Estrogen and estrogen receptor signaling promotes allergic immune responses: Effects on immune cells, cytokines, and inflammatory factors involved in allergy
Main Article Content
Keywords
Allergic disease, Estrogen, Estrogen receptor, Immune cells
Abstract
Hypersensitivity occurs when the body is stimulated by an antigen, resulting in an immune response, and leads to a physiological disorder or abnormal tissue trauma. Various immune cells, cytokines, and inflammatory mediators are involved in the immune responses related to allergic diseases, which are the core of anaphylaxis. Estrogen receptors are widely distributed in immune cells, which combine with estrogen and participate in allergic responses by affecting immune cells, cytokines, and inflammatory factors. We aimed to summarize the association between estrogen and allergic reactions to provide a scientific basis for understanding and studying the mechanisms of allergic diseases.
References
1. Ellenbogen Y, Jiménez-Saiz R, Spill P, Chu DK, Waserman S, Jordana M. The initiation of Th2 immunity towards food allergens. Int J Mol Sci. 2018;19:1447.
2. Fabián S, Ghaemmaghami AM. Allergen recognition by innate immune cells: critical role of dendritic and epithelial cells. Front Immunol. 2013;4:356.
3. He S, Zhang H, Zeng X, Yang P. Self-amplification mechanisms of mast cell activation: a new look in allergy. Curr Mol Med. 2012;12:1329-39.
4. Gonzalez-Perez A, Aponte Z, Vidaurre CF, García Rodríguez LA. Anaphylaxis epidemiology in patients with and patients without asthma: a United Kingdom database review. J Allergy Clin Immunol. 2010;125:1098-104.
5. Liew WK, Williamson E, Tang ML. Anaphylaxis fatalities and admissions in Australia. J Allergy Clin Immunol. 2009;123:434.
6. Marianne PR, Martine F, Debra S, Karl K, Tom S, Stefano L. Analysis of food-allergic and anaphylactic events in the national electronic injury surveillance system. J Allergy Clin Immunol. 2008;121:166-71.
7. Kaufmann DW. Risk of anaphylaxis in a hospital population in relation to the use of various drugs: an international study. Pharmacoepidem Drug Saf. 2003;12:195-202.
8. Bauer CS, Kampitak T, Messieh ML, Kelly K, Vadas P. Heterogeneity in presentation and treatment of catamenial anaphylaxis. Ann Allergy Asthma Immunol. 2013;111:107-11.
9. Brown AF, McKinnon D, Chu K. Emergency department anaphylaxis: a review of 142 patients in a single year. J Allergy Clin Immunol. 2001;108:861-6.
10. Poulos LM, Waters AM, Correll PK, Loblay RH, Marks GB. Trends in hospitalizations for anaphylaxis, angioedema, and urticaria in Australia, 1993-1994 to 2004-2005. J Allergy Clin Immunol. 2007;120:878-84.
11. Asero R. Sex differences in the pathogenesis of chronic urticaria. J Allergy Clin Immunol. 2003;111:425-6.
12. Dorner T, Lawrence K, Rieder A, Kunze M. Epidemiology of allergies in Austria. Results of the first Austrian allergy report. Wien Med Wochenschr. 2007;157:235-42.
13. Hox V, Desai A, Bandara G, Gilfillan AM, Metcalfe DD, Olivera A. Estrogen increases the severity of anaphylaxis in female mice through enhanced endothelial nitric oxide synthase expression and nitric oxide production. J Allergy Clin Immunol. 2015;135:729-32.
14. Cunningham M, Gilkeson G. Estrogen receptors in immunity and autoimmunity. Clin Rev Allergy Immunol. 2011;40:66-73.
15. Klein SL. Immune cells have sex and so should journal articles. Endocrinology. 2012;153:2544-50.
16. Klein SL, Jedlicka A, Pekosz A. The Xs and Y of immune responses to viral vaccines. Lancet Infect Dis. 2010;10:338-49.
17. Engler RJ, Nelson MR, Klote MM, VanRaden MJ, Huang CY, Cox NJ, et al. Half- vs full-dose trivalent inactivated influenza vaccine (2004-2005): age, dose, and sex effects on immune responses. Arch Intern Med. 2008;168:2405-14.
