The influence of sex and gender on the immune response

Oertelt-Prigione, Sabine

doi:10.1016/j.autrev.2011.11.022

Cited by 459Sex and Gender in HealthcareEstrogen and related hormone effectsGenetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities

The influence of sex and gender on the immune response

Oertelt-Prigione, Sabine·2012·Autoimmunity Reviews

DOI 10.1016/j.autrev.2011.11.022

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Abstract

The immune system and its orchestrated response are affected by a multitude of endogenous and exogenous factors, modulators and challenges. One of the most frequent differences described in the immune response is its vigor and activity in females compared to males, leading to the consequent increase in autoimmune conditions seen in the female population as well as differences in the immune response to pathogens and viruses. The following review summarizes our present knowledge on sex differences in the immune response, detailing the hormonal and genetic effects that have been proposed as explanatory mechanisms. Sexual hormones, mostly estrogen but also progesterone and testosterone, affect immune cells quantitatively and qualitatively. Relevant research has focused on the impact of hormones on cytokine production by the different effector cells, as well as impact on immunoglobulin production by B lymphocytes and activity of granulocytes and NK cells. The biological aspects are complemented by research data on the possible modulatory role of the X chromosome. In addition to biological differences, the frequently neglected role of gender as an immunomodulator is introduced and explored. Gender affects all areas of human life and consequently affects the different steps of an immune response. Exposure to various types of antigens, access to health promotion programs and health care, as well as prioritization of health needs and household resource allocation all affect the different response of females and males to immunologic challenges.

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Inflammatory responses are stereotypically greater in females, which may be dictated by greater cytokine release due to the location of cytokine and TLR genes on the X-chromosome.
“Inflammatory responses are ste reotypically greater in females, which may be dictated by greater cytokine release due to the location of cytokine and TLR genes on the X-chromosome (Oertelt-Prigione, 2012).”
From Gene Therapy-Associated Uveitis (GTAU): Understanding and mitigating the adverse immune response in retinal gene therapy (2025) · cites this paper as Oertelt-Prigione, 2012
Gender might have a significant function in shaping the immune response.
“Thus, in addition to the immune factors that regulate the complex immunoendocrine network, gender might have a significant function in shaping the immune response [2].”
From Gender-Related Effects of Sex Steroids on Histamine Release and FcεRI Expression in Rat Peritoneal Mast Cells (2015) · cites this paper as [2]
Zolpidem shows slower drug metabolization and high secondary effects in women, increasing their health risks compared with men.
“zolpidem, a sleep medication35, which shows slower drug metabolization and high secondary effects in women, increasing their health risks compared with men34,36,37.”
From Sex and gender differences and biases in artificial intelligence for biomedicine and healthcare (2020) · cites this paper as [37]

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Kamada, M., Irahara, M., Maegawa, M., Ohmoto, Y., Murata, K., Yasui, T., Yamano, S., & Aono, T. (2001) · Gynecologic and Obstetric Investigation · doi:10.1159/000052948 · Cited by 53 · see citing works
Effect of estrogens on IL-1β promoter activity
Ruh, M. F., Bi, Y., DʼAlonzo, R. C., & Bellone, C. J. (1998) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00042-9 · Cited by 52 · see citing works
Integrating the Dimensions of Sex and Gender into Basic Life Sciences Research: Methodologic and Ethical Issues
Holdcroft, A. (2007) · Gender Medicine · doi:10.1016/s1550-8579(07)80048-9 · Cited by 46 · see citing works
Oestrogen as an inhibitor of human NK cell cytolysis
Ferguson, M. M., & McDonald, F. G. (1985) · FEBS Letters · doi:10.1016/0014-5793(85)81011-5 · Cited by 40 · see citing works
Toll-like receptor 7 and 8 polymorphisms: associations with functional effects and cellular and antibody responses to measles virus and vaccine
Clifford, H. D., Yerkovich, S. T., Khoo, S., Zhang, G., Upham, J. W., Souëf, P. N. L., Richmond, P., & Hayden, C. M. (2011) · Immunogenetics · doi:10.1007/s00251-011-0574-0 · Cited by 32 · see citing works
Cancer epidemiology of woodworking
Mohtashamipur, E., Norpoth, K., & L�hmann, F. (1989) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/bf00391350 · Cited by 28 · see citing works
Families at Financial Risk Due to High Ratio of Out-Of-Pocket Health Care Expenditures to Total Income
Bennett, K. J., & Dismuke, C. E. (2010) · Journal of Health Care for the Poor and Underserved · doi:10.1353/hpu.0.0309 · Cited by 27 · see citing works
HIV/AIDS: Hormonal Contraception and HIV Disease Progression
Stringer, E., & Antonsen, E. (2008) · Clinical Infectious Diseases · doi:10.1086/591697 · Cited by 24 · see citing works
Steroid Receptor Coactivator 1 Links the Steroid and Interferon γ Response Pathways
Tzortzakaki, E., Spilianakis, C. G., Zika, E., Kretsovali, A., & Papamatheakis, J. D. (2003) · Molecular Endocrinology · doi:10.1210/me.2002-0439 · Cited by 20 · see citing works
Vitamins and Mast Cells
Anogeianaki, A., Castellani, M. L., Tripodi, D., Toniato, E., Lutiis, M. A. D., Conti, F., Felaco, P., Fulcheri, M., Theoharides, T. C., Galzio, R. J., et al. (2010) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463201002300403 · Cited by 17 · see citing works
INFLUENCE OF STEROIDS ON OXIDANT GENERATION IN ACTIVATED HUMAN GRANULOCYTES AND MONONUCLEAR LEUKOCYTES
Cassidy, R. A. (2003) · Shock · doi:10.1097/01.shk.0000070740.34700.cd · Cited by 16 · see citing works
Estradiol suppresses vascular monocyte chemotactic protein-1 expression during early atherogenesis
Seli, E. U., Kayisli, U. A., Selam, B., Seli, M., & Arici, A. M. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.127306 · Cited by 14 · see citing works
An IFNG SNP with an estrogen-like response element selectively enhances promoter expression in peripheral but not lamina propria T cells
Gonsky, R., Deem, R. L., Bream, J. H., Young, H. A., & Targan, S. R. (2006) · Genes and Immunity · doi:10.1038/sj.gene.6364305 · Cited by 12 · see citing works
Sex Hormones and Regulation of Host Responses Against Parasites
Alexander, J. K., Irving, K., Snider, H. M., & Satoskar, A. R. (2009) · Springer eBooks · doi:10.1007/978-3-642-02155-8_6 · Cited by 6 · see citing works
HIV Study Renews Scrutiny of Hormonal Contraception
Cohen, J. D. (2011) · Science · doi:10.1126/science.334.6053.166 · Cited by 1 · see citing works

