17β-Estradiol protects females against influenza by recruiting neutrophils and increasing virus-specific CD8 T cell responses in the lungs

Journal of Virology

Volumn 88, Issue 9, 2014, Pages 4711-4720

  Robinson, Dionne P ^a   Hall, Olivia J ^a   Nilles, Tricia L ^a   Bream, Jay H ^a   Klein, Sabra L ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; ESTRADIOL; GAMMA INTERFERON; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFECT; FEMALE; IMMUNOREGULATION; INFECTION PREVENTION; INFLUENZA A; INNATE IMMUNITY; LUNG INFECTION; LUNG PARENCHYMA; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; VIRAL CLEARANCE; VIRUS TITRATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; ESTRADIOL; FEMALE; INFLUENZA A VIRUS; INTERFERON-GAMMA; LUNG; MICE; MICE, INBRED C57BL; NEUTROPHILS; ORTHOMYXOVIRIDAE INFECTIONS; TUMOR NECROSIS FACTOR-ALPHA; VIRAL LOAD;

EID: 84897500365     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02081-13     Document Type: Article

References (64)

1. Cox NJ, Subbarao K. 2000. Global epidemiology of influenza: past and present. Annu. Rev. Med. 51:407-421. http://dx.doi.org/10.1146/annurev.med.51.1.407.
2. Damjanovic D, Small CL, Jeyanathan M, McCormick S, Xing Z. 2012. Immunopathology in influenza virus infection: uncoupling the friend from foe. Clin. Immunol. 144:57-69. http://dx.doi.org/10.1016/j.clim.2012.05.005.
3. Robinson DP, Klein SL. 2012. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm. Behav. 62:263-271. http://dx.doi.org/10.1016/j.yhbeh.2012.02.023.
4. Klein SL. 2012. Immune cells have sex and so should journal articles. Endocrinology 153:2544-2550. http://dx.doi.org/10.1210/en.2011-2120.
5. Brabin L. 2002. Interactions of the female hormonal environment, susceptibility to viral infections, and disease progression. AIDS Patient Care STDs 16:211-221. http://dx.doi.org/10.1089/10872910252972267.
6. Tam A, Morrish D, Wadsworth S, Dorscheid D, Man SP, Sin DD. 2011. The role of female hormones on lung function in chronic lung diseases. BMCWomens Health 11:24. http://dx.doi.org/10.1186/1472-6874-11-24.
7. Klein SL, Pekosz A, Passaretti C, Anker M, Olukoya P. 2010. Sex, gender and influenza. World Health Organization, Geneva, Switzerland.
8. Somma D, Auer C, Abouihia A, Weiss MG. 2004. Gender in tuberculosis research. World Health Organization, Geneva, Switzerland.
9. Kos-Kudla B, Ostrowska Z, Marek B, Ciesielska-Kopacz N, Sieminska L, Kajdaniuk D, Nowak M, Kudla M. 2000. Hormone replacement therapy in postmenopausal asthmatic women. J. Clin. Pharm. Ther. 25: 461-466. http://dx.doi.org/10.1046/j.1365-2710.2000.00310.x.
10. Guilbault C, Stotland P, Lachance C, Tam M, Keller A, Thompson-Snipes L, Cowley E, Hamilton TA, Eidelman DH, Stevenson MM, Radzioch D. 2002. Influence of gender and interleukin-10 deficiency on the inflammatory response during lung infection with Pseudomonas aeruginosa in mice. Immunology 107:297-305. http://dx.doi.org/10.1046/j.1365-2567.2002.01508.x.
11. Robinson DP, Lorenzo ME, Jian W, Klein SL. 2011. Elevated 17betaestradiol protects females from influenza A virus pathogenesis by suppressing inflammatory responses. PLoS Pathog. 7:e1002149. http://dx.doi.org/10.1371/journal.ppat.1002149.
12. Zimmerman JL, Woodruff PG, Clark S, Camargo CA. 2000. Relation between phase of menstrual cycle and emergency department visits for acute asthma. Am. J. Respir. Crit. Care Med. 162:512-515. http://dx.doi.org/10.1164/ajrccm.162.2.9910105.