18. Chan HJ, Petrossian K, Chen S. Structural and functional characterization of aromatase, estrogen receptor, and their genes in endocrine-responsive and -resistant breast cancer cells. J Steroid Biol. 2016;161(SI):73-83.
19. Jordan VC, Brodie AMH. Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids. 2007;72:7-25.
20. Jordan VC, O’Malley BW. Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol. 2007;25:5815-24.
21. Lannigan DA. Estrogen receptor phosphorylation. Steroids. 2003;68:1-9.
22. Straub RH. The complex role of estrogens in inflammation. Endocr Rev. 2007;28:521-74.
23. Eigenmann PA. Mechanisms of food allergy. Pediatr Allergy Immunol. 2009;20:5-11.
24. Soon SH, See HJ, Young JS, Choi DW, Kwon DA, Bae MJ, et al. Turmeric (Curcuma longa) attenuates food allergy symptoms by regulating type1/type2 helper T cells (Th1/Th2) balance in a mouse model of food allergy. J Ethnopharmacol. 2015;175:21-9.
25. Abrahamsson TR, Abelius MS, Forsberg A, Björkstén B, Jenmalm MC. A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy. 2011;41:1729-39.
26. Siracusa MC, Saenz SA, Hill DA, Kim BS, Headley MB, Doering TA, et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature. 2011;477:229-33.
27. Teitelbaum JE, Fox VL, Twarog FJ, Nurko S, Antonioli D, Gleich G, et al. Eosinophilic esophagitis in children: immunopathological analysis and response to fluticasone propionate. Gastroenterology. 2002;122:1216-25.
28. Pali-Schöll I, Jensen-Jarolim E. Anti-acid medication as a risk factor for food allergy. Allergy. 2011;66:469-77.
29. Toyoshima S, Wakamatsu E, Ishida Y, Obata Y, Kurashima Y, Kiyono H, et al. The spleen is the site where mast cells are induced in the development of food allergy. Int Immunol. 2017;29:31-45.
30. Chen W, Mempel M, Schober W, Behrendt H, Ring J. Gender difference, sex hormones, and immediate-type hypersensitivity reactions. Allergy. 2008;63:1418-27.
31. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, et al. Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus. 2004;13: 635-8.
32. Narita S, Goldblum RM, Watson CS, Brooks EG, Estes DM, Curran EM, et al. Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ Health Perspec. 2007;115:48-52.
33. Variadic M, Kempuraj D, Boucher W, Kalogeromitros D, Theoharides TC. Progesterone inhibits mast cell secretion. Int J Immunopathol Pharmacol. 2006;19:787-94.
34. Zaitsu M, Narita S, Lambert KC, Grady JJ, Estes DM, Curran EM, et al. Estradiol activates mast cells via a non-genomic estrogen receptor-alpha and calcium influx. Mol Immunol. 2007;44:1977-85.
35. Piotr H, Pawel D, Karin H. Dendritic cells and their role in allergy: uptake. Proteolytic processing and presentation of allergens. Int J Mol Sci. 2017;18:1491.
36. Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease a role of estrogen signaling? Arterioscler Thromb Vasc Biol. 2013;33:1127-34.
37. Masuda C, Miyasaka T, Kawakami K, Inokuchi J, Kawano T, Dobashi-Okuyama K, et al. Sex-based differences in CD103 + dendritic cells promote female-predominant Th2 cytokine production during allergic asthma. Clin Exp Allergy. 2018;48:379-93.
38. Shen C, Detry B, Lecocq M, Pilette C. A novel IgA/Delta-like 4/Notch axis induces immunosuppressive activity in human dendritic cells. Clin Immunol. 2016;168:37-46.
39. Wei Z, Yan X. The roles of estrogen and its receptors in autoimmune diseases. Int J Immunol. 2010;33:35.
40. Elgart BN, Oriss TB, Qi Z, Dixon-McCarthy B, Geerlings M, Hylkema MN, et al. Macrophages: regulators of sex differences in asthma? Am J Respir Cell Mol Biol. 2010;42:595-603.
41. Susan K. Estrogen receptors regulate an inflammatory pathway of dendritic cell differentiation: mechanisms and implications for immunity. Horm Behav. 2012;62:254-62.
42. Kumar S, Dwivedi PD, Das M, Tripathi A. Macrophages in food allergy: an enigma. Mol Immunol. 2013;56:612-8.
43. Li Z, Ju Z, Fieri M. The T-cell immunoglobulin and mucin domain (Tim) gene family in asthma, allergy, and autoimmunity. Allergy Asthma Proc. 2013;34:21-6.
