Estrogen signaling through the G protein-coupled estrogen receptor regulates granulocyte activation in fish

Journal of Immunology

Volumn 191, Issue 9, 2013, Pages 4628-4639

  Cabas, Isabel ^a   Rodenas, M Carmen ^a   Abellán, Emilia ^b   Meseguer, José ^a   Mulero, Victoriano ^a   García Ayala, Alfonsa ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b Instituto Español de Oceanografía   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESTROGEN; ESTROGEN RECEPTOR; G PROTEIN COUPLED ESTROGEN RECEPTOR; MESSENGER RNA; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2; PROSTAGLANDIN SYNTHASE; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE INDUCTION; GRANULOCYTE; HORMONE ACTION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MALE; MEDIATOR RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA SEQUENCE; SIGNAL TRANSDUCTION; SPARUS AURATA; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; GENETICS; IMMUNOLOGY; LEUKOCYTE ACTIVATION; METABOLISM; NEUTROPHIL; PHOSPHORYLATION; SEA BREAM;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ESTROGENS; GRANULOCYTES; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHOSPHORYLATION; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SEA BREAM; SIGNAL TRANSDUCTION;

EID: 84886005732     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301613     Document Type: Article

References (69)

1. Straub, R. H. 2007. The complex role of estrogens in inflammation. Endocr. Rev. 28: 521-574.
2. Deroo, B. J., and K. S. Korach. 2006. Estrogen receptors and human disease. J. Clin. Invest. 116: 561-570.
3. Alexander, S. P., A. Mathie, and J. A. Peters. 2011. Guide to receptors and channels (GRAC), 5th edition. Br. J. Pharmacol. 164 (Suppl. 1): S1-S324.
4. Thomas, P., Y. Pang, E. J. Filardo, and J. Dong. 2005. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146: 624-632.
5. Revankar, C. M., D. F. Cimino, L. A. Sklar, J. B. Arterburn, and E. R. Prossnitz. 2005. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307: 1625-1630.
6. Filardo, E., J. Quinn, Y. Pang, C. Graeber, S. Shaw, J. Dong, and P. Thomas. 2007. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology 148: 3236-3245.
7. Funakoshi, T., A. Yanai, K. Shinoda, M. M. Kawano, and Y. Mizukami. 2006. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem. Biophys. Res. Commun. 346: 904-910.
8. Filardo, E. J., J. A. Quinn, A. R. Frackelton, Jr., and K. I. Bland. 2002. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptorto-MAPK signaling axis. Mol. Endocrinol. 16: 70-84.
9. Filardo, E. J., J. A. Quinn, K. I. Bland, and A. R. Frackelton, Jr. 2000. Estrogeninduced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14: 1649-1660.
10. Prossnitz, E. R., and M. Maggiolini. 2009. Mechanisms of estrogen signaling and gene expression via GPR30. Mol. Cell. Endocrinol. 308: 32-38.
11. Prossnitz, E. R., and M. Barton. 2009. Signaling, physiological functions and clinical relevance of the G protein-coupled estrogen receptor GPER. Prostaglandins Other Lipid Mediat. 89: 89-97.
12. Ma, L., and G. Pei. 2007. Beta-arrestin signaling and regulation of transcription. J. Cell Sci. 120: 213-218.
13. Moriarty, K., K. H. Kim, and J. R. Bender. 2006. Minireview: estrogen receptormediated rapid signaling. Endocrinology 147: 5557-5563.
14. Bologa, C. G., C. M. Revankar, S. M. Young, B. S. Edwards, J. B. Arterburn, A. S. Kiselyov, M. A. Parker, S. E. Tkachenko, N. P. Savchuck, L. A. Sklar, et al 2006. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2: 207-212.
15. Albanito, L., A. Madeo, R. Lappano, A. Vivacqua, V. Rago, A. Carpino, T. I. Oprea, E. R. Prossnitz, A. M. Musti, S. Andò, and M. Maggiolini. 2007. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 67: 1859-1866.
16. Wang, C., B. Dehghani, I. J. Magrisso, E. A. Rick, E. Bonhomme, D. B. Cody, L. A. Elenich, S. Subramanian, S. J. Murphy, M. J. Kelly, et al 2008. GPR30 contributes to estrogen-induced thymic atrophy. Mol. Endocrinol. 22: 636-648.
17. Isensee, J., L. Meoli, V. Zazzu, C. Nabzdyk, H. Witt, D. Soewarto, K. Effertz, H. Fuchs, V. Gailus-Durner, D. Busch, et al. 2009. Expression pattern of G proteincoupled receptor 30 in LacZ reporter mice. Endocrinology 150: 1722-1730.
