Cited by 441Endometriosis Research and TreatmentReproductive System and PregnancyImmune Cell Function and Interaction

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Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium

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Oosterlynck, Didier J., Cornillie, Freddy J., Waer, Mark, Vandeputte, Michel, Koninckx, Philippe R.·1991·Fertility and Sterility

DOI 10.1016/s0015-0282(16)54414-8

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Abstract

Objective The role of natural killer (NK) cells in the decreased cellular immunity of women with endometriosis was investigated.Design, setting, patients Thirty-four women were investigated prospectively before a CO2-laser laparoscopy for infertility and/or pain at the University Hospital Gasthuisberg. Endometriosis was scored blindly.Main outcome measure The cytotoxicity, directed against the endometrium, was mediated by NK cells because this cytotoxicity could be removed by treating the effector cells with the NK-specific anti-Leu-11b monoclonal antibody. Consequently, we evaluated prospectively in those women the lymphocyte-mediated cytotoxicity toward NK sensitive (K562-assay) and autologous endometrial target cells.Results The NK activity (K562-assay) and the cytotoxicity against autologous endometrial cells were similarly decreased in women with endometriosis and correlated with the severity of the disease. Using heterologous effector cells, the decreased chromium release in women with endometriosis was less pronounced but still present.Conclusion The decreased cytotoxicity to endometrial cells in women with endometriosis is mainly because of a defect in NK activity but is also partially because of a resistance of the endometrium to NK cytotoxicity.

