Endometrial Stromal Cells and Immune Cell Populations Within Lymph Nodes in a Nonhuman Primate Model of Endometriosis
Open accessAbstract
Mounting evidence suggests that immunological responses may be altered in endometriosis. The baboon (Papio anubis) is generally considered the best model of endometriosis pathogenesis. The objective of the current study was to investigate for the first time immunological changes within uterine and peritoneal draining lymph nodes in a nonhuman primate baboon model of endometriosis. Paraffin-embedded femoral lymph nodes were obtained from 22 normally cycling female baboons (induced endometriosis n = 11; control n = 11). Immunohistochemical staining was performed with antibodies for endometrial stromal cells, T cells, immature and mature dendritic cells, and B cells. Lymph nodes were evaluated using an automated cellular imaging system. Endometrial stromal cells were significantly increased in lymph nodes from animals with induced endometriosis, compared to control animals (P = .033). In animals with induced endometriosis, some lymph node immune cell populations including T cells, dendritic cells and B cells were increased, suggesting an efficient early response or peritoneal drainage.
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Significantly increased presence of endometrial cells and altered immune environment has been demonstrated in uterine-draining lymph nodes in the baboon model of induced endometriosis.
“Significantly increased presence of endometrial cells and altered immune environment has also been demonstrated in uterine-draining lymph nodes in the baboon model of induced endometriosis.99”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [99]
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Cites
Eskenazi, B., & Warner, M. L. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70302-8 · Cited by 1,617 · see citing works
(1927) · PubMed Central · Cited by 1,008 · see citing works
Ballard, K., Lowton, K., & Wright, J. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.04.054 · Cited by 628 · see citing works
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 · see citing works
Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK
Hadfield, R., Mardon, H., Barlow, D., & Kennedy, S. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019270 · Cited by 517 · see citing works
Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00405-x · Cited by 299 · see citing works
Antiangiogenic Agents Are Effective Inhibitors of Endometriosis
Hull, M. L., Jones, D. S., Chan, C. L. K., Bruner‐Tran, K. L., Osteen, K. G., Tom, B. D. M., Fan, T. D., & Smith, S. K. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021912 · Cited by 243 · see citing works
Gouill, S. L., Talmant, P., Touzeau, C., Moreau, A., Garand, R., Juge‐Morineau, N., Gaillard, F., Gastinne, T., Milpied, N. J., Moreau, P., et al. (2007) · Haematologica · doi:10.3324/haematol.11305 · Cited by 211 · see citing works
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 · see citing works
Self-citationDendritic 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 · see citing works
Self-citationINTESTINAL ADENOMAS OF ENDOMETRIAL TYPE
SAMPSON, J. A. (1922) · Archives of Surgery · doi:10.1001/archsurg.1922.01110140003001 · Cited by 165 · see citing works
Berbic, M., Hey‐Cunningham, A. J., Ng, C. H. M., Tokushige, N., Ganewatta, S. P., Markham, R., Russell, P. J., & Fraser, I. S. (2010) · Human Reproduction · doi:10.1093/humrep/deq020 · Cited by 158 · see citing works
Self-citationJavert, C. T. (1949) · Cancer · doi:10.1002/1097-0142(194905)2:3 · Cited by 150 · see citing works
Localization of laminin, fibronectin, E-cadherin, and integrins in endometrium and endometriosis
Béliard, A., Donnez, J., Nisolle, M., & Foidart, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81909-7 · Cited by 141 · see citing works
A Modified Baboon Model for Endometriosis
Fazleabas, A. T., Brudney, A., Gürateş, B., Chai, D. C., & Bulun, S. E. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02791.x · Cited by 120 · see citing works
Self-citationIs endometriosis an endometrial disease?