13. Matsubara S, Swasey CH, Loader JE, Dakhama A, Joetham A, Ohnishi H, Balhorn A, Miyahara N, Takeda K, Gelfand EW. 2008. Estrogen determines sex differences in airway responsiveness after allergen exposure. Am. J. Respir. Cell Mol. Biol. 38:501-508. http://dx.doi.org/10.1165/rcmb.2007-0298OC.
14. Yanke SJ, Olson ME, Davies HD, Hart DA. 2000. A CD-1 mouse model of infection with Staphylococcus aureus: influence of gender on infection with MRSA and MSSA isolates. Can. J. Microbiol. 46:920-926. http://dx.doi.org/10.1139/cjm-46-10-920.
15. Vegeto E, Cuzzocrea S, Crisafulli C, Mazzon E, Sala A, Krust A, Maggi A. 2010. Estrogen receptor-alpha as a drug target candidate for preventing lung inflammation. Endocrinology 151:174-184. http://dx.doi.org/10.1210/en.2009-0876.
16. Velez-Ortega AC, Temprano J, Reneer MC, Ellis GI, McCool A, Gardner T, Khosravi M, Marti F. 2013. Enhanced generation of suppressor T cells in patients with asthma taking oral contraceptives. J. Asthma 50:223-230. http://dx.doi.org/10.3109/02770903.2012.761231.
17. Straub RH. 2007. The complex role of estrogens in inflammation. Endocr. Rev. 28:521-574. http://dx.doi.org/10.1210/er.2007-0001.
18. Stein B, Yang MX. 1995. Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol. Cell. Biol. 15:4971-4979.
19. Cvoro A, Tzagarakis-Foster C, Tatomer D, Paruthiyil S, Fox MS, Leitman DC. 2006. Distinct roles of unliganded and liganded estrogen receptors in transcriptional repression. Mol. Cell 21:555-564. http://dx.doi.org/10.1016/j.molcel.2006.01.014.
20. Gilliver SC. 2010. Sex steroids as inflammatory regulators. J. Steroid Biochem. Mol. Biol. 120:105-115. http://dx.doi.org/10.1016/j.jsbmb.2009.12.015.
21. Kovats S, Carreras E, Agrawal H. 2010. Sex steroid receptors in immune cells, p 53-92. In Klein SL, RobertsCW(ed), Sex hormones and immunity to infection. Springer-Verlag, Berlin, Germany.
22. Pfeilschifter J, Koditz R, Pfohl M, Schatz H. 2002. Changes in proinflammatory cytokine activity after menopause. Endocr. Rev. 23:90-119. http://dx.doi.org/10.1210/er.23.1.90.
23. Cunningham M, Gilkeson G. 2011. Estrogen receptors in immunity and autoimmunity. Clin. Rev. Allergy Immunol. 40:66-73. http://dx.doi.org/10.1007/s12016-010-8203-5.
24. Giraud SN, Caron CM, Pham-Dinh D, Kitabgi P, Nicot AB. 2010. Estradiol inhibits ongoing autoimmune neuroinflammation and NFkappaB-dependent CCL2 expression in reactive astrocytes. Proc. Natl. Acad. Sci. U. S. A. 107:8416-8421. http://dx.doi.org/10.1073/pnas.0910627107.
25. Nguyen DC, Masseoud F, Lu X, Scinicariello F, Sambhara S, Attanasio R. 2011. 17Beta-estradiol restores antibody responses to an influenza vaccine in a postmenopausal mouse model. Vaccine 29:2515-2518. http://dx.doi.org/10.1016/j.vaccine.2011.01.080.
26. Pazos MA, Kraus TA, Munoz-Fontela C, Moran TM. 2012. Estrogen mediates innate and adaptive immune alterations to influenza infection in pregnant mice. PLoS One 7:e40502. http://dx.doi.org/10.1371/journal.pone.0040502.
27. Raberg L, Sim D, Read AF. 2007. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318: 812-814. http://dx.doi.org/10.1126/science.1148526.
28. Siracusa MC, Overstreet MG, Housseau F, Scott AL, Klein SL. 2008. 17 Beta-estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J. Immunol. 180:1423-1431. http://www.jimmunol.org/content/180/3/1423.
29. Lorenzo ME, Hodgson A, Robinson DP, Kaplan JB, Pekosz A, Klein SL. 2011. Antibody responses and cross protection against lethal influenza A viruses differ between the sexes in C57BL/6 mice. Vaccine 29:9246-9255. http://dx.doi.org/10.1016/j.vaccine.2011.09.110.