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Background
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Background
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“It has been suggested that persistence of endometrial cells at ectopic sites could be linked to a lack in their proper elimination by cytotoxic mechanisms mediated either by lymphocytes (Vigano et al., 1991), NK cells (Oosterlynck et al., 1991) or macrophages (Braun et al., 1998).”
Background
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Epidemiology of Endometriosis
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Immunoblot Detection of Decreased Antibodies to Haptoglobin-Like Protein in the Serum of Infertile Women with or without Endometriosis1
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“Significant changes have been shown in both cell-mediated immunity [4-7] and humoral immunity [8-11] in the PF and the serum of patients suffering from endometriosis.”
Background
The role of innate and adaptive immunity in endometriosis
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“[51] first found reduced cytotoxicity of NK cells in both peritoneal cavity and peripheral blood of patients with endometriosis, confirmed by subsequent studies [52].”
Result
The Effects of Dienogest on Macrophage and Natural Killer Cells in Adenomyosis: A Randomized Controlled Study.
Prathoomthong, S., Tingthanatikul, Y., Lertvikool, S., Rodratn, N., Waiyaput, W., Dittharot, K., Sroyraya, M., & Sophonsritsuk, A. (2018) · PubMed Central · doi:10.22074/ijfs.2018.5137 · Cited by 16
“The reduction of NK cell activity in peripheral blood and peritoneal fluid has been shown in endometriosis (18, 19).”
Background
Concentration of Interleukin‐12 in the peritoneal fluid is not influenced by the presence of endometriosis, its stage or the phase of the menstrual cycle
Gazvani, R., Bates, M. D., Vince, G. S., Christmas, S. E., Lewis‐Jones, I., & Kingsland, C. R. (2001) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.2001.080002175.x · Cited by 16
Coordinated but depressed expression of human leukocyte antigen-DR, intercellular adhesion molecule-1, and CD14 on peritoneal macrophages in women with pelvic endometriosis
Izumiya, C., Maeda, N., Kusume, T., Masumoto, T., Yamashita, C., Yamamoto, Y., Oguri, H., & Fukaya, T. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00780-5 · Cited by 16
Toll-Like Receptor Responsiveness of Peripheral Blood Mononuclear Cells in Young Women with Dysmenorrhea
Evans, S., Kwok, Y. H., Solterbeck, A., Liu, J., Hutchinson, M. R., Hull, M. L., & Rolan, P. E. (2020) · Journal of Pain Research · doi:10.2147/jpr.s219684 · Cited by 15
Low-dose mifepristone increases uterine natural killer cell cytotoxicity and perforin expression during the receptive phase
Zhou, F., Chen, X., Zhuang, Y., Chen, Y., & Huang, L. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.074 · Cited by 15
p27kip1 overexpression regulates IL-1β in the microenvironment of stem cells and eutopic endometriosis co-cultures
Gonçalves, G. A., Invitti, A. L., Parreira, R. M., Kopelman, A., Schor, E., & Girão, M. J. B. C. (2016) · Cytokine · doi:10.1016/j.cyto.2015.12.015 · Cited by 15
Soluble HLA-G in the peritoneal fluid of women with endometriosis
Eidukaitė, A., & Tamošiūnas, V. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.02.036 · Cited by 15
The Protective Role of Dexpanthenol on the Endometrial Implants in an Experimentally Induced Rat Endometriosis Model
Karapınar, O. S., Pınar, N., Özgür, T., Özcan, O., Bayraktar, H. S., Kurt, R. K., & Nural, O. (2016) · Reproductive Sciences · doi:10.1177/1933719116653682 · Cited by 14
Sexual dimorphism in immunity and longevity among the oldest old
Arakelyan, N. A., Kupriyanova, D. A., Vasiļevska, J., & Rogaev, E. I. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1525948 · Cited by 14
Protective Effects of Colchicine in an Experimental Rat Endometriosis Model: Histopathological Evaluation and Assessment of TNF-α Levels
Kurt, R. K., Pınar, N., Karateke, A., Okyay, A. G., Şilfeler, D. B., Albayrak, A., Özdemir, Ş., & Hakverdi, A. U. (2014) · Reproductive Sciences · doi:10.1177/1933719114542029 · Cited by 13
Decreased human leukocyte antigen–DR expression in the lipid raft by peritoneal macrophages from women with endometriosis
Yamamoto, Y., Maeda, N., Izumiya, C., Kusume, T., Oguri, H., Kawashima, M., Hayashi, K., Nomura, A., Yamashita, C., & Fukaya, T. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.02.027 · Cited by 13
Spread of endometriosis to pelvic sentinel lymph nodes: gene expression analysis
Buerkle, B., Notscheid, N. K., Scheich, J., Hefler, L., Tempfer, C. M., Horvat, R., & Rezniczek, G. A. (2013) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2013.03.029 · Cited by 13
“Endometriosis is considered to be an inflammatory disease [30] and EL contain significantly elevated levels of macrophages [31].”
Background
Aberrant Expression of CD95 and CD69 Molecules among CD56+ Cells in Women with Endometriosis
Eidukaitė, A., Šiaurys, A., & Tamošiūnas, V. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2005.00360.x · Cited by 13
Molecular Action of GnRH Analogues on Ectopic Endometrial Cells
Vignali, M. (1998) · Gynecologic and Obstetric Investigation · doi:10.1159/000052845 · Cited by 13
Suppression of natural killer cell activity by splenocyte transplantation in a rat model of endometriosis
Ota, H., Rong, H., Igarashi, S., & Tanaka, T. (2002) · Human Reproduction · doi:10.1093/humrep/17.6.1453 · Cited by 12
Inhibitory KIR2DL2 Gene: Risk for Deep Endometriosis in Euro-descendants
Marin, M. L. C., Coelho, V. P. C. V., Visentainer, J. E. L., Alves, H. V., Kohler, K. F., Rached, M. R., Abrão, M. S., & Kalil, J. E. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00255-x · Cited by 12
Serum cytokine and growth factor levels in patients with endometriosis
Kubatova, A., Erdem, A., Erdem, M., FiratMutlu, M., & Korucuoğlu, Ü. (2013) · Central European Journal of Immunology · doi:10.5114/ceji.2013.39768 · Cited by 12
“Transforming growth factor β1 expressions by eutopic and ectopic endometrial tissues have been studied immunohistochemically [15, 16].”
Background
Focused ultrasound for the diagnosis of non-palpable endometriotic lesions of the abdominal wall: a not-uncommon surgical complication
Cocco, G., Ricci, V., Boccatonda, A., & Schiavone, C. (2020) · Journal of Ultrasound · doi:10.1007/s40477-019-00425-x · Cited by 11
Plasma and Peritoneal Poly (ADP-Ribose) Polymerase Levels in Patients with Endometriosis
Kacperczyk-Bartnik, J. P., Bartnik, P., Goławski, K., Sierdziński, J., Mańka, G., Kiecka, M., Lipa, M., Warzecha, D., Spaczyński, R., Piekarski, P., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10102451 · Cited by 11