Vinatier, D., Cosson, M., & Dufour, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00263-8 · Cited by 115 · see citing works
Deeply infiltrating endometriosis affecting the rectum and lymph nodes
Abrão, M. S., Podgaec, S., Dias, J., Averbach, M., Garry, R., da Silva, L. F. F., & Carvalho, F. M. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.02.102 · Cited by 107 · see citing works
A baboon model for endometriosis: implications for fertility
Hastings, J. M., & Fazleabas, A. T. (2006) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-4-s1-s7 · Cited by 89 · see citing works
Self-citationLymph node involvement and lymphovascular invasion in deep infiltrating rectosigmoid endometriosis
Noël, J., Chapron, C., Fayt, I., & Anaf, V. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.05.011 · Cited by 81 · see citing works
Gashaw, I., Hastings, J. M., Jackson, K. S., Winterhager, E., & Fazleabas, A. T. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.105.049320 · Cited by 81 · see citing works
Self-citationAkoum, A., Metz, C. N., Al-Akoum, M., & Kats, R. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.10.073 · Cited by 78 · see citing works
Mechsner, S., Weichbrodt, M., Riedlinger, W. F. J., Bartley, J., Kaufmann, A. M., Schneider, A., & Kohler, C. (2008) · Human Reproduction · doi:10.1093/humrep/den259 · Cited by 69 · see citing works
Tawfik, O. W., Kimler, B. F., Davis, M., Donahue, J. K., Persons, D. L., Fan, F., Hagemeister, S., THOMAS, P. A., Connor, C. S., Jewell, W. R., et al. (2005) · Histopathology · doi:10.1111/j.1365-2559.2005.02322.x · Cited by 68 · see citing works
Structural and Functional Anatomy of the Abdominal Wall
Grevious, M. A., Cohen, M., Shah, S. R., & Rodriguez, P. S. (2006) · Clinics in Plastic Surgery · doi:10.1016/j.cps.2005.12.005 · Cited by 67 · see citing works
D’Hooghe, T. M., Bambra, C. S., Xiao, L., Peixe, K., & Hill, J. A. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.111715 · Cited by 59 · see citing works
Bulmer, J. N., Jones, R. K., & Searle, R. F. (1998) · Human Reproduction · doi:10.1093/humrep/13.10.2910 · Cited by 58 · see citing works
Ota, H., IGARASHI, S., & Tanaka, T. (1996) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1996.tb00128.x · Cited by 56 · see citing works
The Estrogen Early Response Gene FOS Is Altered in a Baboon Model of Endometriosis1
Hastings, J. M., Jackson, K. S., Mavrogianis, P. A., & Fazleabas, A. T. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.106.052852 · Cited by 55 · see citing works
Self-citatiońHooghe, T. D., Hill, J. A., Oosterlynck, D. J., Koninckx, P. R., & Bambra, C. S. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019478 · Cited by 47 · see citing works
Descazeaud, A., TAILLE, A. D. L., Allory, Y., Faucon, H., Salomon, L., Bismar, T. A., Kim, R., Hofer, M. D., Chopin, D. K., Abbou, C. C., et al. (2006) · The Prostate · doi:10.1002/pros.20405 · Cited by 46 · see citing works
Pelvic inflammation induced by diagnostic laparoscopy in baboons
D’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., & Hill, J. A. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00406-9 · Cited by 27 · see citing works
Ellis, H. (2011) · Anaesthesia & intensive care medicine · doi:10.1016/j.mpaic.2010.11.005 · Cited by 25 · see citing works
Becker, S., Becker‐Pergola, G., Fehm, T. N., Emig, R., Wallwiener, D. R., & Solomayer, E. (2005) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.20064 · Cited by 16 · see citing works
Microanatomy and function of the eutopic endometrium in women with endometriosis
Al‐Jefout, M., Tokushige, N., Hey‐Cunningham, A. J., Manconi, F., Ng, C. H. M., Schulke, L., Berbic, M., Markham, R., & Is, F. (2008) · Expert Review of Obstetrics & Gynecology · doi:10.1586/17474108.4.1.61 · Cited by 15 · see citing works
Self-citationMcKay, J. S., Bigley, A. L., Bell, A. R., Jenkins, R. P., Somers, R., Brocklehurst, S. R., White, A. M., & Goodwin, L. (2005) · Experimental and Toxicologic Pathology · doi:10.1016/j.etp.2005.09.002 · Cited by 12 · see citing works
Pleuroperitoneal endometriosis.
Irani, S., ATKINSON, L., Cabaniss, C., & Danovitch, S. H. (1976) · PubMed · Cited by 9 · see citing works
Rösner, N., & Böger, A. (1979) · European Urology · doi:10.1159/000473137 · Cited by 7 · see citing works
[Isolated inguinal endometriosis. Report of a clinical case].