18. Wang, C., B. Dehghani, Y. Li, L. J. Kaler, T. Proctor, A. A. Vandenbark, and H. Offner. 2009. Membrane estrogen receptor regulates experimental autoimmune encephalomyelitis through up-regulation of programmed death 1. J. Immunol. 182: 3294-3303.
19. Blasko, E., C. A. Haskell, S. Leung, G. Gualtieri, M. Halks-Miller, M. Mahmoudi, M. K. Dennis, E. R. Prossnitz, W. J. Karpus, and R. Horuk. 2009. Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis. J. Neuroimmunol. 214: 67-77.
20. Brunsing, R. L., K. S. Owens, and E. R. Prossnitz. 2013. The G protein-coupled estrogen receptor (GPER) agonist G-1 expands the regulatory T-cell population under TH17-polarizing conditions. J. Immunother. 36: 190-196.
21. Brunsing, R. L., and E. R. Prossnitz. 2011. Induction of interleukin-10 in the T helper type 17 effector population by the G protein coupled estrogen receptor (GPER) agonist G-1. Immunology 134: 93-106.
22. Rettew, J. A., S. H. McCall, IV, and I. Marriott. 2010. GPR30/GPER-1 mediates rapid decreases in TLR4 expression on murine macrophages. Mol. Cell. Endocrinol. 328: 87-92.
23. Thomas, P., R. Alyea, Y. Pang, C. Peyton, J. Dong, and A. H. Berg. 2010. Conserved estrogen binding and signaling functions of the G protein-coupled estrogen receptor 1 (GPER) in mammals and fish. Steroids 75: 595-602.
24. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
25. Sepulcre, M. P., P. Pelegrín, V. Mulero, and J. Meseguer. 2002. Characterisation of gilthead seabream acidophilic granulocytes by a monoclonal antibody unequivocally points to their involvement in fish phagocytic response. Cell Tissue Res. 308: 97-102.
26. Mulero, I., E. Chaves-Pozo, A. García-Alcázar, J. Meseguer, V. Mulero, and A. García-Ayala. 2007. Distribution of the professional phagocytic granulocytes of the bony fish gilthead seabream (Sparus aurata L.) during the ontogeny of lymphomyeloid organs and pathogen entry sites. Dev. Comp. Immunol. 31: 1024-1033.
27. Sepulcre, M. P., G. López-Castejón, J. Meseguer, and V. Mulero. 2007. 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. 44: 2009-2016.
28. Chaves-Pozo, E., P. Pelegrín, J. García-Castillo, A. García-Ayala, V. Mulero, and J. Meseguer. 2004. Acidophilic granulocytes of the marine fish gilthead seabream (Sparus aurata L.) produce interleukin-1beta following infection with Vibrio anguillarum. Cell Tissue Res. 316: 189-195.
29. Cutolo, M., R. Brizzolara, F. Atzeni, S. Capellino, R. H. Straub, and P. C. Puttini. 2010. The immunomodulatory effects of estrogens: clinical relevance in immunemediated rheumatic diseases. Ann. N. Y. Acad. Sci. 1193: 36-42.
30. Stygar, D., B. Masironi, H. Eriksson, and L. Sahlin. 2007. Studies on estrogen receptor (ER) alpha and beta responses on gene regulation in peripheral blood leukocytes in vivo using selective ER agonists. J. Endocrinol. 194: 101-119.
31. Nalbandian, G., and S. Kovats. 2005. Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol. Res. 31: 91-106.
32. Stygar, D., P. Westlund, H. Eriksson, and L. Sahlin. 2006. Identification of wild type and variants of oestrogen receptors in polymorphonuclear and mononuclear leucocytes. Clin. Endocrinol. 64: 74-81.
33. Molero, L., M. García-Durán, J. Diaz-Recasens, L. Rico, S. Casado, and A. López-Farré. 2002. Expression of estrogen receptor subtypes and neuronal nitric oxide synthase in neutrophils from women and men: regulation by estrogen. Cardiovasc. Res. 56: 43-51.
34. Blesson, C. S., and L. Sahlin. 2012. Expression pattern and signalling pathways in neutrophil like HL-60 cells after treatment with estrogen receptor selective ligands. Mol. Cell. Endocrinol. 361: 179-190.
35. Chaves-Pozo, E., S. Liarte, L. Vargas-Chacoff, A. García- López, V. Mulero, J. Meseguer, J. M. Mancera, and A. García-Ayala. 2007. 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol. Reprod. 76: 142-148.