Flagged first, then by citations

2 of the 102 references couldn’t be matched to a known paper.

Sorted by citations

Cancer immunotherapy efficacy and patients' sex: a systematic review and meta-analysis
Conforti, F., Pala, L., Bagnardi, V., De Pas, T., Martinetti, M., Viale, G., Gelber, R. D., & Goldhirsch, A. (2018) · The Lancet Oncology · doi:10.1016/s1470-2045(18)30261-4 · Cited by 973 · see citing works
How sex and age affect immune responses, susceptibility to infections, and response to vaccination
Giefing, C., Berger, P., Lepperdinger, G., & Grubeck‐Loebenstein, B. (2015) · Aging Cell · doi:10.1111/acel.12326 · Cited by 768 · see citing works
“Partially controversial results were reported regarding hormonal effects on the cytokine secretion pattern of T lymphocytes (reviewed in Bouman et al., 2005; Straub, 2007; Gonzalez et al., 2010; Oertelt-Prigione, 2012).”
Background
Sex Differences in Lifespan
Austad, S. N., & Fischer, K. E. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.05.019 · Cited by 591 · see citing works
“Although there have been numerous studies assessing various aspects of immune responsiveness in adult humans in which females have often proven to have more robust responses (Ferguson et al., 2013; Gubbels Bupp, 2015; Oertelt-Prigione, 2012), there have been few such studies in infants.”
Sex and gender differences and biases in artificial intelligence for biomedicine and healthcare
Cirillo, D., Catuara-Solarz, S., Morey, C., Guney, E., Subirats, L., Mellino, S., Gigante, A., Valencia, A., Rementeria, M. J., Chadha, A. S., et al. (2020) · npj Digital Medicine · doi:10.1038/s41746-020-0288-5 · Cited by 553 · see citing works
Sex and Gender Differences in the Outcomes of Vaccination over the Life Course
Flanagan, K. L., Fink, A. L., Plebanski, M., & Klein, S. L. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060718 · Cited by 508 · see citing works
Host and Environmental Factors Influencing Individual Human Cytokine Responses
ter Horst, R., Jaeger, M., Smeekens, S. P., Oosting, M., Swertz, M. A., Li, Y., Kumar, V., Diavatopoulos, D. A., Jansen, A. F. M., Lemmers, H., et al. (2016) · Cell · doi:10.1016/j.cell.2016.10.018 · Cited by 457 · see citing works
“Another important host factor that influences immune responses is gender (Oertelt-Prigione, 2012), resulting in a differ-”
Inflammation and cerebral small vessel disease: A systematic review
Low, A., Mak, E., Rowe, J. B., Markus, H. S., & O'Brien, J. T. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.100916 · Cited by 445 · see citing works
TFOS DEWS II Sex, Gender, and Hormones Report
Sullivan, D. A., Rocha, E. M., Aragona, P., Clayton, J. A., Ding, J., Golebiowski, B., Hampel, U., McDermott, A. M., Schaumberg, D. A., Srinivasan, S., et al. (2017) · The Ocular Surface · doi:10.1016/j.jtos.2017.04.001 · Cited by 451 · see citing works
Sex differences in vaccine-induced humoral immunity
Fischinger, S., Boudreau, C. M., Butler, A. L., Streeck, H., & Alter, G. (2019) · Seminars in Immunopathology · doi:10.1007/s00281-018-0726-5 · Cited by 410 · see citing works
“The combination of social, cultural, and biological elements factoring into gender differences makes it difficult to differentiate between biological mechanisms and sex-specific behavior [18].”
Background
Myasthenia gravis: A comprehensive review of immune dysregulation and etiological mechanisms
Berrih‐Aknin, S., & Panse, R. L. (2014) · Journal of Autoimmunity · doi:10.1016/j.jaut.2013.12.011 · Cited by 382 · see citing works
“Relevant studies have focused on the impact of these hormones on cytokine production by different effector cells and on immunoglobulin production by B lymphocytes [115].”
Background
Sex differences in the neuro-immune consequences of stress: Focus on depression and anxiety
Bekhbat, M., & Neigh, G. N. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.02.006 · Cited by 359 · see citing works
“Alzheimer’s disease, and chronic pain are more common among females (Loram et al 2012), and dysregulation of immunocyte function, steroid hormone signaling (Oertelt-Prigione 2012), and gut microbiome-driven changes in autoimmunity (Markle et al 2013) have been proposed as potential mediators.”
Background
Sex, the aging immune system, and chronic disease
Bupp, M. G. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.02.002 · Cited by 333 · see citing works
ImmGen report: sexual dimorphism in the immune system transcriptome
Gal-Oz, S. T., Maier, B., Yoshida, H., Seddu, K., Elbaz, N., Czysz, C., Zuk, O., Stranger, B. E., Ner-Gaon, H., & Shay, T. (2019) · Nature Communications · doi:10.1038/s41467-019-12348-6 · Cited by 274 · see citing works
Racial and Gender-Based Differences in COVID-19
Kopel, J. J., Perisetti, A., Roghani, A., Aziz, M., Gajendran, M., & Goyal, H. (2020) · Frontiers in Public Health · doi:10.3389/fpubh.2020.00418 · Cited by 314 · see citing works
“However, the study also found that the hyperactive response in female immune systems to viral infections may increase symptom severity and pathological effects than observed in male patients (49).”
Background
Factors affecting sex-related reporting in medical research: a cross-disciplinary bibliometric analysis