Mascaretti, G., Patacchiola, F., Berardino, C. D., & Moscarini, M. (2000) · PubMed · Cited by 3 · see citing works
Ellis, H. (2008) · Anaesthesia & intensive care medicine · doi:10.1016/j.mpaic.2008.01.010 · Cited by 2 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Halban J. Hysteroadenosis metastatica. Wien klin Woschensch. 1924;37:1205-1206.
- Javert CT. Pathogenesis of endometriosis based on endometrial homeoplasia, direct extension, exfoliation and implantation, lymphatic and hematogenous metastasis. Cancer. 1949;2(3): 399-410.
- Mascaretti G, Patacchiola F, Di Berardino C, Moscarini M. Isolated inguinal endometriosis. A clinical case. Minerva Ginecol. 2000;52(6):249-252.
Cited by
Sorted by citations
Pathogenesis and pathophysiology of endometriosis
Burney, R. O., & Giudice, L. C. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.029 · Cited by 1,590 · see citing works
Rogers, P. A. W., D’Hooghe, T. M., Fazleabas, A., Giudice, L. C., Montgomery, G. W., Petraglia, F., & Taylor, R. N. (2013) · Reproductive Sciences · doi:10.1177/1933719113477495 · Cited by 154 · see citing works
Self-citationThe Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1
Jerman, L. F., & Hey-Cunningham, A. J. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.124313 · Cited by 122 · see citing works
Self-citationImmunological Basis of the Endometriosis: The Complement System as a Potential Therapeutic Target
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 121 · see citing works
Li, W.-N., Hsiao, K., Wang, C.-A., Chang, N., Hsu, P.-L., Sun, C.-H., Wu, S.-R., Wu, M., & Tsai, S. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1920037117 · Cited by 96 · see citing works
Occult microscopic endometriosis: undetectable by laparoscopy in normal peritoneum
Khan, K. N., Fujishita, A., Kitajima, M., Hiraki, K., Nakashima, M., & Masuzaki, H. (2014) · Human Reproduction · doi:10.1093/humrep/det438 · Cited by 72 · see citing works
The known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59 · see citing works
Self-citationBraundmeier, A. G., Jackson, K. S., Hastings, J. M., Koehler, J., Nowak, R. A., & Fazleabas, A. T. (2012) · Human Reproduction · doi:10.1093/humrep/des083 · Cited by 58 · see citing works
Self-citationZhou, C., Zhang, T., Liu, F., Zhou, J., Ni, X., Huo, R., & Shi, Z. (2015) · Molecular BioSystems · doi:10.1039/c5mb00733j · Cited by 37 · see citing works
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 · see citing works
Reproductive Microbiomes: Using the Microbiome as a Novel Diagnostic Tool for Endometriosis
Cregger, M. A., Lenz, K., Leary, E., Leach, R. E., Fazleabas, A. T., White, B. A., & Braundmeier, A. G. (2017) · Reproductive Immunology Open Access · doi:10.21767/2476-1974.100036 · Cited by 32 · see citing works
Self-citationLi, L., Liao, Z., Ye, M., & Jiang, J. (2021) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-021-00811-3 · Cited by 27 · see citing works
Endometriosis: A Role for Stem Cells
Dhesi, A. S., & Morelli, S. S. (2015) · Women s Health · doi:10.2217/whe.14.57 · Cited by 25 · see citing works
Hey‐Cunningham, A. J., Markham, R., Fraser, I. S., & Berbic, M. (2013) · Reproductive Sciences · doi:10.1177/1933719113485299 · Cited by 22 · see citing works
Self-citationFazleabas, A. T., Braundmeier, A. G., & Parkin, K. (2015) · Contraception · doi:10.1016/j.contraception.2015.06.006 · Cited by 19 · see citing works
Self-citationClinical management of endometriosis
Russo, M. L., Chalif, J., & Falcone, T. (2020) · Minerva Obstetrics and Gynecology · doi:10.23736/s0026-4784.20.04544-x · Cited by 18 · see citing works
Characteristics of histologically confirmed endometriosis in cynomolgus monkeys
Nishimoto-Kakiuchi, A., Netsu, S., Matsuo, S., Hayashi, S., Ito, T., Okabayashi, S., Yasmin, L., Yuzawa, K., Kondoh, O., Kato, A., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dew209 · Cited by 13 · see citing works
