Gender differences of B cell signature in healthy subjects underlie disparities in incidence and course of SLE related to estrogen

Journal of Immunology Research

Volumn 2014, Issue , 2014, Pages 1-17

  Fan, Hongye ^a   Dong, Guanjun ^a   Zhao, Guangfeng ^a   Liu, Fei ^a   Yao, Genghong ^a   Zhu, Yichao ^b   Hou, Yayi ^a  

^a NANJING UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; B CELL MATURATION ANTIGEN; CAVEOLIN 1; CD200R1 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; CHLORMETHINE; CYCLIC AMP; DDX3Y PROTEIN; DEAD BOX PROTEIN; DEFENSIN ALPHA 4; ESTRADIOL; ESTROGEN; EUKARYOTIC INITIATION FACTOR 1A Y CHROMOSOME; INITIATION FACTOR 1A; LACTOFERRIN; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFERENTIAL GENE EXPRESSION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC VARIABILITY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INCIDENCE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UNINDEXED SEQUENCE; Y CHROMOSOME; YOUNG ADULT;

EID: 84898896593     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2014/814598     Document Type: Article

References (69)

1. Anderson L. C., Bolling D. Z., Schelinski S., Sex differences in the development of brain mechanisms for processing biological motion. Neuroimage 2013 83 751 760
2. Parks R. J., Howlett S. E., Sex differences in mechanisms of cardiac excitation-contraction coupling. Pflügers Archiv 2013 465 747 763
3. Majek O., Gondos A., Jansen L., Sex differences in colorectal cancer survival: population-based analysis of 164,996 colorectal cancer patients in Germany. PLoS ONE 2013 8 e68077
4. Kwekel J. C., Desai V. G., Moland C. L., Vijay V., Fuscoe J. C., Sex differences in kidney gene expression during the life cycle of F344 rats. Biology of Sex Differences 2013 4 14
5. Donner N. C., Lowry C. A., Sex differences in anxiety and emotional behavior. Pflügers Archiv 2013 465 601 626
6. Valentino R. J., van Bockstaele E., Bangasser D., Sex-specific cell signaling: the corticotropin-releasing factor receptor model. Trends in Pharmacological Sciences 2013 34 437 444
7. McClelland E. E., Smith J. M., Gender specific differences in the immune response to infection. Archivum Immunologiae et Therapiae Experimentalis 2011 59 3 203 213 2-s2.0-79959279272 10.1007/s00005-011-0124-3
8. Choudhry M. A., Bland K. I., Chaudry I. H., Trauma and immune response-Effect of gender differences. Injury 2007 38 12 1382 1391 2-s2.0-36549087165 10.1016/j.injury.2007.09.027
9. Maskew M., Brennan A. T., Westreich D., Gender differences in mortality and CD4 count response among virally suppressed HIV-positive patients. Journal of Women's Health 2013 22 113 120
10. Sankaran-Walters S., Macal M., Grishina I., Sex differences matter in the gut: effect on mucosal immune activation and inflammation. Biology of Sex Differences 2013 4 10
11. Abdullah M., Chai P.-S., Chong M.-Y., Tohit E. R. M., Ramasamy R., Pei C. P., Vidyadaran S., Gender effect on in vitro lymphocyte subset levels of healthy individuals. Cellular Immunology 2012 272 2 214 219 2-s2.0-83955165404 10.1016/j.cellimm.2011.10.009
12. Scotland R. S., Stables M. J., Madalli S., Watson P., Gilroy D. W., Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 2011 118 22 5918 5927 2-s2.0-82155184479 10.1182/blood-2011-03-340281