Sugimoto, C. R., Ahn, Y., Smith, E. M. R., Macaluso, B., & Larivière, V. (2019) · The Lancet · doi:10.1016/s0140-6736(18)32995-7 · Cited by 309 · see citing works
Sex differences and the neurobiology of affective disorders
Rubinow, D. R., & Schmidt, P. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0148-z · Cited by 274 · see citing works
Stress during pregnancy alters temporal and spatial dynamics of the maternal and offspring microbiome in a sex-specific manner
Jašarević, E., Howard, C. D., Misic, A. M., Beiting, D. P., & Bale, T. L. (2017) · Scientific Reports · doi:10.1038/srep44182 · Cited by 262 · see citing works
Sex Drives Dimorphic Immune Responses to Viral Infections
Ghosh, S., & Klein, R. S. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601166 · Cited by 232 · see citing works
Sexual dimorphism in autoimmunity
Rubtsova, K., Marrack, P., & Rubtsov, A. V. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78082 · Cited by 219 · see citing works
“Introduction Differences between female and male immune and autoimmune responses have been well documented (1).”
Background
Gender-related differences in irritable bowel syndrome: Potential mechanisms of sex hormones
Méleine, M. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i22.6725 · Cited by 220 · see citing works
Gender Differences in the Pathogenesis and Outcome of Lupus and of Lupus Nephritis
Schwartzman-Morris, J. S., & Putterman, C. (2012) · Clinical and Developmental Immunology · doi:10.1155/2012/604892 · Cited by 193 · see citing works
“Estrogen-driven upregulation of MHC II in the dendritic cells, enhancement of proinflammatory cytokine production, and an interaction between estrogen andMHCII expression regulation have also been confirmed in animal models [21].”
Background
Modulation of autoimmune rheumatic diseases by oestrogen and progesterone
Hughes, G. C., & Choubey, D. (2014) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2014.144 · Cited by 189 · see citing works
Sexual Dimorphism in the Th17 Signature of Ankylosing Spondylitis
Gracey, E., Yao, Y., Green, B., Qaiyum, Z., Baglaenko, Y., Lin, A., Anton, A., Ayearst, R., Yip, P. S. F., & Inman, R. D. (2015) · Arthritis & Rheumatology · doi:10.1002/art.39464 · Cited by 185 · see citing works
“A sex bias in the humoral and cellular immune response has long been observed, with females showing enhanced Th1-type responses compared with males (11).”
Background
The influence of sex and gender on immunity, infection and vaccination.
Ruggieri, A., Anticoli, S., D’Ambrosio, A., Giordani, L., & Viora, M. (2016) · Annali dell Istituto Superiore di Sanità · doi:10.4415/ann_16_02_11 · Cited by 185 · see citing works
“There is a growing body of evidence from literature [3, 10] showing that both innate and adaptive immune responses to viral infections differ between males and females.”
Background
Sex differences in inflammation, redox biology, mitochondria and autoimmunity
Di Florio, D. N., Sin, J., Coronado, M. J., Atwal, P. S., & Fairweather, D. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101482 · Cited by 185 · see citing works
“is influenced by genetic, environmental and hormonal effects that alter the response to pathogens or damage in a sex-specific manner [19].”
Background
Central pathways causing fatigue in neuro-inflammatory and autoimmune illnesses
Morris, G., Berk, M., Walder, K. R., & Maes, M. H. J. (2015) · BMC Medicine · doi:10.1186/s12916-014-0259-2 · Cited by 179 · see citing works
“Sex hormones also regulate the Th1/Th2 balance of the immune system, the production of regulatory T cells and the functionality of granulocytes and natural killer cells [378,379].”
Background
Androgen receptor modulates Foxp3 expression in CD4+CD25+Foxp3+ regulatory T-cells
Walecki, M., Eisel, F., Klug, J., Baal, N., Paradowska‐Dogan, A., Wahle, E., Hackstein, H., Meinhardt, A., & Fijak, M. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-08-1323 · Cited by 176 · see citing works
“Moreover, many autoimmune diseases are more prevalent in women than in men, so that high androgen levels in men are regarded as protective (Klein, 2012; Oertelt-Prigione, 2012).”
Background
Sexually dimorphic outcomes and inflammatory responses in hypoxic-ischemic encephalopathy
Mirza, M. A., Ritzel, R. M., Xu, Y., McCullough, L. D., & Liu, F. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0251-6 · Cited by 173 · see citing works
“Differences between males and females can be identified at many levels of the immune response (reviewed in [55]).”
Background
Prevalence and incidence of systemic lupus erythematosus in France: A 2010 nation-wide population-based study
Arnaud, L., Fagot, J., Mathian, A., Païta, M., Fagot‐Campagna, A., & Amoura, Z. (2014) · Autoimmunity Reviews · doi:10.1016/j.autrev.2014.08.034 · Cited by 168 · see citing works
“This may underline the wellknown effect of hormones and gender over the risk to develop SLE [36,37].”
Background
Sex differences in the human peripheral blood transcriptome
Jansen, R., Batista, S., Brooks, A. I., Tischfield, J. A., Willemsen, G. A. H. M., van Grootheest, G., Hottenga, J., Milaneschi, Y., Mbarek, H., Madar, V., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-33 · Cited by 166 · see citing works