“Compromised natural-killer-cell activity in the peritoneal fluid can lead to decreased surveillance of ectopic tissue [15].”
Background
Endometrial galectin‐3 causes endometriosis by supporting eutopic endometrial cell survival and engraftment in the peritoneal cavity
Yamashita, S., Hashimoto, K., Sawada, I., Ogawa, M., Nakatsuka, E., Kawano, M., Kinose, Y., Kodama, M., Sawada, K., & Kimura, T. (2022) · American Journal of Reproductive Immunology · doi:10.1111/aji.13533 · Cited by 11
Myeloid-derived suppressor cells: A new emerging player in endometriosis
Zhang, T., He, Y., Man, G. C. W., Ding, Y., Wang, C. C., & Chung, J. P. W. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2022.11.004 · Cited by 13
A functional promoter polymorphism in interleukin 12B gene is associated with an increased risk of ovarian endometriosis
Zhao, W., Li, Y., Zhao, J., & Kang, S. (2018) · Gene · doi:10.1016/j.gene.2018.04.082 · Cited by 11
Th2 Cells and Th17 Cells in the Development of Endometriosis – Possible Roles of Interleukin-4 and Interleukin-17A
Osuga, Y., Hirota, Y., Hirata, T., Takamura, M., Urata, Y., Harada, M., Izumi, G., Fujii, T., & Koga, K. (2016) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.5000257 · Cited by 11
“Cytotoxicity of natural killer (NK) cells is also reduced in women with endometriosis (13, 14).”
Background
The Adhesion Molecules on Human Endometrial Stromal Cells
Busacca, M., Viganò, P., Magri, B., & Vignali, M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb21734.x · Cited by 11
Studies on the Human Leukocyte Antigen Class I Antigens in Japanese Patients with Macroscopically Diagnosed Endometriosis
Ishii, K., Takakuwa, K., Adachi, H., Higashino, M., Hataya, I., & Tanaka, K. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000067882 · Cited by 11
No association between HLA-DRB1 alleles and susceptibility to advanced stage endometriosis in a Korean population
Whang, D. H., Kim, S. H., Choi, Y. M., Park, M. H., Noh, J. H., & Kim, Y. B. (2005) · Human Reproduction · doi:10.1093/humrep/dei304 · Cited by 11
“Decreased T-cell reactivity and natural killer cell-mediated cytotoxicity have also been demonstrated in patients with the disease (Dmowski et al., 1981; Oosterlynck et al., 1991).”
Background
A Preliminary Investigation of the Roles of Endometrial Cells in Endometriosis Development via In Vitro and In Vivo Analyses
Cheng, Y.-H., Huang, C., Lien, H.-T., Hsiao, Y.-Y., Weng, P.-L., Chang, Y.-C., Cheng, J., & Lan, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073873 · Cited by 10
“Several factors contribute to the development of endometriosis, including coelomic metaplasia [6], dysfunctional cellular immunity [7–9], genetic factors [10], and a multifactorial mode of inheritance involving specific genes and aberrant environmental factors [11].”
Background
Proangiogenic properties of complement protein C1q can contribute to endometriosis
Agostinis, C., Toffoli, M., Zito, G., Balduit, A., Pegoraro, S., Spazzapan, M., Pascolo, L., Romano, F., Lorenzo, G. D., Mangogna, A., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1405597 · Cited by 10
“In EM, a decreased activity of peritoneal blood and peritoneal NK cells has consistently been reported, displaying reduced cytotoxicity and chemotaxis (37 – 41).”
Background
The Lymphatic System in Endometriosis: a Pilot Study of Endometrial-Like Cells and Immune Cell Populations in Lymph Nodes Associated with Deep Infiltrating Bowel Lesions
Jerman, L. F., Anderson, L. A., Markham, R., & Hey‐Cunningham, A. J. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00171-0 · Cited by 12
The effects of thalidomide in a rat model of surgically-induced endometriosis
Bakacak, M., Ercan, Ö., Köstü, B., Bostancı, M. S., İnanç, F., Yaylalı, A., Serin, S., Balakan, O., & Kıran, G. (2015) · Journal of Turkish Society of Obstetric and Gynecology · doi:10.4274/tjod.71601 · Cited by 10
“With a genetic predisposition, the endometrial tissue is implanted through transmesothelial invasion when the immune clearance mechanism and inflammatory cytokines are insufficient(4,5).”
Background
Induction of Endometriosis and Adenomyosis by Transvaginal Pituitary Transplantation in Mice with and without Natural Killer Cell Activity
KOUJYO, T., Hatakeyama, S., Yamada, H., Iwabuchi, K., Kajino, K., Ogasawara, K., Onoé, K., & Fujimoto, S. (1998) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1998.tb00431.x · Cited by 10
Danazol Suppresses Both Spontaneous and Activated Human Lymphocyte‐Mediated Cytotoxicity
Viganò, P., Blasio, A. M. D., Busacca, M., Sabbadini, M. G., & Vignali, M. (1992) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1992.tb00754.x · Cited by 10
Hypersensitive intercellular responses of endometrial stromal cells drive invasion in endometriosis
Chen, C.-W., Chavez, J. B., Lin, L.-L., Wang, C., Hsu, Y., Hart, M. J., Ruan, J., Gillette, L., Burney, R. O., Schenken, R. S., et al. (2024) · eLife · doi:10.7554/elife.94778 · Cited by 8
The Effect of Mesenchymal Stromal Cells Derived From Endometriotic Lesions on Natural Killer Cell Function
Abomaray, F., Wagner, A. K., Chrobok, M., Ekblad, Å., Gidlöf, S. B., Alici, E., & Gotherstrom, C. O. T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.612714 · Cited by 9
“One of the components of this reduced immunosurveillance is the inhibition of NK cells (Oosterlynck et al., 1991; Oosterlynck et al., 1992; Liu et al., 2018; Xu, 2019).”
BackgroundMethodInfluential
The deviations of CD4 + T cells during peripheral blood and peritoneal fluid of endometriosis: a systematic review and meta-analysis
Yang, H., & Zhuang, Y. (2023) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-023-06964-3 · Cited by 9
“…Youhong [39], Wang Zhilian [40], Ma Yanping [41], Hu Sha [42] and so on, have reported increased frequency of CD4 + cells in PB of Ems; however, Zhang C [43], Szyllo K [44], Oosterlynck DJ [26], Mier-Cabrera J [32] and so on, have reported no statistical difference between EMs and healthy women.”
Background
Immunosuppressive effect of danazol on lymphocyte-mediated cytotoxicity toward human endometrial stromal cells
Viganò, P., Blasio, A. M. D., Busacca, M., & Vignali, M. (1994) · Gynecological Endocrinology · doi:10.3109/09513599409028452 · Cited by 9
Endometriosis
Kocakoç, E., Bhatt, S., & Dogra, V. S. (2008) · Ultrasound Clinics · doi:10.1016/j.cult.2008.07.001 · Cited by 9
Pentoxifylline versus medical therapies for subfertile women with endometriosis
Lv, D., Song, H., Li, Y.-L., & Clarke, J. (2009) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007677 · Cited by 10