44. Carreras E, Turner S, Frank MB, Knowlton N, Osban J, Centola M, et al. Estrogen receptor signaling promotes dendritic cell differentiation by increasing expression of the transcription factor IRF4. Blood. 2010;115:238-46.
45. Teixeira D, Marques C, Pestana D, Faria A, Norberto S, Calhau C, et al. Effects of xenoestrogens in human M1 and M2 macrophage migration, cytokine release, and estrogen-related signaling pathways. Environ Toxicol. 2015;31:1496-509.
46. Bolego C, Cignarella A, Staels B, Chinettigbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscl Throm Vasc Bio. 2013;33:1127-34.
47. Toniolo A. Polarization in patterns of human monocyte-derived macrophages in relation to estrogen treatment and menopausal status. Adv Mater Res. 2014;15:15-26.
48. Smith KA, Hochweller K, Hämmerling GJ, Boon L, MacDonald AS, Maizels RM. Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103-dendritic cells. J Immunol. 2011;186:7098-109.
49. Van Rijt LS, Vos N, Willart M, Muskens F, Tak PP, van der Horst C, et al. Persistent activation of dendritic cells after resolution of allergic airway inflammation breaks tolerance to inhaled allergens in mice. Am J Respir Crit Care Med. 2011;184:303-11.
50. Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, Kool M, et al. Inflammatory dendritic cells -not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med. 2010;207:2097-111.
51. Kool M, Soulliã T, Van Nimwegen M, Willart MA, Muskens F, Jung SN, et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med. 2008;205:869-82.
52. Hee SS, Hye-Jeong S, Sun YJ, Dae WC, Da-Ae K, Min-Jung B, et al. Turmeric (Curcuma longa) attenuates food allergy symptoms by regulating type 1/type 2 helper T cells (Th1/Th2) balance in a mouse model of food allergy. J Ethnopharmacol. 2015;175:21-9.
53. Abrahamsson TR, Abelius MS, Forsberg A, Björkstén B, Jenmalm MC. A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy. 2011;41:1729-39.
54. Voskamp AL, Leiden U. Clinical allergy: basophils, T cells, and therapeutic design. Leiden Univ Repos. 2016;24:06-16.
55. Zhang L, Zhao MJ, Hu MX, Xu XJ. Effect of pregnancy concentration of progestin on the immune function of T lymphocytes in peripheral blood of ovariectomized mice. J Reprod Med. 2012;21:489.
56. Hasegawa A, Miki T, Hosokawa H, Hossain MB, Shimizu C, Hashimoto K, et al. Impaired GATA3-dependent chromatin remodeling and Th2 cell differentiation leading to attempted allergic airway inflammation in aging mice. J Immunol. 2006;176:2546-54.
57. Liu L, Su SG, Zhang XK, Yang SJ. Serum levels of sex hormone and interferon-gamma, interleukin-4 in patients with Graves’ disease and their relationship. Clin Focus. 2007;22:1768-72.
58. Hong CC, Pajak A, Teitelbaum SL. Younger pubertal age is associated with allergy and other atopic conditions in girls. Pediatr Allergy Immunol. 2015;25:773-80.
59. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med. 2012;18:673-83.
60. Josaine A, Mausumi B, Mark K, Subhajit D. Estrogen receptor signal in regulation of B cell activation during diverse immune responses. Int J Biochem Cell Bio. 2015;68:42-7.
61. Fu Y1, Li L, Liu X, Ma C, Zhang J, Jiao Y, et al. Estrogen promotes B cell activation in vitro through down-regulating CD80 molecule expression. Gynecol Endocrinol. 2011;27:593-6.
62. Bernardi AI, Andersson A, Grahnemo L, Nurkkala-Karlsson M, Ohlsson C, Carlsten H, et al. Effects of lasofoxifene and bazedoxifene on B cell development and function. Immun Inflamm Dis. 2014;2:214-25.
63. Saulep-Easton D, Vincent FB, Quah PS, Wei A, Ting SB, Croce CM, et al. The BAFF receptor TACI controls IL-10 production by regulatory B cells and CLL B cells. Leukemia. 2016;30:163-72.