“From the 95 femalebiased genes linked to the immune system, 45 are regulated by estradiol, which confirms the role of estrogen in the sex-specific immune system functioning [57].”
Background
The critical importance of epigenetics in autoimmunity
Lu, Q. (2013) · Journal of Autoimmunity · doi:10.1016/j.jaut.2013.01.010 · Cited by 160 · see citing works
Sex differences matter in the gut: effect on mucosal immune activation and inflammation
Sankaran‐Walters, S., Macal, M., Grishina, I., Nagy, L. H., Goulart, L., Coolidge, K., Li, J., Fenton, A. N., Williams, T., Miller, M. K., et al. (2013) · Biology of Sex Differences · doi:10.1186/2042-6410-4-10 · Cited by 160 · see citing works
“It is likely that some of these effects in women are due to the immune-modulatory effects of sex hormones [2-4].”
Background
Sex and strain dependent differences in mucosal immunology and microbiota composition in mice
Elderman, M. E., Hugenholtz, F., Belzer, C., Boekschoten, M. V., van Beek, A. A., de Haan, B., Savelkoul, H. F. J., de Vos, P., & Faas, M. M. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0186-6 · Cited by 149 · see citing works
“Such factors can not only interfere with immune responses [68, 69], and with microbiota composition, but may also modulate the sex effects.”
Background
Sex Differences in Longevity and in Responses to Anti-Aging Interventions: A Mini-Review
Austad, S. N., & Bartke, A. (2015) · Gerontology · doi:10.1159/000381472 · Cited by 148 · see citing works
Sex and Gender Disparities in Melanoma
Bellenghi, M., Puglisi, R., Pontecorvi, G., Feo, A. D., Carè, A., & Mattia, G. (2020) · Cancers · doi:10.3390/cancers12071819 · Cited by 153 · see citing works
Sex differences in SARS-CoV-2 infection rates and the potential link to prostate cancer
Chakravarty, D., Nair, S. S., Hammouda, N., Ratnani, P., Gharib, Y., Wagaskar, V. G., Mohamed, N., Lundon, D., Dovey, Z. S., Kyprianou, N., et al. (2020) · Communications Biology · doi:10.1038/s42003-020-1088-9 · Cited by 142 · see citing works
Alpha-2 macroglobulin in Alzheimer’s disease: a marker of neuronal injury through the RCAN1 pathway
Varma, V. R., Varma, S., An, Y., Hohman, T. J., Seddighi, S., Casanova, R., Beri, A., Dammer, E. B., Seyfried, N. T., Pletniková, O., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.206 · Cited by 141 · see citing works
Sex Differences in Tolerability to Anti-Programmed Cell Death Protein 1 Therapy in Patients with Metastatic Melanoma and Non-Small Cell Lung Cancer: Are We All Equal?
Duma, N., Abdel-Ghani, A., Yadav, S., Hoversten, K. P., Reed, C. T., Sitek, A. N., Enninga, E. A. L., Paludo, J., Aguilera, J. V., Leventakos, K., et al. (2019) · The Oncologist · doi:10.1634/theoncologist.2019-0094 · Cited by 135 · see citing works
“No studies have explored possible differences between sexes in the incidence of irAEs, despite many lines of evidence describing differences in immune responses between women and men [15, 16], higher incidence of autoimmune disorders in women [17, 18], and the effect of sex hormones on the immune system from CD4 T cel…”
Background
Gender differences in chronic pruritus: women present different morbidity, more scratch lesions and higher burden
Ständer, S., Stumpf, A., Osada, N., Wilp, S., Chatzigeorgakidis, E., & Pfleiderer, B. (2013) · British Journal of Dermatology · doi:10.1111/bjd.12267 · Cited by 123 · see citing works
Sex differences in neuroinflammation and neuroprotection in ischemic stroke
Spychala, M. S., Honarpisheh, P., & McCullough, L. D. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23962 · Cited by 127 · see citing works
“Importantly, these numbers will only continue to increase in both men and women as our society continues to age, highlighting the urgent need for more therapeutic options for stroke patients (Oertelt-Prigione, 2012).”
Background
Myasthenia Gravis: Paradox versus paradigm in autoimmunity
Berrih‐Aknin, S. (2014) · Journal of Autoimmunity · doi:10.1016/j.jaut.2014.05.001 · Cited by 126 · see citing works
“effect on TNF- production [73].”
Background
Association of Sex with Risk of Kidney Graft Failure Differs by Age
Lepeytre, F., Dahhou, M., Zhang, X., Boucquemont, J., Sapir‐Pichhadze, R., Cardinal, H., & Foster, B. J. (2017) · Journal of the American Society of Nephrology · doi:10.1681/asn.2016121380 · Cited by 121 · see citing works
Male-specific IL-33 expression regulates sex-dimorphic EAE susceptibility
Russi, A. E., Ebel, M. E., Yang, Y., & Brown, M. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710401115 · Cited by 117 · see citing works
Stroke sensitivity in the aged: sex chromosome complement vs. gonadal hormones
McCullough, L. D., Mirza, M. A., Xu, Y., Bentivegna, K., Steffens, E. B., Ritzel, R. M., & Liu, F. (2016) · Aging · doi:10.18632/aging.100997 · Cited by 114 · see citing works
“Immune responses are shaped by biological differences between males and females, not only by hormonal influences but also genetic effects [43].”
Background
Correlation between sex and efficacy of immune checkpoint inhibitors ( PD ‐1 and CTLA ‐4 inhibitors)
Wu, Y. C., Ju, Q., Jia, K., Yu, J., Shi, H. M., Wu, H., & Jiang, M. (2018) · International Journal of Cancer · doi:10.1002/ijc.31301 · Cited by 117 · see citing works
