Reduced progesterone action during endometrial maturation: A potential risk factor for the development of endometriosis
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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.
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Reduced progesterone action in endometrium, called progesterone resistance, in women with endometriosis may play a key role in development of endometriosis and possibly associated pain; progestagens may reverse these effects.
“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
The Abstract and Figure 2 describe reduced endometrial progesterone responsiveness in women with endometriosis and propose that it contributes to disease development. Clinical Considerations identifies progestins as treatments for endometriosis-associated pelvic pain, and the Abstract says progestin-based therapies can lead to disease regression in some women. The paper does not establish that progesterone resistance causes the pain or that progestagens reverse the resistance itself; it also notes that proposed progesterone supplementation for symptoms had not been tested in randomized trials. Our copy provides section labels but no page numbers for these passages. (LLM, conf=0.84)
Experimental — accuracy not yet measuredEutopic endometrium in women with endometriosis shows reduced progesterone action during maturation, called progesterone resistance, which may enhance endometriosis development.
“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
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Cites
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationCurry, T. E., & Osteen, K. G. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0005 · Cited by 606 · see citing works
Self-citationGiguère, V. (1994) · Endocrine Reviews · doi:10.1210/edrv-15-1-61 · Cited by 514 · see citing works
Progesterone Receptor Isoform A But Not B Is Expressed in Endometriosis
Attia, G. R. (2000) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.8.2897 · Cited by 488 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationRedwine, D. B. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54591-9 · Cited by 259 · see citing works
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 · 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
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 238 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Bergqvist, A., Bruse, C., Carlberg, M., & Carlström, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01752-0 · Cited by 190 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Giguere, V. (1994) · Endocrine Reviews · doi:10.1210/er.15.1.61 · Cited by 120 · see citing works
Steroid and Growth Factor Regulation of Matrix Metalloproteinase Expression and Endometriosis
Osteen, K. G., Bruner, K. L., & Sharpe-Timms, K. L. (1996) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016334 · Cited by 117 · see citing works
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 · see citing works
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 · see citing works
Self-citationKothapalli, R., Buyuksal, I., Wu, S., Chegini, N., & TABIBZADEH, S. S. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119415 · Cited by 99 · see citing works
Endometriosis: The Ultimate Hormonal Disease
(2003) · Seminars in Reproductive Medicine · doi:10.1055/s-2003-41319 · Cited by 94 · see citing works
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 · see citing works
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 · see citing works
Injectable depot medroxyprogesterone acetate contraception: an update for U.S. clinicians.
Kaunitz, A. M. (1998) · PubMed · Cited by 74 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationReproductive Medicine and Surgery
Wallach, E. E., & Zacur, H. A. (1995) · Medical Entomology and Zoology · Cited by 53 · see citing works
TABIBZADEH, S. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.7.2526 · Cited by 53 · see citing works
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 · see citing works
Osteen, K. G. (2003) · Frontiers in bioscience · doi:10.2741/938 · Cited by 47 · see citing works
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 · see citing works
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 · see citing works
Self-citationD’Hooghe, T. M. (2003) · PubMed · doi:10.1097/01.gco.0000072859.73466.e3 · Cited by 40 · see citing works
D’Hooghe, T. M. (2003) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200306000-00006 · Cited by 40 · see citing works
METZGER, D. A., Lessey, B. A., Soper, J. T., McCarty, K. S., & Haney, A. F. (1991) · PubMed · Cited by 38 · see citing works
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 · see citing works
Reproductive Medicine and Surgery
Thompson, I. E. (1995) · JAMA · doi:10.1001/jama.1995.03530210079040 · Cited by 29 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Stromal-epithelial cell communication, growth factors, and tissue regulation.
Anderson, T. L., Gorstein, F., & Osteen, K. G. (1990) · PubMed · Cited by 21 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Bruner-Tran KL, Webster-Clair D, Osteen KG. Experimental endome- triosis: the nude mouse as a xenographic host. Ann N Y Acad Sci 2002;955:328 -39.
Cited by
Sorted by citations
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 492 · see citing works
Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing
Crain, D. A., Janssen, S. J., Edwards, T. M., Heindel, J., Ho, S.-M., Hunt, P., Iguchi, T., Juul, A., McLachlan, J. A., Schwartz, J., et al. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.067 · Cited by 465 · see citing works
Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications
Stratton, P., & Berkley, K. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq050 · Cited by 442 · see citing works
Progesterone resistance in endometriosis: link to failure to metabolize estradiol.