64. Jimbo S, Griebel PJ, Townsend H, Babiuk LA, Mutwiri G. Evidence for the existence of regulatory and effector B cell populations in Peyer’s patches of sheep. Vet Immunol Immunop. 2016;174:6-34.
65. Linhart B, Valenta R. Mechanisms underlying allergy vaccination with recombinant hypoallergenic allergen derivatives. Vaccine. 2012;30:4328-35.
66. Cooper AM, Hobson PS, Jutton MR, Kao MW, Drung B, Schmidt B, et al. Soluble CD23 controls IgE synthesis and homeostasis in human B cells. J Immunol. 2012;188:3199-207.
67. Cecilia E, Albert B, Ulrike H, Jasmin R, René P, Alessandro C, et al. Estrogen induces St6gal1 expression and increases IgG sialylation in mice and patients with rheumatoid arthritis: a potential explanation for the increased risk of rheumatoid arthritis in postmenopausal women. Arthritis Res Ther. 2018;20:84.
68. Tohru S, Sakina F, Mariko N, Emi S, Toshio H, Yasuhiko N, et al. The soy isoflavone equol enhances antigen-specific IgE production in ovalbumin-immunized BALB/c mice. J Nutr Sci Vitaminol. 2010;56:72-6.
69. Geunwoong N, Jaeho L. Regulatory B cells and allergic diseases. Allergy Asthma Immunol Res. 2011;3:168-77.
70. MacDonald T. Immunosuppression caused by antigen feeding II. Suppressor T cells mask Peyer’s patch B cell priming to orally administered antigen. Eur J Immunol. 1983;13: 138-42.
71. Reber LL, Frossard N. Targeting mast cells in inflammatory diseases. Pharmacol Ther. 2014;142:416-35.
72. Rana SB, Terumi M. Estrogen effects in allergy and asthma. Curr Opin Allergy Clin Immunol. 2013;13:92-9.
73. Jing H, Wang Z, Chen Y. Effect of oestradiol on mast cell number and histamine level in the mammary glands of rat. Anat Histol Embryol. 2012;41:170-6.
74. Federico J, Mariana W, Ana T, Katja W, Florin T, Serban C, et al. Estradiol and progesterone regulate the migration of mast cells from the periphery to the uterus and induce their maturation and degranulation. PLoS One. 2010;5: e14409.
75. Kennedy RH, Pelletier JH, Tupper EJ, Hutchinson LM, Gosse JA. Estrogen mimetic 4-tert-octylphenol enhances IgE-mediated degranulation of RBL-2H3 mast cells. J Toxicol Environ Health A. 2012;75:1451-5.
76. Takeda M, Tanabe M, Ito W, Ueki S, Konnno Y, Chihara M, et al. Gender difference in allergic airway remodelling and immunoglobulin production in a mouse model of asthma. Respirology. 2013;18:797-806.
77. Blacquiere MJ, Hylkema MN, Postma DS, Geerlings M, Timens W, Melgert BN. Airway inflammation and remodeling in two mouse models of asthma: comparison of males and females. Int Arch Allergy Immunol. 2010;153:173-81.
78. Narita S, Goldblum RM, Watson CS, Brooks EG, Estes DM, Edward M. Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ Health Persp. 2007;1:48-52.
79. Munozcruz ˜ S, Mendozarodríguez Y, Navacastro KE, Yepezmulia L, Moralesmontor J. Gender-related effects of sex steroids on histamine release and FcR1 expression in rat peritoneal mast cells. J Immunol Res. 2015;2015:351829.
80. Janicki JS, Spinale FG, Levick SP. Gender differences in nonischemic myocardial remodeling: are they due to estrogen modulation of cardiac mast cells and/or membrane type 1 matrix metalloproteinase. Pflügers Arch Eur J Physiol. 2013;465:687-97.
81. Zierau O, Zenclusse AC, Jensen F. Role of female sex hormones, estradiol and progesterone, in mast cell behavior. Front Immunol. 2012;3:169.
82. Zhu T, Ding S, Li T, Zhu L, Huang X. Estrogen is an important mediator of mast cell activation in ovarian endometriomas. Reproduction. 2017;155. REP-17-0457.
83. Saito H, Ishizaka T, Ishizaka K. Mast cells and IgE: from history to today. Allergol Int. 2013;62:3-12.
84. Kvedariene V, Martins P, Rouanet L, Demoly P. Diagnosis of iodinated contrast media hypersensitivity: results of a 6-year period. Clin Exp Allergy. 2006;36:1072-7.