“Likewise, gender difference—including health care access, social identity and food intake—tends to affect the immune system.(5,6) From a preclinical perspective, sex difference is correlated with programmed death-ligand 1 (PD-L1)–mediated Treg function.”
Background
Influence of estrogen in non-small cell lung cancer and its clinical implications
Rodríguez-Lara, V., Hernandez‐Martinez, J., & Arrieta, O. G. (2018) · Journal of Thoracic Disease · doi:10.21037/jtd.2017.12.61 · Cited by 113 · see citing works
“Similarly, it has been conclusively shown that males and females differ in their immunological responses (90,91).”
Result
Ethics of AI in Radiology: A Review of Ethical and Societal Implications
Goisauf, M., & Abadía, M. C. (2022) · Frontiers in Big Data · doi:10.3389/fdata.2022.850383 · Cited by 119 · see citing works
“, how gender and race shapes and affects biomedicine and healthcare practice (Roberts, 2008; Schiebinger and Schraudner, 2011; Oertelt-Prigione, 2012; Kaufman, 2013) or how gender and racial bias in algorithms could have a negative impact in certain areas of society (e.”
Background
Effects of the breed, sex and age on cellular content and growth factor release from equine pure-platelet rich plasma and pure-platelet rich gel
Giraldo, C. E., López, C., Álvarez, M. E., Samudio, I. J., Prades, M., & Carmona, J. U. (2013) · BMC Veterinary Research · doi:10.1186/1746-6148-9-29 · Cited by 103 · see citing works
“While it is known that hormonal influences could be associated with these hematological gender differences in human beings [20], we did not measure the concentration of sexual hormones in horses from our study to support this hypothesis.”
Result
Sex disparities in clinical characteristics and prognosis of immunoglobulin G4–related disease: a prospective study of 403 patients
Wang, L., Zhang, P., Zhang, X., Lin, W., Tang, H., Li, J., Wang, M., Liu, X., Fei, Y., Chen, H., et al. (2018) · Lara D. Veeken · doi:10.1093/rheumatology/key397 · Cited by 103 · see citing works
Etiology of myasthenia gravis: Innate immunity signature in pathological thymus
Cavalcante, P., Cufi, P., Mantegazza, R., Berrih‐Aknin, S., Bernasconi, P., & Panse, R. L. (2013) · Autoimmunity Reviews · doi:10.1016/j.autrev.2013.03.010 · Cited by 99 · see citing works
Estrogen, estrogen-like molecules and autoimmune diseases
Merrheim, J., Villegas, J. A., Wassenhove, J. V., Khansa, R., Berrih‐Aknin, S., Panse, R. L., & Dragin, N. (2020) · Autoimmunity Reviews · doi:10.1016/j.autrev.2020.102468 · Cited by 100 · see citing works
Interpersonal life stress, inflammation, and depression in adolescence: Testing Social Signal Transduction Theory of Depression
Slavich, G. M., Giletta, M., Helms, S. W., Hastings, P. D., Rudolph, K. D., Nock, M. K., & Prinstein, M. J. (2020) · Depression and Anxiety · doi:10.1002/da.22987 · Cited by 98 · see citing works
“Finally, concentrations of the sex hormones estrogen and progesterone, which undergo major changes as girls become more pubertally developed, can enhance the depressogenic potential of cytokines (Oertelt-Prigione, 2012; Schwarz & Bilbo, 2012), and this may explain why rates of MDD increase so substantially for adolesc…”
Sex, gender and immunosenescence: a key to understand the different lifespan between men and women?
Caruso, C., Accardi, G., Virruso, C., & Candore, G. (2013) · Immunity & Ageing · doi:10.1186/1742-4933-10-20 · Cited by 92 · see citing works
“While from a gender point of view food intake and variety, exposure to nonmicrobiological antigens and health care access have to be take into account [2,10].”
Background
Peripheral immune cell reactivity and neural response to reward in patients with depression and anhedonia
Costi, S., Morris, L. S., Collins, A., Fernandez, N. F., Patel, M., Xie, H., Kim-Schulze, S., Stern, E. R., Collins, K. A., Cathomas, F., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01668-1 · Cited by 87 · see citing works
The effect of sex on immune cells in healthy aging: Elderly women have more robust natural killer lymphocytes than do elderly men
Al‐Attar, A., Presnell, S. R., Peterson, C. A., Thomas, D. T., & Lutz, C. T. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.04.001 · Cited by 88 · see citing works
The association of mid-to late-life systemic inflammation with white matter structure in older adults: The Atherosclerosis Risk in Communities Study
Walker, K. A., Windham, B. G., Power, M. C., Hoogeveen, R. C., Folsom, A. R., Ballantyne, C. M., Knopman, D. S., Selvin, E., Jack, C. R., & Gottesman, R. F. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.03.031 · Cited by 89 · see citing works
Impact of sex disparities on the clinical manifestations in patients with systemic lupus erythematosus
Boodhoo, K. D., Liu, S., & Zuo, X. (2016) · Medicine · doi:10.1097/md.0000000000004272 · Cited by 87 · see citing works
“It is generally recognized that the male hormone, testosterone, is immunosuppressive, whereas the female hormone, estrogen, stimulates immune response.([23,24]) Lower”
Sex/gender-related differences in inflammaging
Olivieri, F., Marchegiani, F., Matacchione, G., Giuliani, A., Ramini, D., Fazioli, F., Sabbatinelli, J., & Bonafè, M. (2023) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2023.111792 · Cited by 86 · see citing works