Bulun, S. E., Cheng, Y.-H., Yin, P., Imir, G., Utsunomiya, H., Attar, E., Innes, J., & Julie Kim, J. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.11.041 · Cited by 397 · see citing works
Role of nuclear progesterone receptor isoforms in uterine pathophysiology
Patel, B., Elguero, S., Thakore, S., Dahoud, W., Bedaiwy, M., & Mesiano, S. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmu056 · Cited by 353 · see citing works
Endometriosis-associated infertility: From pathophysiology to tailored treatment
Bonavina, G., & Taylor, H. S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1020827 · Cited by 359 · see citing works
Role of Estrogen Receptor-β in Endometriosis
Bulun, S., Monsavais, D., Pavone, M., Dyson, M., Xue, Q., Attar, E., Tokunaga, H., & Su, E. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1299596 · Cited by 307 · see citing works
“17,19 This abnormal pattern of gene expression could also be traced to primary stromal cells isolated from endometriotic tissue, eutopic endometrium from endo-metriosis, and eutopic endometrium from disease-free women.”
BackgroundLessey, B. A., & Kim, J. J. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.05.031 · Cited by 286 · see citing works
Estrogen Receptor-β, Estrogen Receptor-α, and Progesterone Resistance in Endometriosis
Bulun, S., Cheng, Y.-H., Pavone, M., Xue, Q., Attar, E., Trukhacheva, E., Tokunaga, H., Utsunomiya, H., Yin, P., Luo, X., et al. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242991 · Cited by 243 · see citing works
Immune interactions in endometriosis
Herington, J. L., Bruner‐Tran, K. L., Lucas, J. A., & Osteen, K. G. (2011) · Expert Review of Clinical Immunology · doi:10.1586/eci.11.53 · Cited by 226 · see citing works
Self-citationThe Role of Endometrium in Endometriosis
Ulukuş, M., Çakmak, H., & Arici, A. M. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2006.07.005 · Cited by 171 · see citing works
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 · see citing works
Self-citationGuo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000096047 · Cited by 140 · see citing works
Neuroendocrine–immune disequilibrium and endometriosis: an interdisciplinary approach
Tariverdian, N., Theoharides, T. C., Siedentopf, F., Gutiérrez, G., Jeschke, U., Rabinovich, G. A., Blois, S. M., & Arck, P. C. (2007) · Seminars in Immunopathology · doi:10.1007/s00281-007-0077-0 · Cited by 120 · see citing works
Gut Microbiota Exceeds Cervical Microbiota for Early Diagnosis of Endometriosis
Huang, L., Liu, B., Liu, Z., Feng, W.-Q., Liu, M., Wang, Y., Peng, D., Fu, X., Zhu, H., Cui, Z., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.788836 · Cited by 117 · see citing works
Epidemiology of Endometriosis:
MCLEOD, B. S., & Retzloff, M. G. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7bde · Cited by 112 · see citing works
Hayashi, A., Tanabe, A., Kawabe, S., Hayashi, M., Yuguchi, H., Yamashita, Y., Okuda, K., & Ohmichi, M. (2012) · Journal of Ovarian Research · doi:10.1186/1757-2215-5-31 · Cited by 111 · see citing works
Pabona, J. M. P., Simmen, F. A., Nikiforov, M. A., Zhuang, D., Shankar, K., Velarde, M. C., Zelenko, Z., Giudice, L. C., & Simmen, R. C. M. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2562 · Cited by 110 · see citing works
Role of AMPK/mTOR, mitochondria, and ROS in the pathogenesis of endometriosis
Assaf, L., Eid, A. A., & Nassif, J. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120805 · Cited by 108 · see citing works
Banu, S. K., Lee, J., Starzinski‐Powitz, A., & Arosh, J. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.07.1358 · Cited by 96 · see citing works
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 · see citing works
Sofo, V., Götte, M., Laganà, A. S., Salmeri, F. M., Triolo, O., Sturlese, E., Retto, G., Alfa, M., Granese, R., & Abrão, M. S. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3739-5 · Cited by 88 · see citing works
Houshdaran, S., Oke, A., Fung, J. C., Vo, K. C., NEZHAT, C. R., & Giudice, L. C. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008601 · Cited by 87 · see citing works
Nayyar, T., Bruner‐Tran, K. L., Piestrzeniewicz‐Ulanska, D., & Osteen, K. G. (2006) · Reproductive Toxicology · doi:10.1016/j.reprotox.2006.09.007 · Cited by 82 · see citing works