2. Fabián S, Ghaemmaghami AM. Allergen recognition by innate immune cells: critical role of dendritic and epithelial cells. Front Immunol. 2013;4:356.
3. He S, Zhang H, Zeng X, Yang P. Self-amplification mechanisms of mast cell activation: a new look in allergy. Curr Mol Med. 2012;12:1329-39.
4. Gonzalez-Perez A, Aponte Z, Vidaurre CF, García Rodríguez LA. Anaphylaxis epidemiology in patients with and patients without asthma: a United Kingdom database review. J Allergy Clin Immunol. 2010;125:1098-104.
5. Liew WK, Williamson E, Tang ML. Anaphylaxis fatalities and admissions in Australia. J Allergy Clin Immunol. 2009;123:434.
6. Marianne PR, Martine F, Debra S, Karl K, Tom S, Stefano L. Analysis of food-allergic and anaphylactic events in the national electronic injury surveillance system. J Allergy Clin Immunol. 2008;121:166-71.
7. Kaufmann DW. Risk of anaphylaxis in a hospital population in relation to the use of various drugs: an international study. Pharmacoepidem Drug Saf. 2003;12:195-202.
8. Bauer CS, Kampitak T, Messieh ML, Kelly K, Vadas P. Heterogeneity in presentation and treatment of catamenial anaphylaxis. Ann Allergy Asthma Immunol. 2013;111:107-11.
9. Brown AF, McKinnon D, Chu K. Emergency department anaphylaxis: a review of 142 patients in a single year. J Allergy Clin Immunol. 2001;108:861-6.
10. Poulos LM, Waters AM, Correll PK, Loblay RH, Marks GB. Trends in hospitalizations for anaphylaxis, angioedema, and urticaria in Australia, 1993-1994 to 2004-2005. J Allergy Clin Immunol. 2007;120:878-84.
11. Asero R. Sex differences in the pathogenesis of chronic urticaria. J Allergy Clin Immunol. 2003;111:425-6.
12. Dorner T, Lawrence K, Rieder A, Kunze M. Epidemiology of allergies in Austria. Results of the first Austrian allergy report. Wien Med Wochenschr. 2007;157:235-42.
13. Hox V, Desai A, Bandara G, Gilfillan AM, Metcalfe DD, Olivera A. Estrogen increases the severity of anaphylaxis in female mice through enhanced endothelial nitric oxide synthase expression and nitric oxide production. J Allergy Clin Immunol. 2015;135:729-32.
14. Cunningham M, Gilkeson G. Estrogen receptors in immunity and autoimmunity. Clin Rev Allergy Immunol. 2011;40:66-73.
15. Klein SL. Immune cells have sex and so should journal articles. Endocrinology. 2012;153:2544-50.
16. Klein SL, Jedlicka A, Pekosz A. The Xs and Y of immune responses to viral vaccines. Lancet Infect Dis. 2010;10:338-49.
17. Engler RJ, Nelson MR, Klote MM, VanRaden MJ, Huang CY, Cox NJ, et al. Half- vs full-dose trivalent inactivated influenza vaccine (2004-2005): age, dose, and sex effects on immune responses. Arch Intern Med. 2008;168:2405-14.
18. Chan HJ, Petrossian K, Chen S. Structural and functional characterization of aromatase, estrogen receptor, and their genes in endocrine-responsive and -resistant breast cancer cells. J Steroid Biol. 2016;161(SI):73-83.
19. Jordan VC, Brodie AMH. Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids. 2007;72:7-25.
20. Jordan VC, O’Malley BW. Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol. 2007;25:5815-24.
21. Lannigan DA. Estrogen receptor phosphorylation. Steroids. 2003;68:1-9.
22. Straub RH. The complex role of estrogens in inflammation. Endocr Rev. 2007;28:521-74.
23. Eigenmann PA. Mechanisms of food allergy. Pediatr Allergy Immunol. 2009;20:5-11.
24. Soon SH, See HJ, Young JS, Choi DW, Kwon DA, Bae MJ, et al. Turmeric (Curcuma longa) attenuates food allergy symptoms by regulating type1/type2 helper T cells (Th1/Th2) balance in a mouse model of food allergy. J Ethnopharmacol. 2015;175:21-9.