“…modulate immunosenescence differently in men and women, it has been highlighted that in the reproductive age steroids can differentially modulate the immune system; while estrogens increase the immune response, progesterone and androgens exert immune suppressive actions (Oertelt-Prigione, 2012).”
An intracrine view of sex steroids, immunity, and metabolic regulation
Rubinow, K. B. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.03.001 · Cited by 82 · see citing works
Soluble Mediators Regulating Immunity in Early Life
Pettengill, M. A., van Haren, S. D., & Levy, O. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00457 · Cited by 84 · see citing works
Sex-specific regulation of immune responses by PPARs
Park, H.-J., & Choi, J. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.102 · Cited by 86 · see citing works
Age and sex in drug development and testing for adults
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“For example, the action of gonadal hormones up- or down-regulates cytokine levels, cell numbers, and receptor expression for many types of immune cells, and this varies with age [27,28].”
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Regulation of mi RNA biogenesis and turnover in the immune system
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“Estrogens are steroid hormones that mediate sex differences, but they also affect the function of lymphocytes and monocytes and may contribute to the increased frequency of autoimmune disorders in females (65).”
Background
CCL19 as a Chemokine Risk Factor for Posttreatment Lyme Disease Syndrome: a Prospective Clinical Cohort Study
Aucott, J. N., Soloski, M. J., Rebman, A. W., Crowder, L. A., Lahey, L. J., Wagner, C. A., Robinson, W. H., & Bechtold, K. T. (2016) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00071-16 · Cited by 83 · see citing works
Gender Differences of B Cell Signature in Healthy Subjects Underlie Disparities in Incidence and Course of SLE Related to Estrogen
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Aging-associated DNA methylation changes in middle-aged individuals: the Young Finns study
Kananen, L., Marttila, S., Nevalainen, T., Jylhävä, J., Mononen, N., Kähönen, M. A. P., Raitakari, O. T., Lehtimäki, T. J., & Hurme, M. (2016) · BMC Genomics · doi:10.1186/s12864-016-2421-z · Cited by 81 · see citing works
“As aging influences the immune system of men and women differently and as the risk rates of several diseases between sexes are unequal [25, 26], 1) an interaction analysis was performed to address the sex specificity of a-CpGs, and 2) the aging-associations were also evaluated in separate analyses among men and women.”
Method
Matters of the heart: Cellular sex differences
Walker, C. J., Schroeder, M. E., Aguado, B. A., Anseth, K. S., & Leinwand, L. A. (2021) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2021.04.010 · Cited by 74 · see citing works
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Achalasia and Obstructive Motor Disorders Are Not Uncommon in Patients With Eosinophilic Esophagitis
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“Although the impact of the expression differences between male and female HUVEC for the in vivo situation remains to be elucidated, our data in endothelial cells are in accordancewith the clinical finding that overall immune reactivity is higher in females than in males [30].”
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Pulmonary group 2 innate lymphoid cells: surprises and challenges
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“Several immune cell lineages, including myeloid cells and lymphocytes express receptors for estrogen, progesterone and androgens (testosterone, dihydrotestosterone and androstenedione) and are hormone regulated and influence both innate and adaptive immune responses.(96) In macrophages, estrogen receptor signaling inh…”
The fate is not always written in the genes: Epigenomics in epidemiologic studies
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“Since personal characteristics, behaviors, exogenous exposures, or pathologic states can modulate the circulating immune profile [Cheng et al., 2004; Mehta et al., 2008; Szabo and Mandrekar, 2009; Federico et al., 2010; Kiecolt-Glaser et al., 2010; Oertelt-Prigione, 2012], inter-subject variation in leukocyte distribu…”
Risk factors for immune-related adverse events: what have we learned and what lies ahead?
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“Immune system function is known to vary between sexes as a result of hormonal and genetic effects [114].”
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Gender aspects in food allergy
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Sex and gender affect immune aging
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“For example, the transmission of sexually transmitted diseases is faster in women who use oral contraceptives than in men, particularly in the case of HIV infection (Oertelt-Prigione, 2012; Addo and Altfel, 2014).”
BackgroundInfluential
The limitations and hidden gems of the epidemiology of primary biliary cirrhosis
Podda, M., Selmi, C. F., Lleò, A., Moroni, L., & Invernizzi, P. (2013) · Journal of Autoimmunity · doi:10.1016/j.jaut.2013.06.015 · Cited by 71 · see citing works
