The DOI matches its Crossref record; 62 of the 63 references it cites were found in a registry or an index.
Reduced progesterone action during endometrial maturation: A potential risk factor for the development of endometriosis
Open accessAbstract
Objective To discuss the role that reduced endometrial responsiveness to progesterone (P) might play in the pathophysiology of endometriosis. Design A review of experimental evidence regarding the failure of P to regulate the expression of matrix metalloproteinases (MMPs) in the endometrium of patients with endometriosis. Conclusion(s) Progesterone and locally produced differentiation factors act cooperatively to reduce MMP expression by maternal endometrial cells within the pro-inflammatory micro-environment of early pregnancy. Our in vitro studies with normal human endometrium demonstrate that prior P exposure not only down-regulates MMP expression, but also limits the ability of locally produced proinflammatory cytokines to stimulate expression of these enzymes. In contrast, endometrial tissues from women with endometriosis demonstrate an altered response to P, allowing a continuous expression of MMPs throughout the secretory phase. Although the factors that influence the loss of P sensitivity in the endometrium of patients with endometriosis have not yet been defined, alterations in cell-cell communication seem to contribute to dysregulated MMP expression. Specifically, proinflammatory cytokines produced by epithelial cells oppose stromal cell responses to P, inhibiting production of key differentiation factors necessary for cell-specific MMP regulation. The resulting loss in normal MMP regulation enhances the invasive capacity of endometrial tissue, promoting ectopic establishment in an experimental model.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“A reduction in progesterone action in endometrium, 'progesterone resistance', of women with endometriosis (Osteen et al., 2005; Table V) may play a key role in development of endometriosis and possibly with associated pain; use of progestagens may reverse these effects.”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Osteen et al., 2005
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Osteen et al. (2005) demonstrated that eutopic endometrium of women with endometriosis has reduced progesterone action during maturation or 'progesterone resistance', that, in turn, may enhance development of endometriosis.”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Osteen et al., 2005
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334
TISSUE CHANGES FOLLOWING DEPRIVATION OF FAT-SOLUBLE A VITAMIN
Wolbach, S., & Howe, P. R. (1925) · Journal of Experimental Medicine · doi:10.1084/jem.42.6.753 · Cited by 1,674
Global gene profiling in human endometrium during the window of implantation
Kao, L. C., Tulac, S., Lobo, S., Imani, B., Yang, J. P., Germeyer, A., Osteen, K., Taylor, R. N., Lessey, B. A., & Giudice, L. C. (2002) · Endocrinology · doi:10.1210/endo.143.6.8885 · Cited by 727
Self-citationKao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696
Self-citationCurry, T. E., & Osteen, K. G. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0005 · Cited by 606
Self-citationGiguère, V. (1994) · Endocrine Reviews · doi:10.1210/edrv-15-1-61 · Cited by 522
Vitamin A and reproduction in rats
Thompson, J. N., Howell, J., & Pitt, G. A. (1964) · Proceedings of the Royal Society of London. Series B. Biological Sciences · doi:10.1098/rspb.1964.0017 · Cited by 381
Rodgers, W. H., Matrisian, L. M., Giudice, L. C., Dsupin, B. A., Cannon, P., Svitek, C., Gorstein, F., & Osteen, K. G. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117461 · Cited by 377
Self-citationThe Relation of Endometriosis to Menstrual Characteristics, Smoking, and Exercise
Cramer, D. W. (1986) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1986.03370140102032 · Cited by 367
Bruner‐Tran, K. L., Matrisian, L. M., Rodgers, W. H., Gorstein, F., & Osteen, K. G. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119478 · Cited by 283
Self-citationRedwine, D. B. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54591-9 · Cited by 259
Sutton, C. J. G., Pooley, A. S., Ewen, S. P., & Haines, P. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00403-2 · Cited by 247
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
Self-citationIncidence of symptom recurrence after hysterectomy for endometriosis
Namnoum, A. B., Hickman, T. N., Goodman, S. B., Gehlbach, D. L., & Rock, J. A. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57899-6 · Cited by 239
Bruner‐Tran, K. L., Rodgers, W. H., Gold, L. I., Korc, M., Hargrove, J. T., Matrisian, L. M., & Osteen, K. G. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.16.7362 · Cited by 222
Self-citationRodgers, W. H., steen, K. G., Matrisian, L. M., Navre, M., Giudice, L. C., & Gorstein, F. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(12)90922-9 · Cited by 217
The endocrinology of menstruation – a role for the immune system