36. Chaves-Pozo, E., V. Mulero, J. Meseguer, and A. García-Ayala. 2005. Professional phagocytic granulocytes of the bony fish gilthead seabream display functional adaptation to testicular microenvironment. J. Leukoc. Biol. 78: 345-351.
37. Chaves-Pozo, E., P. Pelegrín, V. Mulero, J. Meseguer, and A. García-Ayala. 2003. A role for acidophilic granulocytes in the testis of the gilthead seabream (Sparus aurata L., Teleostei). J. Endocrinol. 179: 165-174.
38. Cabas, I., E. Chaves-Pozo, A. G. Alcázar, J. Meseguer, V. Mulero, and A. García-Ayala. 2011. Dietary intake of 17a-ethinylestradiol promotes leukocytes infiltration in the gonad of the hermaphrodite gilthead seabream. Mol. Immunol. 48: 2079-2086.
39. Chaves-Pozo, E., P. Castillo-Briceño, A. García- Alcázar, J. Meseguer, V. Mulero, and A. García-Ayala. 2008. A role for matrix metalloproteinases in granulocyte infiltration and testicular remodelation in a seasonal breeding teleost. Mol. Immunol. 45: 2820-2830.
40. Liarte, S., E. Chaves-Pozo, E. Abellán, J. Meseguer, V. Mulero, and A. García-Ayala. 2011. 17b-Estradiol regulates gilthead seabream professional phagocyte responses through macrophage activation. Dev. Comp. Immunol. 35: 19-27.
41. Pinto, P. I., A. L. Passos, R. S. Martins, D. M. Power, and A. V. Canário. 2006. Characterization of estrogen receptor betab in sea bream (Sparus auratus): phylogeny, ligand-binding, and comparative analysis of expression. Gen. Comp. Endocrinol. 145: 197-207.
42. Watson, C. S., Y. J. Jeng, and J. Guptarak. 2011. Endocrine disruption via estrogen receptors that participate in nongenomic signaling pathways. J. Steroid Biochem. Mol. Biol. 127: 44-50.
43. Thomas, P., and J. Dong. 2006. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J. Steroid Biochem. Mol. Biol. 102: 175-179.
44. Shved, N., G. Berishvili, H. D'Cotta, J. F. Baroiller, H. Segner, E. Eppler, and M. Reinecke. 2007. Ethinylestradiol differentially interferes with IGF-I in liver and extrahepatic sites during development of male and female bony fish. J. Endocrinol. 195: 513-523.
45. Roca, F. J., M. A. Sepulcre, G. López-Castejón, J. Meseguer, and V. Mulero. 2006. The colony-stimulating factor-1 receptor is a specific marker of macrophages from the bony fish gilthead seabream. Mol. Immunol. 43: 1418-1423.
46. Esteban, M. A., V. Mulero, J. Muñoz, and J. Meseguer. 1998. 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. 293: 133-141.
47. Mulero, V., P. Pelegrín, M. P. Sepulcre, J. Muñoz, and J. Meseguer. 2001. A fish cell surface receptor defined by a mAb mediates leukocyte aggregation and deactivation. Dev. Comp. Immunol. 25: 619-627.
48. Sepulcre, M. P., A. López-Muñoz, D. Angosto, A. García-Alcazar, J. Meseguer, and V. Mulero. 2011. TLR agonists extend the functional lifespan of professional phagocytic granulocytes in the bony fish gilthead seabream and direct precursor differentiation towards the production of granulocytes. Mol. Immunol. 48: 846-859.
49. Sumpter, J. P., and S. Jobling. 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103(Suppl. 7): 173-178.
50. Mizukami, Y. 2010. In vivo functions of GPR30/GPER-1, a membrane receptor for estrogen: from discovery to functions in vivo. Endocr. J. 57: 101-107.
51. Pang, Y., and P. Thomas. 2009. Involvement of estradiol-17beta and its membrane receptor, G protein coupled receptor 30 (GPR30) in regulation of oocyte maturation in zebrafish, Danio rario. Gen. Comp. Endocrinol. 161: 58-61.
52. Liu, X., P. Zhu, K. W. Sham, J. M. Yuen, C. Xie, Y. Zhang, Y. Liu, S. Li, X. Huang, C. H. Cheng, and H. Lin. 2009. Identification of a membrane estrogen receptor in zebrafish with homology to mammalian GPER and its high expression in early germ cells of the testis. Biol. Reprod. 80: 1253-1261.
53. Pang, Y., J. Dong, and P. Thomas. 2008. Estrogen signaling characteristics of Atlantic croaker G protein-coupled receptor 30 (GPR30) and evidence it is involved in maintenance of oocyte meiotic arrest. Endocrinology 149: 3410-3426.