Developmental Exposure to Bisphenol A Modulates Innate but Not Adaptive Immune Responses to Influenza A Virus Infection
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“However, the idea that estrogens polarize toward Th2-biased responses is likely an oversimplification of the physiological and pharmacological effects of endogenous and exogenous estrogens on immune function [64], and therefore is probably not an adequate explanation.”
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TLR7, IFNγ, and T-bet: Their roles in the development of ABCs in female-biased autoimmunity
Rubtsova, K., Marrack, P., & Rubtsov, A. V. (2014) · Cellular Immunology · doi:10.1016/j.cellimm.2014.12.002 · Cited by 69 · see citing works
“It is a welldocumented fact that there are differences in immune responses between males and females [1].”
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Self-protection as an adaptive female strategy
Benenson, J. F., Webb, C. E., & Wrangham, R. W. (2021) · Behavioral and Brain Sciences · doi:10.1017/s0140525x21002417 · Cited by 70 · see citing works
Passive transfer of narcolepsy: Anti-TRIB2 autoantibody positive patient IgG causes hypothalamic orexin neuron loss and sleep attacks in mice
Katzav, A., Arango, M., Kivity, S., Tanaka, S., Givaty, G., Agmon‐Levin, N., Honda, M., Anaya, J., Chapman, J., & Shoenfeld, Y. (2013) · Journal of Autoimmunity · doi:10.1016/j.jaut.2013.06.010 · Cited by 66 · see citing works
Environmentally enriched housing conditions affect pig welfare, immune system and gut microbiota in early life
Wen, C., van Dixhoorn, I. D. E., Schokker, D., Woelders, H., Stockhofe-Zurwieden, N., Rebel, J. M. J., & Smidt, H. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00115-2 · Cited by 65 · see citing works
The Natural Agonist of Estrogen Receptor β Silibinin Plays an Immunosuppressive Role Representing a Potential Therapeutic Tool in Rheumatoid Arthritis
Dupuis, M. L., Conti, F., Maselli, A., Pagano, M., Ruggieri, A., Anticoli, S., Fragale, A., Gabriele, L., Gagliardi, M. C., Sanchez, M., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01903 · Cited by 64 · see citing works
“The immunomodulatory effects exerted by E2 are, at least partially, responsible for the existing differences between female and male immune systems, with females mounting stronger humoral and cellular immune responses than males (6).”
Background
Long-term exposure to low 17α-ethinylestradiol (EE2) concentrations disrupts both the reproductive and the immune system of juvenile rainbow trout, Oncorhynchus mykiss
Rehberger, K., von Siebenthal, E. W., Bailey, C., Bregy, P., Fasel, M., Herzog, E. L., Neumann, S., Schmidt‐Posthaus, H., & Segner, H. E. (2020) · Environment International · doi:10.1016/j.envint.2020.105836 · Cited by 64 · see citing works
“Since the response of fish to toxicants as well as pathogens may differ between sexes (Koehler 2004, Le Manach et al., 2016, Oertelt-Prigione 2012, Winzer et al., 2002a, Winzer et al., 2002b), we analyzed the data for male and female fish separately.”
Background
Normal Values of T, B and NK Lymphocyte Subpopulations in Peripheral Blood of Healthy Cuban Adults
Kokuina, E., Breff-Fonseca, M. C., Valverde, C. A. V., & Díaz, I. M. (2019) · MEDICC Review · doi:10.37757/mr2019.v21.n2-3.5 · Cited by 59 · see citing works
“[36,37] The difference in values of CD3+CD4+ cells can be attributed to the effect of sex hormones on their specifi c receptors expressed in T and B lymphocytes.[38] Sex chromosome genes and sex hormones such as estrogen, progesterone and androgens contribute to male/female differences in immune response.”
Background
Impact of progesterone on the immune system in women: a systematic literature review
Zwahlen, M., & Stute, P. (2023) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-023-06996-9 · Cited by 59 · see citing works
Risk factors of transient and permanent hypoparathyroidism after thyroidectomy: a systematic review and meta-analysis
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“Additionally, females often exhibit stronger immune responses, which may affect postoperative in ﬂ ammation and healing processes, thereby increasing the risk of hypoPT [116] .”
Background
Balance between Estrogens and Proinflammatory Cytokines Regulates Chemokine Production Involved in Thymic Germinal Center Formation
Dragin, N., Nancy, P., Villegas, J. A., Roussin, R., Panse, R. L., & Berrih‐Aknin, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-08631-5 · Cited by 58 · see citing works
The causes and consequences of variation in human cytokine production in health
Schirmer, M., Kumar, V., Netea, M. G., & Xavier, R. J. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.05.012 · Cited by 58 · see citing works
Breach of Tolerance: Primary Biliary Cirrhosis
Wang, L., Chang, C. C.-C., Gershwin, M. E., & Wang, F. (2014) · Seminars in Liver Disease · doi:10.1055/s-0034-1383729 · Cited by 54 · see citing works
Do Human Endogenous Retroviruses Contribute to Multiple Sclerosis, and if So, How?
Morris, G., Maes, M. H. J., Murdjeva, M., & Puri, B. K. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1255-x · Cited by 57 · see citing works