Critchley, H. O. D., Kelly, R. W., Brenner, R. M., & Baird, D. T. (2001) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2001.01432.x · Cited by 203
Progesterone Receptor Isoform A But Not B Is Expressed in Endometriosis1
Attia, G. R., Zeitoun, K., Edwards, D., Johns, A., Carr, B. R., & Bulun, S. E. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.8.6739 · Cited by 193
Bergqvist, A., Bruse, C., Carlberg, M., & Carlström, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01752-0 · Cited by 190
Bruner‐Tran, K. L., Eisenberg, E., Yeaman, G. R., Anderson, T. A., McBean, J. H., & Osteen, K. G. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020418 · Cited by 187
Self-citationOsteen, K. G., Rodgers, W. H., Gaire, M., Hargrove, J. T., Gorstein, F., & Matrisian, L. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.21.10129 · Cited by 185
Self-citationLeukocyte networks and human endometrial remodelling
Salamonsen, L. A., Zhang, J., & Brasted, M. (2002) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(02)00011-6 · Cited by 181
Igarashi, T. M., Bruner-Tran, K. L., Yeaman, G. R., Lessey, B. A., Edwards, D. P., Eisenberg, E., & Osteen, K. G. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.01.113 · Cited by 163
Self-citationEarly endometriosis invades the extracellular matrix
Spuijbroek, M. D. E. H., Dunselman, G. A. J., Menheere, P. P. C. A., & Evers, J. L. H. (1993) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(93)90482-c · Cited by 151
Experimental endometriosis in the human
Ridley, J. H., & Edwards, I. K. (1958) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(58)90011-5 · Cited by 139
Early endometriosis invades the extracellular matrix
Spuijbroek, M. D. E. H., Dunselman, G. A. J., Menheere, P. P. C. A., & Evers, J. L. H. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55437-5 · Cited by 131
Recurrent endometriosis: Incidence, management, and prognosis
Wheeler, J. M., & Malinak, L. R. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90744-5 · Cited by 130
Giguere, V. (1994) · Endocrine Reviews · doi:10.1210/er.15.1.61 · Cited by 120
Steroid and Growth Factor Regulation of Matrix Metalloproteinase Expression and Endometriosis
Osteen, K. G., Bruner‐Tran, K. L., & Sharpe-Timms, K. L. (1996) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016334 · Cited by 119
Self-citationParacrine Regulation of Matrix Metalloproteinase Expression in the Normal Human Endometrium
Osteen, K. G., Keller, N. R., Feltus, F. A., & Melner, M. H. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052863 · Cited by 108
Self-citationBruner‐Tran, K. L., Eisenberg, E., Gorstein, F., & Osteen, K. G. (1999) · Steroids · doi:10.1016/s0039-128x(99)00048-3 · Cited by 104
Self-citationKothapalli, R., Buyuksal, I., Wu, S., Chegini, N., & TABIBZADEH, S. S. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119415 · Cited by 99
Endometriosis: The Ultimate Hormonal Disease
(2003) · Seminars in Reproductive Medicine · doi:10.1055/s-2003-41319 · Cited by 94
Regulation and Function of LEFTY-A/EBAF in the Human Endometrium
Cornet, P. B., Picquet, C., Lemoine, P., Osteen, K. G., Bruner‐Tran, K. L., TABIBZADEH, S. S., Courtoy, P. J., Eeckhout, Y., Marbaix, É., & Henriet, P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201793200 · Cited by 86
Self-citationNew medical treatments for endometriosis
Olive, D. L., Lindheim, S. R., & Pritts, E. A. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.03.005 · Cited by 86
Injectable depot medroxyprogesterone acetate contraception: an update for U.S. clinicians.
Kaunitz, A. M. (1998) · PubMed · Cited by 74
Bruner‐Tran, K. L., Webster-Clair, D. C., & Osteen, K. G. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02793.x · Cited by 73
Self-citationKeller, N. R., Sierra‐Rivera, E., Eisenberg, E., & Osteen, K. G. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.4.6502 · Cited by 70
Self-citationSTUDIES ON UROBILIN PHYSIOLOGY AND PATHOLOGY
McMaster, P. D., & Elman, R. (1926) · The Journal of Experimental Medicine · doi:10.1084/jem.43.6.753 · Cited by 69
The Potential Role of Environmental Toxins in the Pathophysiology of Endometriosis
Bruner‐Tran, K. L., Rier, S. E., Eisenberg, E., & Osteen, K. G. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052868 · Cited by 66
Self-citationTABIBZADEH, S. S., Mason, J. M., Shea, W., Cai, Y., Murray, M. J., & Lessey, B. A. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.7.6674 · Cited by 63
Sharpe-Timms, K. L., Zimmer, R. L., Griffin, W. T., & Penney, L. L. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56285-2 · Cited by 59
Paracrine Mediators of Endometrial Matrix Metalloproteinase Expression
Osteen, K. G., Bruner‐Tran, K. L., Ong, D. E., & Eisenberg, E. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02774.x · Cited by 58
Self-citationZheng, W. L., Sierra‐Rivera, E., Luan, J., Osteen, K. G., & Ong, D. E. (2000) · Endocrinology · doi:10.1210/endo.141.2.7323 · Cited by 58
Self-citationReproductive Medicine and Surgery