13. Wikby A., Månsson I. A., Johansson B., Strindhall J., Nilsson S. E., The immune risk profile is associated with age and gender: findings from three Swedish population studies of individuals 20-100 years of age. Biogerontology 2008 9 5 299 308 2-s2.0-50649111879 10.1007/s10522-008-9138-6
14. Yan J., Greer J. M., Hull R., O'Sullivan J. D., Henderson R. D., Read S. J., McCombe P. A., The effect of ageing on human lymphocyte subsets: comparison of males and females. Immunity and Ageing 2010 7, article 4 2-s2.0-77952306780 10.1186/1742-4933-7-4
15. Garcia Verdecia B., Saavedra Hernandez D., Lorenzo-Luaces P., Immunosenescence and gender: a study in healthy Cubans. Immunity & Ageing 2013 10 16
16. Straface E., Gambardella L., Brandani M., Malorni W., Sex differences at cellular level 'cells have a sex'. Sex and Gender Differences in Pharmacology 2012 49 65 Handbook of Experimental Pharmacology
17. Giampietri C., Petrungaro S., Filippini A., Ziparo E., Sex-related differences in death control of somatic cells. Journal of Cellular and Molecular Medicine 2013 17 550 551
18. Korganow A.-S., Knapp A.-M., Nehme-Schuster H., Soulas-Sprauel P., Poindron V., Pasquali J.-L., Martin T., Peripheral B cell abnormalities in patients with systemic lupus erythematosus in quiescent phase: decreased memory B cells and membrane CD19 expression. Journal of Autoimmunity 2010 34 4 426 434 2-s2.0-77952240188 10.1016/j.jaut.2009.11.002
19. Mok M. Y., The immunological basis of B-cell therapy in systemic lupus erythematosus. International Journal of Rheumatic Diseases 2010 13 1 3 11 2-s2.0-75649121143 10.1111/j.1756-185X.2009.01458.x
20. Liossis S.-N. C., Kovacs B., Dennis G., Kammer G. M., Tsokos G. C., B cells from patients with systemic lupus erythematosus display abnormal antigen receptor-mediated early signal transduction events. Journal of Clinical Investigation 1996 98 11 2549 2557 2-s2.0-0029829026
21. Reininger L., Winkler T. H., Kalberer C. P., Jourdan M., Melchers F., Rolink A. G., Intrinsic B cell defects in NZB and NZW mice contribute to systemic lupus erythematosus in (NZB x NZW)F1 mice. Journal of Experimental Medicine 1996 184 3 853 861 2-s2.0-0029838992
22. Isenberg D. A., B cell targeted therapies in autoimmune diseases. Journal of Rheumatology 2006 33 77 24 28 2-s2.0-33646438805
23. Garaud J.-C., Schickel J.-N., Blaison G., Knapp A.-M., Dembele D., Ruer-Laventie J., Korganow A.-S., Martin T., Soulas-Sprauel P., Pasquali J.-L., B cell signature during inactive systemic lupus is heterogeneous: toward a biological dissection of lupus. PLoS ONE 2011 6 8 2-s2.0-80051983086 10.1371/journal.pone.0023900 e23900
24. Becker A. M., Dao K. H., Han B. K., SLE peripheral blood B cell, T cell and myeloid cell transcriptomes display unique profiles and each subset contributes to the interferon signature. PLoS ONE 2013 8 e67003
25. Sakiani S., Olsen N. J., Kovacs W. J., Gonadal steroids and humoral immunity. Nature Reviews Endocrinology 2013 9 56 62
26. Oertelt-Prigione S., The influence of sex and gender on the immune response. Autoimmunity Reviews 2012 11 6-7 A479 A485 2-s2.0-84858447329 10.1016/j.autrev.2011.11.022
27. Candore G., Balistreri C. R., Colonna-Romano G., Lio D., Listì F., Vasto S., Caruso C., Gender-related immune-inflammatory factors, age-related diseases, and longevity. Rejuvenation Research 2010 13 2-3 292 297 2-s2.0-77952347333 10.1089/rej.2009.0942