25. Abrahamsson TR, Abelius MS, Forsberg A, Björkstén B, Jenmalm MC. A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy. 2011;41:1729-39.
26. Siracusa MC, Saenz SA, Hill DA, Kim BS, Headley MB, Doering TA, et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature. 2011;477:229-33.
27. Teitelbaum JE, Fox VL, Twarog FJ, Nurko S, Antonioli D, Gleich G, et al. Eosinophilic esophagitis in children: immunopathological analysis and response to fluticasone propionate. Gastroenterology. 2002;122:1216-25.
28. Pali-Schöll I, Jensen-Jarolim E. Anti-acid medication as a risk factor for food allergy. Allergy. 2011;66:469-77.
29. Toyoshima S, Wakamatsu E, Ishida Y, Obata Y, Kurashima Y, Kiyono H, et al. The spleen is the site where mast cells are induced in the development of food allergy. Int Immunol. 2017;29:31-45.
30. Chen W, Mempel M, Schober W, Behrendt H, Ring J. Gender difference, sex hormones, and immediate-type hypersensitivity reactions. Allergy. 2008;63:1418-27.
31. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, et al. Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus. 2004;13: 635-8.
32. Narita S, Goldblum RM, Watson CS, Brooks EG, Estes DM, Curran EM, et al. Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ Health Perspec. 2007;115:48-52.
33. Variadic M, Kempuraj D, Boucher W, Kalogeromitros D, Theoharides TC. Progesterone inhibits mast cell secretion. Int J Immunopathol Pharmacol. 2006;19:787-94.
34. Zaitsu M, Narita S, Lambert KC, Grady JJ, Estes DM, Curran EM, et al. Estradiol activates mast cells via a non-genomic estrogen receptor-alpha and calcium influx. Mol Immunol. 2007;44:1977-85.
35. Piotr H, Pawel D, Karin H. Dendritic cells and their role in allergy: uptake. Proteolytic processing and presentation of allergens. Int J Mol Sci. 2017;18:1491.
36. Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease a role of estrogen signaling? Arterioscler Thromb Vasc Biol. 2013;33:1127-34.
37. Masuda C, Miyasaka T, Kawakami K, Inokuchi J, Kawano T, Dobashi-Okuyama K, et al. Sex-based differences in CD103 + dendritic cells promote female-predominant Th2 cytokine production during allergic asthma. Clin Exp Allergy. 2018;48:379-93.
38. Shen C, Detry B, Lecocq M, Pilette C. A novel IgA/Delta-like 4/Notch axis induces immunosuppressive activity in human dendritic cells. Clin Immunol. 2016;168:37-46.
39. Wei Z, Yan X. The roles of estrogen and its receptors in autoimmune diseases. Int J Immunol. 2010;33:35.
40. Elgart BN, Oriss TB, Qi Z, Dixon-McCarthy B, Geerlings M, Hylkema MN, et al. Macrophages: regulators of sex differences in asthma? Am J Respir Cell Mol Biol. 2010;42:595-603.
41. Susan K. Estrogen receptors regulate an inflammatory pathway of dendritic cell differentiation: mechanisms and implications for immunity. Horm Behav. 2012;62:254-62.
42. Kumar S, Dwivedi PD, Das M, Tripathi A. Macrophages in food allergy: an enigma. Mol Immunol. 2013;56:612-8.
43. Li Z, Ju Z, Fieri M. The T-cell immunoglobulin and mucin domain (Tim) gene family in asthma, allergy, and autoimmunity. Allergy Asthma Proc. 2013;34:21-6.
44. Carreras E, Turner S, Frank MB, Knowlton N, Osban J, Centola M, et al. Estrogen receptor signaling promotes dendritic cell differentiation by increasing expression of the transcription factor IRF4. Blood. 2010;115:238-46.
45. Teixeira D, Marques C, Pestana D, Faria A, Norberto S, Calhau C, et al. Effects of xenoestrogens in human M1 and M2 macrophage migration, cytokine release, and estrogen-related signaling pathways. Environ Toxicol. 2015;31:1496-509.
46. Bolego C, Cignarella A, Staels B, Chinettigbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscl Throm Vasc Bio. 2013;33:1127-34.
47. Toniolo A. Polarization in patterns of human monocyte-derived macrophages in relation to estrogen treatment and menopausal status. Adv Mater Res. 2014;15:15-26.