54. Di Vito, C., S. Bergante, A. Balduini, A. Rastoldo, A. Bagarotti, N. Surico, A. Bertoni, and F. Sinigaglia. 2010. The oestrogen receptor GPER is expressed in human haematopoietic stem cells but not in mature megakaryocytes. Br. J. Haematol. 149: 150-152.
55. Owman, C., P. Blay, C. Nilsson, and S. J. Lolait. 1996. Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt's lymphoma and widely distributed in brain and peripheral tissues. Biochem. Biophys. Res. Commun. 228: 285-292.
56. Cabas, I., S. Liarte, A. García-Alcázar, J. Meseguer, V. Mulero, and A. García-Ayala. 2012. 17a-Ethynylestradiol alters the immune response of the teleost gilthead seabream (Sparus aurata L.) both in vivo and in vitro. Dev. Comp. Immunol. 36: 547-556.
57. Liu, F. C., Y. J. Day, J. T. Liou, H. P. Yu, and H. R. Liao. 2012. Splitomicin inhibits fMLP-induced superoxide anion production in human neutrophils by activate cAMP/PKA signaling inhibition of ERK pathway. Eur. J. Pharmacol. 688: 68-75.
58. Maggiolini, M., A. Vivacqua, G. Fasanella, A. G. Recchia, D. Sisci, V. Pezzi, D. Montanaro, A. M. Musti, D. Picard, and S. Andò. 2004. The G proteincoupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J. Biol. Chem. 279: 27008-27016.
59. Kanda, N., and S. Watanabe. 2003. 17Beta-estradiol enhances the production of nerve growth factor in THP-1-derived macrophages or peripheral blood monocyte-derived macrophages. J. Invest. Dermatol. 121: 771-780.
60. Albanito, L., D. Sisci, S. Aquila, E. Brunelli, A. Vivacqua, A. Madeo, R. Lappano, D. P. Pandey, D. Picard, L. Mauro, et al. 2008. Epidermal growth factor induces G protein-coupled receptor 30 expression in estrogen receptornegative breast cancer cells. Endocrinology 149: 3799-3808.
61. Tamassia, N., M. Zimmermann, M. Castellucci, R. Ostuni, K. Bruderek, B. Schilling, S. Brandau, F. Bazzoni, G. Natoli, and M. A. Cassatella. 2013. Cutting edge: an inactive chromatin configuration at the IL-10 locus in human neutrophils. J. Immunol. 190: 1921-1925.
62. Platzer, C., E. Fritsch, T. Elsner, M. H. Lehmann, H. D. Volk, and S. Prösch. 1999. Cyclic adenosine monophosphate-responsive elements are involved in the transcriptional activation of the human IL-10 gene in monocytic cells. Eur. J. Immunol. 29: 3098-3104.
63. Cadieux, J. S., P. Leclerc, M. St-Onge, A. A. Dussault, C. Laflamme, S. Picard, C. Ledent, P. Borgeat, and M. Pouliot. 2005. Potentiation of neutrophil cyclooxygenase-2 by adenosine: an early anti-inflammatory signal. J. Cell Sci. 118: 1437-1447.
64. Avni, D., O. Ernst, A. Philosoph, and T. Zor. 2010. Role of CREB in modulation of TNFalpha and IL-10 expression in LPS-stimulated RAW264.7 macrophages. Mol. Immunol. 47: 1396-1403.
65. Pouliot, M., M. E. Fiset, M. Massé, P. H. Naccache, and P. Borgeat. 2002. Adenosine up-regulates cyclooxygenase-2 in human granulocytes: impact on the balance of eicosanoid generation. J. Immunol. 169: 5279-5286.
66. Van Eynde, A., M. Beullens, W. Stalmans, and M. Bollen. 1994. Full activation of a nuclear species of protein phosphatase-1 by phosphorylation with protein kinase A and casein kinase-2. Biochem. J. 297: 447-449.
67. Beullens, M., A. Van Eynde, M. Bollen, and W. Stalmans. 1993. Inactivation of nuclear inhibitory polypeptides of protein phosphatase-1 (NIPP-1) by protein kinase A. J. Biol. Chem. 268: 13172-13177.
68. Otto, C., I. Fuchs, G. Kauselmann, H. Kern, B. Zevnik, P. Andreasen, G. Schwarz, H. Altmann, M. Klewer, M. Schoor, et al. 2009. GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol. Reprod. 80: 34-41.
69. Köllner, B., B. Wasserrab, G. Kotterba, and U. Fischer. 2002. Evaluation of immune functions of rainbow trout (Oncorhynchus mykiss) - how can environmental influences be detected? Toxicol. Lett. 131: 83-95.