28. Yang L., Hu Y., Hou Y., Effects of 17 β -estradiol on the maturation, nuclear factor kappa B p65 and functions of murine spleen CD11c-positive dendritic cells. Molecular Immunology 2006 43 4 357 366 2-s2.0-27944502986 10.1016/j.molimm.2005.02.012
29. Hao S., Li P., Zhao J., Hu Y., Hou Y., 17 β -estradiol suppresses cytotoxicity and proliferative capacity of murine splenic NK1.1+ cells. Cellular and Molecular Immunology 2008 5 5 357 364 2-s2.0-65849391010 10.1038/cmi.2008.44
30. Xie H., Hua C., Sun L., Zhao X., Fan H., Dou H., Sun L., Hou Y., 17 β -estradiol induces CD40 expression in dendritic cells via MAPK signaling pathways in a minichromosome maintenance protein 6-dependent manner. Arthritis and Rheumatism 2011 63 8 2425 2435 2-s2.0-79961104904 10.1002/art.30420
31. Xu Y., Fan H., Li X., Sun L., Hou Y., beta-Estradiol enhances response of mice spleen B cells elicited by TLR9 agonist. Cellular Immunology 2012 278 125 135 10.1016/j.cellimm.2012.07.007
32. Lee T.-P., Chiang B.-L., Sex differences in spontaneous versus induced animal models of autoimmunity. Autoimmunity Reviews 2012 11 6-7 A422 A429 2-s2.0-84858441796 10.1016/j.autrev.2011.11.020
33. Hochberg M. C., Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis and Rheumatism 1997 40 9 1725 2-s2.0-0031229830
34. Bombardier C., Gladman D. D., Urowitz M. B., Caron D., Chi Hsing Chang C. H. C., Derivation of the SLEDAI: a disease activity index for lupus patients. Arthritis and Rheumatism 1992 35 6 630 640 2-s2.0-0026777352 10.1002/art.1780350606
35. Actor J. K., Hwang S.-A., Kruzel M. L., Lactoferrin as a natural immune modulator. Current Pharmaceutical Design 2009 15 17 1956 1973 2-s2.0-68449088241 10.2174/138161209788453202
36. Kin N. W., Chen Y., Stefanov E. K., Gallo R. L., Kearney J. F., Cathelin-related antimicrobial peptide differentially regulates T- and B-cell function. European Journal of Immunology 2011 41 10 3006 3016 2-s2.0-80053165002 10.1002/eji.201141606
37. Zilbauer M., Jenke A., Wenzel G., Goedde D., Postberg J., Phillips A. D., Lucas M., Noble-Jamieson G., Torrente F., Salvestrini C., Heuschkel R., Wirth S., Intestinal alpha-defensin expression in pediatric inflammatory bowel disease. Inflammatory Bowel Diseases 2011 17 10 2076 2086 2-s2.0-80052717948 10.1002/ibd.21577
38. Hewagama A., Patel D., Yarlagadda S., Strickland F. M., Richardson B. C., Stronger inflammatory/cytotoxic T-cell response in women identified by microarray analysis. Genes and Immunity 2009 10 5 509 516 2-s2.0-67849128689 10.1038/gene.2009.12
39. Aravamudan B., VanOosten S. K., Meuchel L. W., Caveolin-1 knockout mice exhibit airway hyperreactivity. American Journal of Physiology-Lung Cellular and Molecular Physiology 2012 303 L669 L681
40. Guo C.-J., Yang X.-B., Wu Y.-Y., Yang L.-S., Mi S., Liu Z.-Y., Jia K.-T., Huang Y.-X., Weng S.-P., Yu X.-Q., He J.-G., Involvement of caveolin-1 in the Jak-Stat signaling pathway and infectious spleen and kidney necrosis virus infection in mandarin fish (Siniperca chuatsi). Molecular Immunology 2011 48 8 992 1000 2-s2.0-79952428529 10.1016/j.molimm.2011.01.001
41. Gilling C. E., Mittal A. K., Chaturvedi N. K., Iqbal J., Aoun P., Lymph node-induced immune tolerance in chronic lymphocytic leukaemia: a role for caveolin-1. British Journal of Haematology 2012 158 216 231
