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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Association between MMP1 and MMP9 activities and ICAM1 cleavage induced by tumor necrosis factor in stromal cell cultures from eutopic endometria of women with endometriosis
Pino, M., Galleguillos, C., Torres, M. J., Hugo Sovino, S., Fuentes, A., Boric, M. A., & Johnson, M. C. (2009) · Reproduction · doi:10.1530/rep-09-0196 · Cited by 42
“Alteration of the interaction between ITGAL and ICAM1 may be one of the crucial stimuli for the initiation and progression of endometriosis (Oosterlynck et al. 1991).”
Background
Evolving Spectrum:
Jensen, J. R., & Coddington, C. C. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7b84 · Cited by 39
“Decreased peripheral cytotoxicity toward endometrial cells has also been correlated with decreased natural killer cell activity.(52) Garzetti et al(53) studied 33 patients with variable stages of disease and observed a progressive reduction of natural killer cell activity with the increasing stage and spread of diseas…”
Background
Endometriosis: What is the Influence of Immune Cells?
Crispim, P. C. A., Jammal, M. P., Murta, E. F. C., & Nomelini, R. S. (2020) · Immunological Investigations · doi:10.1080/08820139.2020.1764577 · Cited by 40
“These cells have diminished function in women diagnosed with endometriosis to ensure the survival of endometrial cells in the peritoneal cavity (Oosterlynck et al. 1991; Sikora et al. 2011).”
Background
Expression of AhR and ARNT mRNA in Cultured Human Endometrial Explants Exposed to TCDD
Pitt, J. A. (2001) · Toxicological Sciences · doi:10.1093/toxsci/62.2.289 · Cited by 39
“, 1987), decreased cell-mediated immune function (Oosterlynck et al., 1991; Steeleet al., 1984), and diminished proliferative T-cell response to endometrial antigens (Gilmoreet al.”
Background
The impact of HLA-G, LILRB1 and LILRB2 gene polymorphisms on susceptibility to and severity of endometriosis
Bylińska, A., Wilczyńska, K., Malejczyk, J., Milewski, Ł., Wagner, M., Jasek, M., Niepiekło-Miniewska, W., Wiśniewski, A., Płoski, R., Barcz, E., et al. (2018) · Molecular Genetics and Genomics · doi:10.1007/s00438-017-1404-3 · Cited by 38
Pentoxifylline for endometriosis
Lu, D., Song, H., Li, Y., Clarke, J., & Shi, G. (2012) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007677.pub3 · Cited by 38
The effects of immunosuppression on development and progression of endometriosis in baboons (Papio anubis)
D’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., Jonge, I. D., Hill, J. A., & Koninckx, P. R. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57675-4 · Cited by 37
Enhanced Expression of Resident Leukocyte Interferon γ mRNA in Endometriosis
Klein, N. A., PÉRGOLA, G. M., TEKMAL, R. R., DEY, T. D., & Schenken, R. S. (1993) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1993.tb00605.x · Cited by 38
Telocytes Enhances M1 Differentiation and Phagocytosis While Inhibits Mitochondria-Mediated Apoptosis Via Activation of NF-κB in Macrophages
Huang, Y.-L., Zhang, F.-L., Tang, X.-L., & Yang, X. (2021) · Cell Transplantation · doi:10.1177/09636897211002762 · Cited by 37
The uterine immune profile: A method for individualizing the management of women who have failed to implant an embryo after IVF/ICSI
Lédée, N., Petitbarat, M., Prat-Ellenberg, L., Dray, G., Cassuto, N. G., Chevrier, L., Kazhalawi, A., Vezmar, K., & Chaouat, G. (2020) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2020.103207 · Cited by 36
The role of dendritic cells in endometriosis: A systematic review
Laginha, P. A., Arcoverde, F. V. L., Riccio, L. G. C., Andres, M. P., & Abrão, M. S. (2021) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2021.103462 · Cited by 37
Autoreactive epitopes within the human α-enolase and their recognition by sera from patients with endometriosis
Walter, M., Berg, H., Leidenberger, F. A., Schweppe, K.-W., & Northemann, W. (1995) · Journal of Autoimmunity · doi:10.1016/s0896-8411(95)80027-1 · Cited by 36
The Suppression of Peritoneal Cellular Immunity in Women With Endometriosis Could Be Restored After Gonadotropin Releasing Hormone Agonist Treatment
Wu, M., Chao, K., Chen, S., Chen, H., Yang, Y., Huang, S., & Ho, H. (1996) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1996.tb00050.x · Cited by 36
Cytotoxic T-Cells in Peripheral Blood in Women with Endometriosis
Slabe, N., Meden‐Vrtovec, H., Verdenik, I., Pogačnik, R. K., & Ihan, A. (2013) · Geburtshilfe und Frauenheilkunde · doi:10.1055/s-0033-1350702 · Cited by 35
Expression of Human Endogenous Gammaretroviral Sequences in Endometriosis and Ovarian Cancer
Hu, L., Hornung, D., Kurek, R., Östman, H., Blomberg, J., & Bergqvist, A. (2006) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2006.22.551 · Cited by 35
“25 Whether this is the result of a primary defect in the immune system or of different signaling from the desquamated endometrial cells is not known.”