Authors: Oosterlynck, D. J., Cornillie, F. J., Waer, M., Vandeputte, M., & Koninckx, P. R.
Affiliations: Rega Institute for Medical Research (BE)
Venue: Fertility and Sterility
Publisher: Elsevier BV
Published: 1991-07
Volume: 56
Issue: 1
Pages: 45-51
ISSN: 0015-0282 (ISSN-L)
DOI: 10.1016/s0015-0282(16)54414-8
OpenAlex: W141728048
Cited by: 441
References: 13
Citations by year: 2026: 3 · 2025: 9 · 2024: 11 · 2023: 6 · 2022: 13 · 2021: 12 · 2020: 18 · 2019: 12 · 2018: 11 · 2017: 7 · 2016: 12 · 2015: 14 · 2014: 21 · 2013: 16 · 2012: 13
FWCI: 16.08
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 11288 d)
Locations: Fertility and Sterility (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
Keywords: endometriosis, natural killer cells, NK cell cytotoxicity, cell-mediated immunity, infertility, disease severity
MeSH terms: Chromium Radioisotopes, Cytotoxicity, Immunologic, Endometriosis, Endometrium, Female, Flow Cytometry, Humans, Immunity, Cellular, Killer Cells, Natural, Leukocyte Count, Prospective Studies

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Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium

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