Do, H., Díaz‐Sylvester, P., Groesch, K. A., Wilson, T., Delfino, K. R., de Mola, J. R. L., & Braundmeier‐Fleming, A. (2024) · Archives of Medical Research · doi:10.1016/j.arcmed.2024.103112 · Cited by 9 · see citing works
Marcellin, L., Morin, C., Santulli, P., Marzouk, P., Bourret, A., Dousset, B. E., Borghese, B., & Chapron, C. (2016) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2016.08.817 · Cited by 8 · see citing works
Modèles animaux dans la recherche expérimentale sur l’endométriose
Colette, S., & Donnez, J. (2012) · Gynécologie Obstétrique & Fertilité · doi:10.1016/j.gyobfe.2012.07.009 · Cited by 8 · see citing works
Lymphatic Vessels in Peritoneal Endometriotic Lesions
Hey-Cunningham, A. J., Berbic, M., Ng, C. H. M., Markham, R., & Fraser, I. S. (2011) · Journal of Endometriosis · doi:10.5301/je.2011.8522 · Cited by 7 · see citing works
Self-citationAnimal Models in Endometriosis Research
Asally, R., Markham, R., & Manconi, F. (2015) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.5000228 · Cited by 4 · see citing works
Self-citationManconi, F., Fazleabas, A. T., Markham, R., & Fraser, I. S. (2018) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026518810594 · Cited by 5 · see citing works
Self-citationEndometriosis immune microenvironment timing shifts: from immune escape to immune exhaustion
Fan, W., Zhai, F., & Ruihua, Z. (2026) · Cell Death Discovery · doi:10.1038/s41420-026-02965-8 · Cited by 3 · see citing works
The role of stem cells in the pathogenesis of endometriosis (а review)
Farkhat, K. N., Савилова, А. М., Makiyan, Z., & Adamyan, L. V. (2016) · Russian Journal of Human Reproduction · doi:10.17116/repro201622120-27 · Cited by 2 · see citing works
Li, K., Wang, J., Liu, X., Dang, Y., Wang, K., Li, M., Zhang, X., & Liu, Y. (2025) · Scientific Reports · doi:10.1038/s41598-025-86164-y · Cited by 2 · see citing works
Nijkang, N. P., Anderson, L. A., Markham, R., Fraser, I. S., & Manconi, F. (2018) · SAGE Open Medicine · doi:10.1177/2050312118761287 · Cited by 1 · see citing works
Self-citationKansouh, A., Elbalshy, A. E. M., & Ghanem, S. (2019) · Journal of Medicine in Scientific Research · doi:10.4103/jmisr.jmisr_76_18 · Cited by 1 · see citing works
NEZHAT, C. R., Nezhat, F. R., NEZHAT, C. R., Lakhi, N., & Nezhat, A. A. (2025) · Cambridge University Press eBooks · doi:10.1017/9781108561440.013
Philip, C. (2020) · theses.fr (ABES) · doi:10.70675/17902a36zc903z4351zaebez36f9f6cfcbf8
- Authors
- Hey-Cunningham, A. J., Fazleabas, A. T., Braundmeier, A. G., Markham, R., Fraser, I. S., & Berbic, M.
- Affiliations
- Michigan State University (US)
- University of Illinois Urbana-Champaign (US)
- The University of Sydney (AU)
- Venue
- Reproductive Sciences
- Published
- 2011-08
- Volume
- 18
- Issue
- 8
- Pages
- 747-754
- ISSN
- 1933-7191 (ISSN-L)
- 1933-7205
- PMC
- PMC4051399
- OpenAlex
- W2121115944
- Cited by
- 30
- References
- 39
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2021: 3 · 2020: 3 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 3 · 2015: 5 · 2013: 3 · 2012: 3
- FWCI
- 2.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Reproductive Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Thyne Reid Foundation
- University of Sydney
- National Institutes of Health
- University of Illinois at Urbana-Champaign
- National Institute of Child Health and Human Development (U54 HD 40093)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD040093, U54-HD40093)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, endometrial stromal cells, lymph nodes, baboon model, nonhuman primate model, immune cell subsets, T cells, dendritic cells, B cells
- MeSH terms
- Animals, Disease Models, Animal, Endometriosis, Female, Immunohistochemistry, Lymph Nodes, Papio, Stromal Cells
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