The DOI matches its Crossref record; 51 of the 52 references it cites were found in a registry or an index.
Regulatory T cells and other leukocytes in the pathogenesis of endometriosis
Abstract
Endometriosis is a common and puzzling gynaecological condition which shows a great deal of variability between women. It affects up to 15% of all women of reproductive age. There is a strong familial component, but the aetiology and pathogenesis are still uncertain. Endometriosis is an 'inflammatory' condition with substantial numbers of leukocytes recruited into the lesion sites. There is increasing evidence to demonstrate marked changes in numbers and functions of these leukocytes in the eutopic endometrium and peritoneal fluid as well as in the lesions. We hypothesise that endometriosis is primarily an endometrial disease with underlying genetic disturbances which lead to a number of major molecular changes in function, enhancing the likelihood that viable fragments of endometrial tissue will pass through the fallopian tubes and attach and grow on the peritoneum. We have demonstrated disturbances in the populations of T cells, B cells, mast cells, dendritic cells and macrophages within the endometrium and ectopic lesions, and are intrigued by the potential for changes in regulatory T cells to influence disease establishment and progression. Interestingly, we have shown that in endometriosis, naturally occurring FOXP3+ regulatory T cells fail to undergo the expected decline in number during the secretory phase, which may account for a decreased ability of newly recruited leukocytes to initiate effective immune responses against viable endometrial fragments, permitting their survival and subsequent establishment. To better understand the pathogenesis of endometriosis, we must learn about how the immune system recognises this disease and how the endometrial immune response is regulated.
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“There is increasing evidence for marked changes in numbers and functions of leukocytes in the eutopic endometrium, peritoneal fluid, and in endometriotic lesions.68”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [68]
Citations
Cites
Dendritic cells and the control of immunity
Banchereau, J., & Steinman, R. M. (1998) · Nature · doi:10.1038/32588 · Cited by 14,486
Regulatory T Cells and Immune Tolerance
Sakaguchi, S., Yamaguchi, T., Nomura, T., & Ono, M. (2008) · Cell · doi:10.1016/j.cell.2008.05.009 · Cited by 5,475
Gabrilovich, D., Ishida, T., Oyama, T., Ran, S., Kravtsov, V., Nadaf, S., & Carbone, D. P. (1998) · Blood · doi:10.1182/blood.v92.11.4150 · Cited by 1,048
Kerschensteiner, M., Gallmeier, E., Behrens, L., Vargas-Leal, V., Misgeld, T., Klinkert, W. E. F., Kolbeck, R., Hoppe, E., Oropeza-Wekerle, R. L., Bartke, I., et al. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.5.865 · Cited by 1,019
Foxp3 in control of the regulatory T cell lineage
Zheng, Y., & Rudensky, A. Y. (2007) · Nature Immunology · doi:10.1038/ni1455 · Cited by 707
Shifren, J. L., Tseng, J. F., Zaloudek, C. J., Ryan, I., Meng, Y. G., Ferrara, N., Jaffe, R. B., & Taylor, R. N. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.8.8768883 · Cited by 656
Vascular endothelial growth factor (VEGF) in endometriosis
Donnez, J., Smoes, P., Gillerot, S., Casanas-Roux, F., & Nisolle, M. (1998) · Human Reproduction · doi:10.1093/humrep/13.6.1686 · Cited by 531
Fehervari, Z. T., & Sakaguchi, S. (2004) · Journal of Clinical Investigation · doi:10.1172/jci23395 · Cited by 451
Arruvito, L., Sanz, M., Banham, A. H., & Fainboim, L. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.4.2572 · Cited by 444
Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis
Gazvani, R., & Templeton, A. (2002) · Reproduction · doi:10.1530/rep.0.1230217 · Cited by 393
Jasper, M. J. (2006) · Molecular Human Reproduction · doi:10.1093/molehr/gal032 · Cited by 319
Anaf, V., Simon, P., El Nakadi, I., Fayt, I., Simonart, T., Buxant, F., & Noel, J.-C. (2002) · Human Reproduction · doi:10.1093/humrep/17.7.1895 · Cited by 317
Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease?