30. Reed LJ, Meunch H. 1938. A simple method of estimating 50 percent endpoints. Am. J. Hyg. 27:493.
31. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, Doherty PC. 1998. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8:683-691. http://dx.doi.org/10.1016/S1074-7613(00)80573-7.
32. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, Slight SR, Khader SA, Dubin PJ, Enelow RI, Kolls JK, Alcorn JF. 2011. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J. Immunol. 186:1666-1674. http://dx.doi.org/10.4049/jimmunol.1002194.
33. Tate MD, Deng YM, Jones JE, Anderson GP, Brooks AG, Reading PC. 2009. Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J. Immunol. 183:7441-7450. http://dx.doi.org/10.4049/jimmunol.0902497.
34. Medzhitov R, Schneider DS, Soares MP. 2012. Disease tolerance as a defense strategy. Science 335:936-941. http://dx.doi.org/10.1126/science.1214935.
35. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YH, Yuen KY, Webster RG, Peiris JS. 2004. H5N1 influenza: a protean pandemic threat. Proc. Natl. Acad. Sci. U. S. A. 101:8156-8161. http://dx.doi.org/10.1073/pnas.0402443101.
36. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha DQ, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12:1203-1207. http://dx.doi.org/10.1038/nm1477.
37. Szretter KJ, Gangappa S, Lu X, Smith C, Shieh WJ, Zaki SR, Sambhara S, Tumpey TM, Katz JM. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81:2736-2744. http://dx.doi.org/10.1128/JVI.02336-06.
38. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, Van Rooijen N, Katz JM, Basler CF. 2005. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J. Virol. 79:14933-14944. http://dx.doi.org/10.1128/JVI.79.23.14933-14944.2005.
39. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115. http://dx.doi.org/10.1371/journal.ppat.1000115.
40. Braciale TJ, Sun J, Kim TS. 2012. Regulating the adaptive immune response to respiratory virus infection. Nat. Rev. Immunol. 12:295-305. http://dx.doi.org/10.1038/nri3166.
41. McGill J, Heusel JW, Legge KL. 2009. Innate immune control and regulation of influenza virus infections. J. Leukoc. Biol. 86:803-812. http://dx.doi.org/10.1189/jlb.0509368.
42. Tate MD, Brooks AG, Reading PC, Mintern JD. 2012. Neutrophils sustain effective CD8(+) T-cell responses in the respiratory tract follow-ing influenza infection. Immunol. Cell Biol. 90:197-205. http://dx.doi.org/10.1038/icb.2011.26.
43. Hufford MM, Richardson G, Zhou H, Manicassamy B, Garcia-Sastre A, Enelow RI, Braciale TJ. 2012. Influenza-infected neutrophils within the infected lungs act as antigen presenting cells for anti-viral CD8(+) T cells. PLoS One 7:e46581. http://dx.doi.org/10.1371/journal.pone.0046581.
44. Gosselin EJ, Wardwell K, Rigby WF, Guyre PM. 1993. Induction of MHC class II on human polymorphonuclear neutrophils by granulocyte/macrophage colony-stimulating factor, IFN-gamma, and IL-3. J. Immunol. 151:1482-1490.
45. Culshaw S, Millington OR, Brewer JM, McInnes IB. 2008. Murine neutrophils present class II restricted antigen. Immunol. Lett. 118:49-54. http://dx.doi.org/10.1016/j.imlet.2008.02.008.
46. Robinson DP, Klein SL. 2012. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm. Behav. 62:263-271. http://dx.doi.org/10.1016/j.yhbeh.2012.02.023.
47. Brandes M, Klauschen F, Kuchen S, Germain RN. 2013. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154:197-212. http://dx.doi.org/10.1016/j.cell.2013.06.013.
48. Hashimoto Y, Moki T, Takizawa T, Shiratsuchi A, Nakanishi Y. 2007. Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J. Immunol. 178:2448-2457. http://www.jimmunol.org/content/178/4/2448.
49. Tate MD, Ioannidis LJ, Croker B, Brown LE, Brooks AG, Reading PC. 2011. The role of neutrophils during mild and severe influenza virus infections of mice. PLoS One 6:e17618. http://dx.doi.org/10.1371/journal.pone.0017618.