48. Smith KA, Hochweller K, Hämmerling GJ, Boon L, MacDonald AS, Maizels RM. Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103-dendritic cells. J Immunol. 2011;186:7098-109.
49. Van Rijt LS, Vos N, Willart M, Muskens F, Tak PP, van der Horst C, et al. Persistent activation of dendritic cells after resolution of allergic airway inflammation breaks tolerance to inhaled allergens in mice. Am J Respir Crit Care Med. 2011;184:303-11.
50. Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, Kool M, et al. Inflammatory dendritic cells -not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med. 2010;207:2097-111.
51. Kool M, Soulliã T, Van Nimwegen M, Willart MA, Muskens F, Jung SN, et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med. 2008;205:869-82.
52. Hee SS, Hye-Jeong S, Sun YJ, Dae WC, Da-Ae K, Min-Jung B, et al. Turmeric (Curcuma longa) attenuates food allergy symptoms by regulating type 1/type 2 helper T cells (Th1/Th2) balance in a mouse model of food allergy. J Ethnopharmacol. 2015;175:21-9.
53. Abrahamsson TR, Abelius MS, Forsberg A, Björkstén B, Jenmalm MC. A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy. 2011;41:1729-39.
54. Voskamp AL, Leiden U. Clinical allergy: basophils, T cells, and therapeutic design. Leiden Univ Repos. 2016;24:06-16.
55. Zhang L, Zhao MJ, Hu MX, Xu XJ. Effect of pregnancy concentration of progestin on the immune function of T lymphocytes in peripheral blood of ovariectomized mice. J Reprod Med. 2012;21:489.
56. Hasegawa A, Miki T, Hosokawa H, Hossain MB, Shimizu C, Hashimoto K, et al. Impaired GATA3-dependent chromatin remodeling and Th2 cell differentiation leading to attempted allergic airway inflammation in aging mice. J Immunol. 2006;176:2546-54.
57. Liu L, Su SG, Zhang XK, Yang SJ. Serum levels of sex hormone and interferon-gamma, interleukin-4 in patients with Graves’ disease and their relationship. Clin Focus. 2007;22:1768-72.
58. Hong CC, Pajak A, Teitelbaum SL. Younger pubertal age is associated with allergy and other atopic conditions in girls. Pediatr Allergy Immunol. 2015;25:773-80.
59. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med. 2012;18:673-83.
60. Josaine A, Mausumi B, Mark K, Subhajit D. Estrogen receptor signal in regulation of B cell activation during diverse immune responses. Int J Biochem Cell Bio. 2015;68:42-7.
61. Fu Y1, Li L, Liu X, Ma C, Zhang J, Jiao Y, et al. Estrogen promotes B cell activation in vitro through down-regulating CD80 molecule expression. Gynecol Endocrinol. 2011;27:593-6.
62. Bernardi AI, Andersson A, Grahnemo L, Nurkkala-Karlsson M, Ohlsson C, Carlsten H, et al. Effects of lasofoxifene and bazedoxifene on B cell development and function. Immun Inflamm Dis. 2014;2:214-25.
63. Saulep-Easton D, Vincent FB, Quah PS, Wei A, Ting SB, Croce CM, et al. The BAFF receptor TACI controls IL-10 production by regulatory B cells and CLL B cells. Leukemia. 2016;30:163-72.
64. Jimbo S, Griebel PJ, Townsend H, Babiuk LA, Mutwiri G. Evidence for the existence of regulatory and effector B cell populations in Peyer’s patches of sheep. Vet Immunol Immunop. 2016;174:6-34.
65. Linhart B, Valenta R. Mechanisms underlying allergy vaccination with recombinant hypoallergenic allergen derivatives. Vaccine. 2012;30:4328-35.
66. Cooper AM, Hobson PS, Jutton MR, Kao MW, Drung B, Schmidt B, et al. Soluble CD23 controls IgE synthesis and homeostasis in human B cells. J Immunol. 2012;188:3199-207.
67. Cecilia E, Albert B, Ulrike H, Jasmin R, René P, Alessandro C, et al. Estrogen induces St6gal1 expression and increases IgG sialylation in mice and patients with rheumatoid arthritis: a potential explanation for the increased risk of rheumatoid arthritis in postmenopausal women. Arthritis Res Ther. 2018;20:84.