Wallach, E. E., & Zacur, H. A. (1995) · Medical Entomology and Zoology · Cited by 53
TABIBZADEH, S. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.7.2526 · Cited by 53
Timing of Estrogen Replacement Therapy Following Hysterectomy With Oophorectomy for Endometriosis
Hickman, T. N., Namnoum, A. B., Hinton, E. L., Zacur, H. A., & Rock, J. A. (1998) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(98)00071-4 · Cited by 48
Osteen, K. G. (2003) · Frontiers in bioscience · doi:10.2741/938 · Cited by 47
Self-citationImmune Aspects of Endometriosis: Relevance of the Uterine Mucosal Immune System
Rier, S. E., & Yeaman, G. R. (1997) · Seminars in Reproductive Medicine · doi:10.1055/s-2008-1068750 · Cited by 47
Osteen, K. G., Bruner‐Tran, K. L., Keller, N. R., & Eisenberg, E. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02764.x · Cited by 44
Self-citationD’Hooghe, T. M. (2003) · PubMed · doi:10.1097/01.gco.0000072859.73466.e3 · Cited by 40
D’Hooghe, T. M. (2003) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200306000-00006 · Cited by 40
METZGER, D. A., Lessey, B. A., Soper, J. T., McCarty, K. S., & Haney, A. F. (1991) · PubMed · Cited by 38
Loughney, A. D., Kumarendran, M. K., Thomas, E. J., & Redfern, C. P. F. (1995) · Molecular Human Reproduction · doi:10.1093/molehr/1.3.133 · Cited by 30
Reproductive Medicine and Surgery
Thompson, I. E. (1995) · JAMA · doi:10.1001/jama.1995.03530210079040 · Cited by 29
Siddiqui, N. A., Loughney, A. D., Thomas, E. J., Dunlop, W., & Redfern, C. P. F. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138720 · Cited by 27
Loughney, A. D., Kumarendran, M. K., Thomas, E. J., & Redfern, C. P. F. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136137 · Cited by 26
Sachdeva, G., Patil, V., Katkam, R. R., Manjramkar, D. D., Kholkute, S. D., & Puri, C. P. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.1.1 · Cited by 24
Stromal-epithelial cell communication, growth factors, and tissue regulation.
Anderson, T. L., Gorstein, F., & Osteen, K. G. (1990) · PubMed · Cited by 21
Self-citationInterleukin‐1α Opposes Progesterone‐mediated Suppression of MMP‐7
Osteen, K. G., Sierra‐Rivera, E., Keller, N. R., & Fox, D. B. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48532.x · Cited by 20
Self-citationIn Vitro Regulation of Stromelysin‐1 in Human Endometrial Stromal Cells
Schatz, F., Papp, C., Tóth‐Pál, E., Aigner, S., HAUSKNECHT, V., Krikun, G., Gordon, R. E., Berkowitz, R. L., & Lockwood, C. J. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb24791.x · Cited by 2
EBAF/Lefty-1 antagonizes progesterone action in human endometrium and in experimental endometriosis
Bruner‐Tran, K. L., TABIBZADEH, S. S., Cornet, P. B., Henriet, P., Eisenberg, E., & Osteen, K. G. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)01894-6 · Cited by 1
Self-citation
Research works printed but not linked: 1
- Attia, 2000, Progesterone receptor isoform A but not B is expressed in endometriosis, J Clin Endocrinol Metab, 85, 2897
Cited by
Sorted by citations
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772
Bulun, S. E., Yilmaz, B. D., Sison, C., Miyazaki, K., Bernardi, L., Liu, S., Kohlmeier, A., Yin, P., Milad, M., & Wei, J. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00242 · Cited by 844
Burney, R. O., Talbi, S., Hamilton, A. E., Vo, K. C., Nyegaard, M., Nezhat, C. R., Lessey, B. A., & Giudice, L. C. (2007) · Endocrinology · doi:10.1210/en.2006-1692 · Cited by 735
Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer
Kim, J. J., Kurita, T., & Bulun, S. E. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1043 · Cited by 520
The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights
Laganà, A. S., Garzon, S., Götte, M., Viganò, P., Franchi, M. P., Ghezzi, F., & Martin, D. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225615 · Cited by 503
Metadata
- Authors
- Osteen, K. G., Bruner-Tran, K. L., & Eisenberg, E.
- Affiliations
- Vanderbilt University (US)
- Corresponding author
- Osteen, Kevin G.
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 2005-03
- Volume
- 83
- Issue
- 3
- Pages
- 529-537
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W1966049599
- Cited by
- 122
- References
- 63
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 2 · 2022: 7 · 2021: 8 · 2020: 2 · 2019: 6 · 2018: 3 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 5 · 2013: 4 · 2012: 11
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Environmental Health Sciences (R21ES12298-01, R21ES012298)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (5K12HD43483, U54HD037321, U54 HD37321, K12HD043483)
- 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, progesterone, endometrial maturation, matrix metalloproteinases, endometrial receptivity, inflammatory cytokines, endometrial invasion, luteal phase, intercellular communication, ectopic endometrium
- MeSH terms
- Endometriosis, Endometrium, Female, Humans, Pregnancy, Progesterone, Risk Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