Honey bee protein atlas at organ-level resolutionPreprint
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“In humans, there are measurable differences between males and females with regard to lipid metabolism (Sugiyama and Agellon 2012), the handling of oxidative stress (Vina et al. 2011), and the immune system (Oertelt-Prigione 2012), to name a few.”
Background
Gender-Related Effects of Sex Steroids on Histamine Release and FcεRI Expression in Rat Peritoneal Mast Cells
Muñoz-Cruz, S., Mendoza-Rodríguez, Y., Nava-Castro, K. E., Yepez-Mulia, L., & Morales-Montor, J. (2015) · Journal of Immunology Research · doi:10.1155/2015/351829 · Cited by 54 · see citing works
“Thus, in addition to the immune factors that regulate the complex immunoendocrine network, gender might have a significant function in shaping the immune response [2].”
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Gender Differences in Acute and Chronic Pain in the Emergency Department: Results of the 2014Academic Emergency MedicineConsensus Conference Pain Section
Musey, P. I., Linnstaedt, S. D., Platts-Mills, T. F., Miner, J. R., Bortsov, A. V., Safdar, B., Bijur, P., Rosenau, A., Tsze, D. S., Chang, A. K., et al. (2014) · Academic Emergency Medicine · doi:10.1111/acem.12529 · Cited by 55 · see citing works
Sex‐specific control of central nervous system autoimmunity by p38 mitogen‐activated protein kinase signaling in myeloid cells
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“In humans, gender influences immunity, although controversial results regarding gender and/or sex hormone treatment in ex vivo studies are frequently reported.(58) p38 MAPK is well known to control proinflammatory functions in human monocytes/macrophages,(6) but to the best of our knowledge, little has been reported o…”
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Reference Values for Peripheral Blood Lymphocyte Subsets in a Healthy Korean Population
Choi, J., Lee, S. J., Lee, Y. A., Maeng, H. G., Lee, J. K., & Kang, Y. W. (2014) · Immune Network · doi:10.4110/in.2014.14.6.289 · Cited by 51 · see citing works
Proposal for targeted, neo-evolutionary-oriented, secondary prevention of early-onset endometriosis and adenomyosis. Part I: pathogenic aspects
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“In addition to local stimulation of eutopic and ectopic endometrium, oestrogens also exert a systemic pro-inflammatory effect (Straub, 2007; Oertelt-Prigione, 2012a,b; Cutolo et al. , 2014; Dodd and Menon, 2022).”
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Sex Disparities in Cancer Mortality: The Risks of Being a Man in the United States
Najari, B. B., Rink, M., Li, P. S., Karakiewicz, P. I., Scherr, D. S., Shabsigh, R., Meryn, S., Schlegel, P. N., & Shariat, S. F. (2012) · The Journal of Urology · doi:10.1016/j.juro.2012.11.153 · Cited by 48 · see citing works
Gender Differences in Cardiovascular Drugs
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Immunology and Reproduction
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Selection for brain size impairs innate, but not adaptive immune responses
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The conneXion between sex and immune responses
Forsyth, K. S., Jiwrajka, N., Lovell, C. D., Toothacre, N. E., & Anguera, M. C. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-00996-9 · Cited by 226 · see citing works
Immune Response—The Impact of Biological Sex and Gender
Oertelt‐Prigione, S. (2017) · Principles of Gender-Specific Medicine · doi:10.1016/b978-0-12-803506-1.00023-1 · Cited by 1 · see citing works
Self-citation
Effect of Sex on Humoral and Innate Immunity
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Immune Cells Have Sex and So Should Journal Articles
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Sexual Dimorphism in Innate Immunity
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Authors: Oertelt-Prigione, S.
Venue: Autoimmunity Reviews
Publisher: Elsevier BV
Published: 2012-05
Volume: 11
Issue: 6-7
Pages: A479-A485
ISSN: 1568-9972 (ISSN-L)
DOI: 10.1016/j.autrev.2011.11.022
OpenAlex: W2045019335
Cited by: 459
References: 102
Citations by year: 2026: 21 · 2025: 31 · 2024: 38 · 2023: 28 · 2022: 32 · 2021: 43 · 2020: 45 · 2019: 23 · 2018: 28 · 2017: 35 · 2016: 32 · 2015: 36 · 2014: 37 · 2013: 22 · 2012: 7
FWCI: 3.21
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Autoimmunity Reviews (publishedVersion)
PubMed (publishedVersion)
Publikationen an der Universität Bielefeld (Universität Bielefeld) (submittedVersion)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
Keywords: sex differences in immune response, gender differences, autoimmune disease, sex hormones, estrogen, progesterone, testosterone, cytokine production, antibody production, B cells, granulocytes, natural killer cells, X chromosome, social determinants of health, health care access
MeSH terms: B-Lymphocytes, Bone Marrow Cells, Dendritic Cells, Female, Humans, Immunity, Active, Immunologic Factors, Killer Cells, Natural, Male, Sex Factors, Gonadal Steroid Hormones, T-Lymphocytes

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The influence of sex and gender on the immune response

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