Matarese, G., De Placido, G., Nikas, Y., & Alviggi, C. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00051-0 · Cited by 315
Zeitoun, K., Takayama, K., Sasano, H., Suzuki, T., Moghrabi, N., Andersson, S., Johns, A., Meng, L., Putman, M., Carr, B., et al. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.12.5301 · Cited by 308
Angiogenic Factors in Endometriosis
Taylor, R. N., Lebovic, D. I., & Mueller, M. D. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02769.x · Cited by 304
Nerve fibres in peritoneal endometriosis
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/del260 · Cited by 299
Self-citationEndometrial leukocytes and menstruation
Salamonsen, L. A. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.16 · Cited by 295
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/dei368 · Cited by 236
Self-citationLi, B., Lalani, A. S., Harding, T. C., Luan, B., Koprivnikar, K. E., Tu, G. H., Prell, R. A., VanRoey, M. J., Simmons, A. D., & Jooss, K. U. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1558 · Cited by 233
Dmowski, W. P., & Braun, D. P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.02.001 · Cited by 225
The origin of FOXP3-expressing CD4+ regulatory T cells: thymus or periphery
Sakaguchi, S. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20274 · Cited by 219
Macrophage expression in endometrium of women with and without endometriosis
Berbic, M., Schulke, L., Markham, R., Tokushige, N., Russell, P. J., & Fraser, I. S. (2008) · Human Reproduction · doi:10.1093/humrep/den393 · Cited by 204
Self-citationEndometrial Anomalies in Women with Endometriosis
Sharpe-Timms, K. L. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03797.x · Cited by 187
Neurotrophin Regulation of the Developing Nervous System: Analyses of Knockout Mice
Conover, J. C., & Yancopoulos, G. D. (1997) · Reviews in the Neurosciences · doi:10.1515/revneuro.1997.8.1.13 · Cited by 184
Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis
Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep071 · Cited by 176
Self-citationAngiongenesis: a new theory for endometriosis
Healy, D. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.736 · Cited by 173
Macrophages and nerve fibres in peritoneal endometriosis
Tran, L. V. P., Tokushige, N., Berbic, M., Markham, R., & Fraser, I. S. (2008) · Human Reproduction · doi:10.1093/humrep/den483 · Cited by 138
Self-citationGilabert–Estellés, J., Ramón, L., España, F., Gilabert, J., Vila, V., Regañón, E., Castelló, R., Chirivella, M., & Estellés, A. (2007) · Human Reproduction · doi:10.1093/humrep/dem149 · Cited by 126
Endometriosis: abnormal endometrium and dysfunctional immune response
Braun, D. P., & Dmowski, W. P. (1998) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199810000-00003 · Cited by 123
Chuang, P., Wu, M., Shoji, Y., & Tsai, S. (2009) · The Journal of Pathology · doi:10.1002/path.2588 · Cited by 117
Phenotypic and functional studies of leukocytes in human endometrium and endometriosis
Jones, R. K. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.702 · Cited by 115
Vascular endothelial growth factor A and C gene expression in endometriosis
Takehara, M., Ueda, M., Yamashita, Y., Terai, Y., Hung, Y., & Ueki, M. (2004) · Human Pathology · doi:10.1016/j.humpath.2004.07.020 · Cited by 110
Giatromanolaki, A. N., Bates, G. J., Koukourakis, M. I., Sivridis, E., Gatter, K. C., Harris, A. L., & Banham, A. H. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2008.04.021 · Cited by 108
Tan, X., Lang, J., Liu, D., Shen, K., Leng, J., & Zhu, L. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03187-4 · Cited by 100
Matalliotakis, I., Goumenou, A. G., Koumantakis, G. E., Neonaki, M., Koumantakis, E., Dionyssopoulou, E., Athanassakis, I., & Vassiliadis, S. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(02)00216-3 · Cited by 96