Altered expression of interleukin-18 in the ectopic and eutopic endometrium of women with endometriosis
Luo, Q., Ning, W., Wu, Y., Zhu, X., Jin, F., Sheng, J., & Huang, H. (2006) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2006.03.003 · Cited by 35
“NK cells have shown alteration in women with endometriosis, and both peripheral and peritoneal NK cells from women with endometriosis displayed decreased cytotoxicity to autologous and heterologous endometrium (Oosterlynck et al., 1991; Wilson et al., 1994).”
Background
The endometria of patients with endometriosis show higher expression of class I human leukocyte antigen than the endometria of healthy women
Vernet-Tomás, M. D. M., Pérez-Ares, C. T., Verdú, N., Molinero, J. L., Fernández‐Figueras, M. T., & Carreras, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.06.057 · Cited by 35
“ince deficient NK activity has been found in women afected by endometriosis, it has been suggested that a particlar resistance of their endometria against NK lysis could xplain the development of endometriotic implants during etrograde menstruation (6, 7, 12).”
Background
3 Endometriosis: The host response
Grosskinsky, C. M., & Halme, J. K. (1993) · Baillière s Clinical Obstetrics and Gynaecology · doi:10.1016/s0950-3552(05)80459-6 · Cited by 35
The landscape of non-coding RNAs in the immunopathogenesis of Endometriosis
Abbaszadeh, M., Karimi, M., & Rajaei, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1223828 · Cited by 35
“Several investigations have revealed that women with endometriosis have NK cell malfunction, which leads to the immunological escape of fragments refluxed into the peritoneal cavity (95, 96).”
Background
Killer cell immunoglobulin-like receptors (KIR) and human leukocyte antigen-C (HLA-C) allorecognition patterns in women with endometriosis
Chou, Y.-C., Chen, C., Chen, M.-J., Chang, C.-W., Chen, P.-H., Yu, M., Chen, Y., Tsai, E., Yang, P.-S., Lin, S.-Y., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-61702-y · Cited by 34
Ultrasound Imaging of Abdominal Wall Endometriosis: A Pictorial Review
Cocco, G., Delli Pizzi, A., Scioscia, M., Ricci, V., Boccatonda, A., Candeloro, M., Tana, M., Balconi, G., Romano, M., & Schiavone, C. (2021) · Diagnostics · doi:10.3390/diagnostics11040609 · Cited by 34
Infection as a potential cofactor in the genetic-epigenetic pathophysiology of endometriosis: a systematic review
Koninckx, P. R., Ussia, A., Tahlak, M., Adamyan, L., Wattiez, A., Martin, D. C., & Gomel, V. (2019) · Lirias · Cited by 34
Primate Model Research for Endometriosis
Yamanaka, A., Kimura, F., Takebayashi, A., Kita, N., Takahashi, K., & Murakami, T. (2012) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.226.95 · Cited by 33
“…November 29, 2011; revision accepted for publication January 6, 2012. doi: 10.1620/tjem.226.95 Correspondence: Akiyoshi Yamanaka, Department of Obstetrics and Gynecology, Shiga University of Medical Science, Tsukinowa-cho, Otsu, Shiga, 520-2192, Japan. e-mail: ykiyoshi@belle.shiga-med.ac.jp”
BackgroundInfluential
Endometriosis Markers: Immunologic Alterations as Diagnostic Indicators for Endometriosis
BOHLER, H. C. L., Gerçel-Taylor, Ç., Lessey, B. A., & Taylor, D. D. (2007) · Reproductive Sciences · doi:10.1177/1933719107307910 · Cited by 34
Therapeutic potential of andrographolide for treating endometriosis
