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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Agostinis, C., Balduit, A., Mangogna, A., Zito, G., Romano, F., Ricci, G., Kishore, U., & Bulla, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.599117 · Cited by 123
Immunological aspects of endometriosis
Vinatier, D. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.371 · Cited by 114
“In endometriosis, the endometrium becomes resistant to the cytotoxicity of NK cells, as it is less efficiently destroyed by NK cells obtained from men, compared to endometrium of women without endometriosis (Oosterlynck et al., 1991).”
Background
Pathogenesis of endometriosis
Nap, A. W., Groothuis, P. G., Demir, A. Y., Evers, J. L. H., & Dunselman, G. A. J. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.005 · Cited by 138
Pathogenesis of endometriosis
Rock, J. A., & Markham, S. M. (1992) · The Lancet · doi:10.1016/0140-6736(92)92959-j · Cited by 110
Platelet-derived TGF-β1 mediates the down-modulation of NKG2D expression and may be responsible for impaired natural killer (NK) cytotoxicity in women with endometriosis
Guo, S., Du, Y., & Liu, X. (2016) · Human Reproduction · doi:10.1093/humrep/dew057 · Cited by 111
Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis
Wu, M., Yang, J., Chao, K., Hwang, J.-L., Yang, Y., & Ho, H. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01592-2 · Cited by 105
Implantation versus infiltration: the Sampson versus the endometriotic disease theory
Koninckx, P. R., Barlow, D., & Kennedy, S. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052853 · Cited by 100
Decreased apoptosis and sensitivity to macrophage mediated cytolysis of endometrial cells in endometriosis
Dmowski, W. P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.696 · Cited by 101
“More than 70 years ago, John Sampson (1925) proposed that endometriosis develops as a result of the ’retrograde tubal regurgitation’ of endometrial cells and tissue fragments followed by implantation of these cells and tissue fragments in the ectopic locations.”
Background
Animal Studies in Endometriosis: A Review
Story, L., & Kennedy, S. (2004) · ILAR Journal · doi:10.1093/ilar.45.2.132 · Cited by 94
“…women may experience some degree of retrograde menstruation (Halme et al. 1984) yet not all develop endometriosis, which has led to the hypothesis that women with endometriosis have decreased immunological clearance of shed endometrial cells within the peritoneal cavity (Oosterlynck et al. 1991).”
Increased killer inhibitory receptor KIR2DL1 expression among natural killer cells in women with pelvic endometriosis
Maeda, N., Izumiya, C., Yamamoto, Y., Oguri, H., Kusume, T., & Fukaya, T. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02964-8 · Cited by 93
“In a previous report, NK cell activity in peritoneal blood similarly failed to recover after LASER cautery of the endometriotic lesion (33).”
Background
Implantation Defects in Infertile Women with Endometriosis
Lessey, B. A. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02787.x · Cited by 92
Secretion of monocyte chemotactic protein-1 by cytokine-stimulated endometrial cells of women with endometriosis
Akoum, A., Lemay, A., Brunet, C., & Hébert, J. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57363-4 · Cited by 92
Granulated metrial gland cells: A natural killer cell subset of the pregnant murine uterus
Croy, B. A., & Kiso, Y. (1993) · Microscopy Research and Technique · doi:10.1002/jemt.1070250302 · Cited by 92
“Indeed, endometriosis in women is reported to correlate with decreased NK cell activity (Oosterlynck et al., 1991).”
Background
异常在位子宫内膜是内异症的病因吗？-在位内膜在内异症发病中的作用
Liu, H., & Lang, J. H. (2011) · Medical Science Monitor · doi:10.12659/msm.881707 · Cited by 93
“There is a decreased cytotoxic activity of NK cells in peripheral blood and peritoneal fluid from patients with endometriosis [9,10].”
Background
Anti-TNF-α treatment for pelvic pain associated with endometriosis
Lu, D., Song, H., & Shi, G. (2013) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd008088.pub3 · Cited by 91
Characterization of Lymphocyte Subpopulations and T Cell Activation In Endometriosis
Witz, C. A., Montoya, I. A., DEY, T. D., & Schenken, R. S. (1994) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1994.tb01110.x · Cited by 90
Characterization of endometriosis-associated immune cell infiltrates (EMaICI)
Scheerer, C., Bauer, P., Chiàntera, V., Sehouli, J., Kaufmann, A. M., & Mechsner, S. (2016) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-016-4142-6 · Cited by 88
“Although in other studies [22], NK cells were present in the overall decreased numbers as scattered cells within the endometrial epithelium and stroma, their activity was reduced [6, 22, 23], and they were not capable of gathering in clusters.”
Result
Endometrial vascular and glandular expression of integrin alpha(v)beta3 in women with and without endometriosis
Hii, L. L., & Rogers, P. A. W. (1998) · Human Reproduction · doi:10.1093/humrep/13.4.1030 · Cited by 88
Suppression of natural killer cell activity by sera from patients with endometriosis
Kanzaki, H., Wang, H.-S., Kariya, M., & Mori, T. (1992) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(11)91670-6 · Cited by 87
Effects of dienogest, a synthetic steroid, on experimental endometriosis in rats
Katsuki, Y., Takano, Y., Futamura, Y., Shibutani, Y., Aoki, D., Udagawa, Y., & Nozawa, S. (1998) · European Journal of Endocrinology · doi:10.1530/eje.0.1380216 · Cited by 84
NK Cells as Potential Targets for Immunotherapy in Endometriosis
Ścieżyńska, A., Komorowski, M., Soszyńska, M., & Malejczyk, J. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8091468 · Cited by 83
“Unfortunately, endometrial cells were used as targets only in two independent studies [69,80].”
Background
The non-human primate model of endometriosis: research and implications for fecundity
Braundmeier, A. G., & Fazleabas, A. T. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap057 · Cited by 85
“It is known that endometriosis induces an inflammatory environment in the peritoneal cavity of women (Oosterlynck et al., 1991, 1994; D’Hooghe et al., 2001; Gazvani and Templeton, 2002; Umezawa et al., 2009), but does the presence of ectopic lesions also induce an inflammatory environment in the…”
Background
Pathogenesis of Endometriosis: The Role of Peritoneal Fluid
Koninckx, P. R., Kennedy, S., & Barlow, D. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052856 · Cited by 85
A Novel Noninvasive Model of Endometriosis for Monitoring the Efficacy of Antiangiogenic Therapy
Becker, C. M., Wright, R. D., Satchi‐Fainaro, R., Funakoshi, T., Folkman, J., Kung, A. L., & D’Amato, R. J. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.051133 · Cited by 84
“It has been reported that impaired immunity may be responsible for the local attachment and invasion of endometrial tissue.(12,13) Aromatase was found to be overexpressed in endometriotic lesions, while at the same time, production of 17- -hydroxysteroid dehydrogenase type 2 is reduced.”
Background
Treatment strategies for endometriosis
Rodgers, A. K., & Falcone, T. (2008) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.9.2.243 · Cited by 72
“Any decrease in these cells may lead to an increase in the number of active endometrial cells in the peritoneal cavity [14] .”
Background
Pathogenesis of Endometriosis
Witz, C. A. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049425 · Cited by 73

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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