Thornton, A. M. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.048 · Cited by 91
Vigé, X., Costa, E., & Wise, B. C. (1991) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)12940-4 · Cited by 77
Endometriosis is sustained by tumour necrosis factor-α
Bullimore, D. W. (2002) · Medical Hypotheses · doi:10.1016/s0306-9877(02)00336-5 · Cited by 63
Endometrial antigens involved in the autoimmunity of endometriosis
MATHUR, S. P., Chihal, H. J., Homm, R. J., Garza, D. E., Rust, P. F., & Williamson, H. O. (1988) · Fertility and Sterility · doi:10.1016/s0015-0282(16)60362-x · Cited by 62
Nerve Fibers and Histopathology of Endometriosis-Harboring Peritoneum
Tulandi, T., Felemban, A., & Fong Chen, M. (2001) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60556-7 · Cited by 60
Bulmer, J. N., Jones, R. K., & Searle, R. F. (1998) · Human Reproduction · doi:10.1093/humrep/13.10.2910 · Cited by 58
T regulatory cells: an overview and intervention techniques to modulate allergy outcome
Nandakumar, S., Miller, C. W. T., & Kumaraguru, U. (2009) · Clinical and Molecular Allergy · doi:10.1186/1476-7961-7-5 · Cited by 51
Venezie, R. D., Toews, A. D., & Morell, P. (1995) · Journal of Neuroscience Research · doi:10.1002/jnr.490400111 · Cited by 48
Novel finding of high density of activated mast cells in endometrial polyps
Al‐Jefout, M., Black, K. I., Schulke, L., Berbic, M., Luscombe, G. M., Tokushige, N., Manconi, F., Markham, R., & Fraser, I. S. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.02.016 · Cited by 46
Self-citationImmune Response and Neurotrophic Factor Interactions in Peripheral Nerve Transplants
Gulati, A. K. (1998) · Acta Haematologica · doi:10.1159/000040832 · Cited by 35
Kennedy, S., Sargent, I. L., Starkey, P. M., Hicks, B. R., & Barlow, D. H. (1990) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1990.tb16236.x · Cited by 33
Lebovic, D. I., Chao, V. A., & Taylor, R. N. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031010 · Cited by 32
Mitsuma, N., Yamamoto, M., Iijima, M., Hattori, N., Ito, Y., Tanaka, F., & Sobue, G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.083 · Cited by 12
Ganewatta, S. P., Berbic, M., Luscombe, G. M., Markham, R., & Fraser, I. S. (2010) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/228402651000200403 · Cited by 11
Self-citationGanewatta, S. P., Berbic, M., Luscombe, G. M., et al. (2010) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.2010.6205 · Cited by 6
Self-citationFoxP3: a life beyond regulatory T cells.
Liu, Y., & Zheng, P. (2009) · PubMed Central · Cited by 4
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The Role of the Immune System in the Development of Endometriosis
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Metadata
- Authors
- Berbic, M., & Fraser, I. S.
- Affiliations
- The University of Sydney (AU)
- Corresponding author
- Fraser, I.S.
- Venue
- Journal of Reproductive Immunology
- Publisher
- Elsevier BV
- Published
- 2011-03
- Volume
- 88
- Issue
- 2
- Pages
- 149-155
- ISSN
- 0165-0378 (ISSN-L)
- OpenAlex
- W2048798995
- Cited by
- 135
- References
- 52
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 6 · 2023: 7 · 2022: 7 · 2021: 11 · 2020: 12 · 2019: 4 · 2018: 9 · 2017: 7 · 2016: 8 · 2015: 14 · 2014: 14 · 2013: 15 · 2012: 8
- FWCI
- 15.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Reproductive Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Obstetrics and Gynecology › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, regulatory T cells, Foxp3, leukocyte recruitment, endometrial immune response, mast cells, dendritic cells, macrophages, B cells, peritoneal fluid, luteal phase, ectopic endometrium, pathogenesis
- MeSH terms
- Animals, Choristoma, Endometriosis, Endometrium, Female, Humans, Inflammation, Pregnancy, Pregnancy, Ectopic, Uterus, T-Lymphocytes, Regulatory, Forkhead Transcription Factors
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