Zheng, Y., Liu, X., & Guo, S. (2012) · Human Reproduction · doi:10.1093/humrep/des063 · Cited by 34
“…by increased macrophage activation (Halme et al., 1984) and decreased NK cell cytotoxicity against endometrial and haematopoietic cells (Oosterlynck et al., 1991; Oosterlynck et al., 1993), while the latter is characterized by increased production of proinflammatory cytokines such as…”
Background
Genetic Contribution of the Interleukin‐10 Promoter Polymorphism in Endometriosis Susceptibility
Kitawaki, J., Obayashi, H., Ohta, M., Kado, N., Ishihara, H., Koshiba, H., Kusuki, I., Tsukamoto, K., Hasegawa, G., Nakamura, N., et al. (2002) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2002.1o029.x · Cited by 34
Soluble ICAM-1 levels in the serum of endometriotic patients appear to be independent of medical treatment
Matalliotakis, I., Vassiliadis, S., Goumenou, A. G., Athanassakis, I., Koumantakis, G. E., Neonaki, M., & Koumantakis, E. E. (2001) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(01)00064-x · Cited by 34
“Other laboratories had previously hypothesized that when endometriotic patients were treated by various regiments, the shedding of soluble ICAM-1 in the serum could block the attachment of cytotoxic T-cells and/or natural killer cells to ectopic endometriotic cells in the peritoneum and thereby prevent the formation o…”
Background
IMMUNOLOGY AND ENDOMETRIOSIS
Hill, J. A. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70305-3 · Cited by 34
Paracrine regulation of endometriotic tissue
Minici, F., Tiberi, F., Tropea, A., Miceli, F., Orlando, M., Gangale, M. F., Romani, F., Catino, S., Campo, S., Lanzone, A., et al. (2007) · Gynecological Endocrinology · doi:10.1080/09513590701581721 · Cited by 33
“The key factor involved in the abnormal autoimmune response is probably the presence of NK lymphocytes with a reduced cytotoxicity against autologous endometrium [19].”
Background
Patients With Endometriosis of the Rectosigmoid Have a Higher Percentage of Natural Killer Cells in Peripheral Blood
Dias, J., Podgaec, S., de Oliveira, R. M., Marin, M. L. C., Baracat, E. C., & Abrão, M. S. (2012) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2011.12.021 · Cited by 32
Expression of Soluble Adhesion Molecules in Sera of Women With Stage III and IV Endometriosis
Barrier, B. F., & Sharpe-Timms, K. L. (2002) · Journal of the Society for Gynecologic Investigation · doi:10.1177/107155760200900209 · Cited by 33
Glucocorticoid treatment decreases sera embryotoxicity in endometriosis patients
Simón, C., Gómez, E., Mir, A., Santos, M. J. D. L., & Pellicer, A. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55198-x · Cited by 33
Theories on the Pathogenesis of Endometriosis
Nap, A. W. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch5 · Cited by 33
Diagnostic Potential of Cytokine Biomarkers in Endometriosis: Challenges and Insights
Krygere, L., Jukna, P., Jarienė, K., & Drejerienė, E. (2024) · Biomedicines · doi:10.3390/biomedicines12122867 · Cited by 33
Expressions of natural cytotoxicity receptor, NKG2D and NKG2D ligands in endometriosis
Xu, H. (2019) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2019.102615 · Cited by 33

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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