68. Tohru S, Sakina F, Mariko N, Emi S, Toshio H, Yasuhiko N, et al. The soy isoflavone equol enhances antigen-specific IgE production in ovalbumin-immunized BALB/c mice. J Nutr Sci Vitaminol. 2010;56:72-6.
69. Geunwoong N, Jaeho L. Regulatory B cells and allergic diseases. Allergy Asthma Immunol Res. 2011;3:168-77.
70. MacDonald T. Immunosuppression caused by antigen feeding II. Suppressor T cells mask Peyer’s patch B cell priming to orally administered antigen. Eur J Immunol. 1983;13: 138-42.
71. Reber LL, Frossard N. Targeting mast cells in inflammatory diseases. Pharmacol Ther. 2014;142:416-35.
72. Rana SB, Terumi M. Estrogen effects in allergy and asthma. Curr Opin Allergy Clin Immunol. 2013;13:92-9.
73. Jing H, Wang Z, Chen Y. Effect of oestradiol on mast cell number and histamine level in the mammary glands of rat. Anat Histol Embryol. 2012;41:170-6.
74. Federico J, Mariana W, Ana T, Katja W, Florin T, Serban C, et al. Estradiol and progesterone regulate the migration of mast cells from the periphery to the uterus and induce their maturation and degranulation. PLoS One. 2010;5: e14409.
75. Kennedy RH, Pelletier JH, Tupper EJ, Hutchinson LM, Gosse JA. Estrogen mimetic 4-tert-octylphenol enhances IgE-mediated degranulation of RBL-2H3 mast cells. J Toxicol Environ Health A. 2012;75:1451-5.
76. Takeda M, Tanabe M, Ito W, Ueki S, Konnno Y, Chihara M, et al. Gender difference in allergic airway remodelling and immunoglobulin production in a mouse model of asthma. Respirology. 2013;18:797-806.
77. Blacquiere MJ, Hylkema MN, Postma DS, Geerlings M, Timens W, Melgert BN. Airway inflammation and remodeling in two mouse models of asthma: comparison of males and females. Int Arch Allergy Immunol. 2010;153:173-81.
78. Narita S, Goldblum RM, Watson CS, Brooks EG, Estes DM, Edward M. Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ Health Persp. 2007;1:48-52.
79. Munozcruz ˜ S, Mendozarodríguez Y, Navacastro KE, Yepezmulia L, Moralesmontor J. Gender-related effects of sex steroids on histamine release and FcR1 expression in rat peritoneal mast cells. J Immunol Res. 2015;2015:351829.
80. Janicki JS, Spinale FG, Levick SP. Gender differences in nonischemic myocardial remodeling: are they due to estrogen modulation of cardiac mast cells and/or membrane type 1 matrix metalloproteinase. Pflügers Arch Eur J Physiol. 2013;465:687-97.
81. Zierau O, Zenclusse AC, Jensen F. Role of female sex hormones, estradiol and progesterone, in mast cell behavior. Front Immunol. 2012;3:169.
82. Zhu T, Ding S, Li T, Zhu L, Huang X. Estrogen is an important mediator of mast cell activation in ovarian endometriomas. Reproduction. 2017;155. REP-17-0457.
83. Saito H, Ishizaka T, Ishizaka K. Mast cells and IgE: from history to today. Allergol Int. 2013;62:3-12.
84. Kvedariene V, Martins P, Rouanet L, Demoly P. Diagnosis of iodinated contrast media hypersensitivity: results of a 6-year period. Clin Exp Allergy. 2006;36:1072-7.
Article Sidebar
Published
Oct 15, 2019
Article Details
How to Cite
Fan, Z., Che, H., Yang, S., & Chen, C. (2019). Estrogen and estrogen receptor signaling promotes allergic immune responses: Effects on immune cells, cytokines, and inflammatory factors involved in allergy. Allergologia Et Immunopathologia, 47(5), 506-512. https://all-imm.com/index.php/aei/article/view/289
Issue
Section
Review Article
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
Fan, Z., Che, H., Yang, S., & Chen, C. (2019). Estrogen and estrogen receptor signaling promotes allergic immune responses: Effects on immune cells, cytokines, and inflammatory factors involved in allergy. Allergologia Et Immunopathologia, 47(5), 506-512. https://all-imm.com/index.php/aei/article/view/289