42. Caserta S., Nausch N., Sawtell A., Drummond R., Barr T., MacDonald A. S., Mutapi F., Zamoyska R., Chronic infection drives expression of the inhibitory receptor CD200R, and its ligand CD200, by mouse and human CD4 T cells. PLoS ONE 2012 7 4 2-s2.0-84859480681 10.1371/journal.pone.0035466 e35466
43. Uyama T., Jin X.-H., Tsuboi K., Tonai T., Ueda N., Characterization of the human tumor suppressors TIG3 and HRASLS2 as phospholipid-metabolizing enzymes. Biochimica et Biophysica Acta 2009 1791 12 1114 1124 2-s2.0-73949097337 10.1016/j.bbalip.2009.07.001
44. Schmidt J., Riechers A., Bosserhoff A. K., MIA-a new target protein for malignant melanoma therapy. Histology and Histopathology 2013 28 421 426
45. Hara-Chikuma M., Chikuma S., Sugiyama Y., Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake. The Journal of Experimental Medicine 2012 209 1743 1752
46. Bund D., Buhmann R., Gokmen F., Zorn J., Kolb H. J., Minor histocompatibility antigen UTY as target for graft-versus-leukemia and graft-versus-haematopoiesis in the canine model. Scandinavian Journal of Immunology 2013 77 39 53
47. Gil J., Busto E. M., Garcillan B., Chean C., A leaky mutation in CD3D differentially affects alphabeta and gammadelta T cells and leads to a Talphabeta-Tgammadelta+B+NK+ human SCID. Journal of Clinical Investigation 2011 121 3872 3876
48. Sud N., Wiseman D. A., Black S. M., Caveolin 1 is required for the activation of endothelial nitric oxide synthase in response to 17 β -estradiol. Molecular Endocrinology 2010 24 8 1637 1649 2-s2.0-77954968035 10.1210/me.2010-0043
49. Li Y., Zhao L. D., Tong L. S., Aberrant CD200/CD200R1 expression and function in systemic lupus erythematosus contributes to abnormal T-cell responsiveness and dendritic cell activity. Arthritis Research & Therapy 2012 14 R123
50. Liu Y., Hong X., Kappler J., Jiang L., Zhang R., Xu L., Pan C.-H., Martin W. E., Murphy R. C., Shu H.-B., Dai S., Zhang G., Ligand-receptor binding revealed by the TNF family member TALL-1. Nature 2003 423 6935 49 56 2-s2.0-0038076049 10.1038/nature01543
51. Lacotte S., Decossas M., le Coz C., Early differentiated CD138(high) MHCII+ IgG+ plasma cells express CXCR3 and localize into inflamed kidneys of lupus mice. PLoS ONE 2013 8 e58140
52. Tian Y., Stamova B., Jickling G. C., Xu H., Liu D., Ander B. P., Bushnell C., Zhan X., Turner R. J., Davis R. R., Verro P., Pevec W. C., Hedayati N., Dawson D. L., Khoury J., Jauch E. C., Pancioli A., Broderick J. P., Sharp F. R., Y chromosome gene expression in the blood of male patients with ischemic stroke compared with male controls. Gender Medicine 2012 9 2 68.e3 75.e3 2-s2.0-84859522337 10.1016/j.genm.2012.01.005
53. Koenecke C., Förster R., CCR9 and inflammatory bowel disease. Expert Opinion on Therapeutic Targets 2009 13 3 297 306 2-s2.0-65549087533 10.1517/14728220902762928
54. Liu Z. K., Wang R. C., Han B. C., Yang Y., Peng J. P., A novel role of IGFBP7 in mouse uterus: regulating uterine receptivity through Th1/Th2 lymphocyte balance and decidualization. PLoS ONE 2012 7 e45224
55. Aporta A., Catalan E., Galan-Malo P., Granulysin induces apoptotic cell death and cleavage of the autophagy regulator Atg5 in human hematological tumors. Biochemical Pharmacology 2013 10.1016/j.bcp.2013.11.004
