioural diversity of the main innate immune cells of bony fish. Mol. Immunol. 2007, 44:2009-2016.
38. Slater C.H., Schreck C.B. Physiological levels of testosterone kill salmonid leukocytes in vitro. Gen. Comp. Endocrinol. 1997, 106:113-119.
39. Slater C.H., Fitzpatrick M.S., Schreck C.B. Characterization of an androgen receptor in salmonid lymphocytes: possible link to androgen-induced immunosuppression. Gen. Comp. Endocrinol. 1995, 100:218-225.
40. Sperry T.S., Thomas P. Identification of two nuclear androgen receptors in kelp bass (Paralabrax clathratus) and their binding affinities for xenobiotics: comparison with Atlantic croaker (Micropogonias undulatus) androgen receptors. Biol. Reprod. 1999, 61:1152-1161.
41. Sperry T.S., Thomas P. Characterization of two nuclear androgen receptors in Atlantic croaker: comparison of their biochemical properties and binding specificities. Endocrinology 1999, 140:1602-1611.
42. Svensson E.I., McAdam A.G., Sinervo B. Intralocus sexual conflict over immune defense, gender load, and sex-specific signaling in a natural lizard population. Evolution 2009, 63:3124-3135.
43. Takeo J., Yamashita S. Two distinct isoforms of cDNA encoding rainbow trout androgen receptors. J. Biol. Chem. 1999, 274:5674-5680.
44. Watanuki H., Yamaguchi T., Sakai M. Suppression in function of phagocytic cells in common carp Cyprinus carpio L. injected with estradiol, progesterone or 11-ketotestosterone. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2002, 132:407-413.
45. Yamaguchi T., Watanuki H., Sakai M. Effects of estradiol, progesterone and testosterone on the function of carp, Cyprinus carpio, phagocytes in vitro. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2001, 129:49-55.
46. Yeh S.H., Chen P.J. Gender disparity of hepatocellular carcinoma: the roles of sex hormones. Oncology 2010, 78:172-179.