50. Jilma B, Eichler HG, Breiteneder H, Wolzt M, Aringer M, Graninger W, Rohrer C, Veitl M, Wagner OF. 1994. Effects of 17 beta-estradiol on circulating adhesion molecules. J. Clin. Endocrinol. Metab. 79:1619-1624. http://dx.doi.org/10.1210/jc.79.6.1619.
51. Wang Y, Cela E, Gagnon S, Sweezey NB. 2010. Estrogen aggravates inflammation in Pseudomonas aeruginosa pneumonia in cystic fibrosis mice. Respir. Res. 11:166. http://dx.doi.org/10.1186/1465-9921-11-166.
52. Stygar D, Westlund P, Eriksson H, Sahlin L. 2006. Identification of wild type and variants of oestrogen receptors in polymorphonuclear and mononuclear leucocytes. Clin. Endocrinol. (Oxf.) 64:74-81. http://dx.doi.org/10.1111/j.1365-2265.2005.02420.x.
53. Molero L, Garcia-Duran M, Diaz-Recasens J, Rico L, Casado S, Lopez-Farre A. 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. http://dx.doi.org/10.1016/S0008-6363(02)00505-9.
54. Molloy EJ, O'Neill AJ, Grantham JJ, Sheridan-Pereira M, Fitzpatrick JM, Webb DW, Watson RW. 2003. Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood 102:2653-2659. http://dx.doi.org/10.1182/blood-2003-02-0649.
55. Chiang K, Parthasarathy S, Santanam N. 2004. Estrogen, neutrophils and oxidation. Life Sci. 75:2425-2438. http://dx.doi.org/10.1016/j.lfs.2004.04.035.
56. Cid MC, Kleinman HK, Grant DS, Schnaper HW, Fauci AS, Hoffman GS. 1994. Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1. J. Clin. Invest. 93:17-25. http://dx.doi.org/10.1172/JCI116941.
57. Mantovani A, Cassatella MA, Costantini C, Jaillon S. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11:519-531. http://dx.doi.org/10.1038/nri3024.
58. Bordon J, Aliberti S, Fernandez-Botran R, Uriarte SM, Rane MJ, Duvvuri P, Peyrani P, Morlacchi LC, Blasi F, Ramirez JA. 2013. Understanding the roles of cytokines and neutrophil activity and neutrophil apoptosis in the protective versus deleterious inflammatory response in pneumonia. Int. J. Infect. Dis. 17:e76-e83. http://dx.doi.org/10.1016/j.ijid.2012.06.006.
59. Gresnigt MS, Joosten LA, Verschueren I, van der Meer JW, Netea MG, Dinarello CA, van de Veerdonk FL. 2012. Neutrophil-mediated inhibition of proinflammatory cytokine responses. J. Immunol. 189:4806-4815. http://dx.doi.org/10.4049/jimmunol.1103551.
60. Brincks EL, Gurung P, Langlois RA, Hemann EA, Legge KL, Griffith TS. 2011. The magnitude of the T cell response to a clinically significant dose of influenza virus is regulated by TRAIL. J. Immunol. 187:4581-4588. http://dx.doi.org/10.4049/jimmunol.1002241.
61. Brincks EL, Katewa A, Kucaba TA, Griffith TS, Legge KL. 2008. CD8 T cells utilize TRAIL to control influenza virus infection. J. Immunol. 181: 4918-4925. http://www.jimmunol.org/content/181/7/4918.
62. Wiley JA, Hogan RJ, Woodland DL, Harmsen AG. 2001. Antigenspecific CD8(+) T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167:3293-3299. http://www.jimmunol.org/content/167/6/3293.
63. Wiley JA, Cerwenka A, Harkema JR, Dutton RW, Harmsen AG. 2001. Production of interferon-gamma by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am. J. Pathol. 158:119-130. http://dx.doi.org/10.1016/S0002-9440(10)63950-8.
64. Fernandez-Sesma A, Marukian S, Ebersole BJ, Kaminski D, Park MS, Yuen T, Sealfon SC, Garcia-Sastre A, Moran TM. 2006. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 80: 6295-6304. http://dx.doi.org/10.1128/JVI.02381-05.