56. Ewen C. L., Kane K. P., Bleackley R. C., Granzyme H induces cell death primarily via a Bcl-2-sensitive mitochondrial cell death pathway that does not require direct Bid activation. Molecular Immunology 2013 54 309 318
57. de Weerd N. A., Vivian J. P., Nguyen T. K., Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1. Nature Immunology 2013 14 901 907
58. Nickerson K. M., Cullen J. L., Kashgarian M., Shlomchik M. J., Exacerbated autoimmunity in the absence of TLR9 in MRL.Fas(lpr) mice depends on Ifnar1. The Journal of Immunology 2013 190 3889 3894
59. Lobo E. O., Zhang Z., Shively J. E., Pivotal Advance: CEACAM1 is a negative coreceptor for the B cell receptor and promotes CD19-mediated adhesion of B cells in a PI3K-dependent manner. Journal of Leukocyte Biology 2009 86 2 205 218 2-s2.0-69449100854 10.1189/jlb.0109037
60. Busslinger M., Transcriptional control of early B cell development. Annual Review of Immunology 2004 22 55 79 2-s2.0-2542442633 10.1146/annurev. immunol.22.012703.104807
61. DeKoter R. P., Schweitzer B. L., Kamath M. B., Jones D., Tagoh H., Bonifer C., Hildeman D. A., Huang K. J., Regulation of the interleukin-7 receptor α promoter by the Ets transcription factors PU.1 and GA-binding protein in developing B cells. Journal of Biological Chemistry 2007 282 19 14194 14204 2-s2.0-34347203727 10.1074/jbc.M700377200
62. Pogue S. L., Preston B. T., Stalder J., Bebbington C. R., Cardarelli P. M., The receptor for type I IFNs is highly expressed on peripheral blood B cells and monocytes and mediates a distinct profile of differentiation and activation of these cells. Journal of Interferon and Cytokine Research 2004 24 2 131 139 2-s2.0-1342288115 10.1089/107999004322813372
63. Sullivan N. L., Eickhoff C. S., Zhang X., Giddings O. K., Lane T. E., Hoft D. F., Importance of the CCR5-CCL5 axis for mucosal Trypanosoma cruzi protection and B cell activation. Journal of Immunology 2011 187 3 1358 1368 2-s2.0-80051609609 10.4049/jimmunol.1100033
64. Serre K., Cunningham A. F., Coughlan R. E., CD8 T cells induce T-bet-dependent migration toward CXCR3 ligands by differentiated B cells produced during responses to alum-protein vaccines. Blood 2012 120 4552 4559
65. Xu Y., Xu Q., Yang L., Gene expression analysis of peripheral blood cells reveals Toll-like receptor pathway deregulation in colorectal cancer. PLoS One 2013 8 e62870
66. Menon R., di Dario M., Cordiglieri C., Musio S., la Mantia L., Milanese C., di Stefano A. L., Crabbio M., Franciotta D., Bergamaschi R., Pedotti R., Medico E., Farina C., Gender-based blood transcriptomes and interactomes in multiple sclerosis: involvement of SP1 dependent gene transcription. Journal of Autoimmunity 2012 38 2-3 J144 J155 2-s2.0-84858749570 10.1016/j.jaut.2011.11.004
67. Choi K. Y., Chow L. N., Mookherjee N., Cationic host defence peptides: multifaceted role in immune modulation and inflammation. Journal of Innate Immunity 2012 4 361 370
68. Steinstraesser L., Kraneburg U., Jacobsen F., Al-Benna S., Host defense peptides and their antimicrobial-immunomodulatory duality. Immunobiology 2011 216 3 322 333 2-s2.0-79251599753 10.1016/j.imbio.2010.07.003
69. Nadkarni S., McArthur S., Oestrogen and immunomodulation: new mechanisms that impact on peripheral and central immunity. Current Opinion in Pharmacology 2013 13 576 581