Self-citationBruner‐Tran, K. L., Mokshagundam, S., Herington, J. L., Ding, T., & Osteen, K. G. (2018) · Current Women s Health Reviews · doi:10.2174/1573404813666170921162041 · Cited by 77 · see citing works
Self-citationJackson, K. S., Brudney, A., Hastings, J. M., Mavrogianis, P. A., Kim, J. J., & Fazleabas, A. T. (2007) · Reproductive Sciences · doi:10.1177/1933719106298409 · Cited by 77 · see citing works
Bedaiwy, M. A., Dahoud, W., Skomorovska-Prokvolit, Y., Yi, L., LIU, J. H., Falcone, T., Hurd, W. W., & Mesiano, S. A. (2015) · Reproductive Sciences · doi:10.1177/1933719115585145 · Cited by 74 · see citing works
Wu, Y., Starzinski‐Powitz, A., & Guo, S. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.008 · Cited by 73 · see citing works
Bianco, B. A. V., André, G. M., Vilariño, F. L., Peluso, C., Mafra, F., Christofolini, D. M., & Barbosa, C. P. (2011) · Human Immunology · doi:10.1016/j.humimm.2011.12.009 · Cited by 72 · see citing works
Bruner-Tran, K. L., Zhang, Z., Eisenberg, E., Winneker, R. C., & Osteen, K. G. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2024 · Cited by 65 · see citing works
Self-citationHeard, M. E., Simmons, C. D., Simmen, F. A., & Simmen, R. C. M. (2014) · Endocrinology · doi:10.1210/en.2013-1947 · Cited by 68 · see citing works
Dioxin may promote inflammation-related development of endometriosis
Bruner‐Tran, K. L., Yeaman, G. R., Crispens, M. A., Igarashi, T. M., & Osteen, K. G. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.02.102 · Cited by 66 · see citing works
Self-citationBruner‐Tran, K. L., Herington, J. L., Dulęba, A. J., Taylor, H. S., & Osteen, K. G. (2013) · PubMed · Cited by 61 · see citing works
Self-citationMatsuzaki, S., Canis, M. J., Pouly, J. L., Déchelotte, P. J., & Mage, G. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.08.017 · Cited by 61 · see citing works
Resuehr, D., Glore, D. R., Taylor, H. S., Bruner‐Tran, K. L., & Osteen, K. G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.009 · Cited by 58 · see citing works
Self-citationCheng, Y.-H., Imir, A. G., Fenkçi, V., Yılmaz, M. B., & Bulun, S. E. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2006.12.014 · Cited by 56 · see citing works
Rocha, C. V., Broi, M. G. D., Furtado, C. L. M., Navarro, P. A., Ferriani, R. A., & Meola, J. (2019) · Reproductive Sciences · doi:10.1177/1933719119828078 · Cited by 58 · see citing works
Bisphenol-A exposure alters endometrial progesterone receptor expression in the nonhuman primate
Aldad, T. S., Rahmani, N., Leranth, C., & Taylor, H. S. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.04.010 · Cited by 51 · see citing works
Ding, T., McConaha, M. E., Boyd, K. L., Osteen, K. G., & Bruner‐Tran, K. L. (2010) · Reproductive Toxicology · doi:10.1016/j.reprotox.2010.11.003 · Cited by 50 · see citing works
Self-citationInfluence of AKT on Progesterone Action in Endometrial Diseases
Lee, I. I., & Kim, J. J. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.119255 · Cited by 45 · see citing works
Pathogenesis of Endometriosis: Roles of Retinoids and Inflammatory Pathways
Kane, M. A., Sidell, N., & Taylor, R. N. (2015) · Seminars in Reproductive Medicine · doi:10.1055/s-0035-1554920 · Cited by 47 · see citing works
Du, Y., Gao, M., Shi, Y. X., Sun, Z., & Wang, J. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2567-0 · Cited by 44 · see citing works
MicroRNA expression pattern differs depending on endometriosis lesion type†
Haikalis, M. E., Wessels, J. M., Leyland, N. A., Agarwal, S. K., & Foster, W. G. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy019 · Cited by 41 · see citing works
Szukiewicz, D., Stangret, A., Ruiz‐Ruiz, C., Olivares, E. G., Şoriţău, O., Șușman, S., & Szewczyk, G. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-10115-5 · Cited by 41 · see citing works
Progesterone receptor profile in the decidua and fetal membrane
Goldman, S. (2006) · Frontiers in bioscience · doi:10.2741/2088 · Cited by 39 · see citing works
Calpain and the Glutamatergic Synapse
Doshi, S. (2009) · Frontiers in Bioscience-Elite · doi:10.2741/e38 · Cited by 38 · see citing works
Pazhohan, A., Amidi, F., Akbari-Asbagh, F., Seyedrezazadeh, E., Farzadi, L., Khodarahmin, M., Mehdinejadiani, S., & Sobhani, A. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2017.10.025 · Cited by 38 · see citing works
Herington, J. L., Crispens, M. A., Carvalho-Macedo, A. C., Camargos, A. F., Lebovic, D. I., Bruner‐Tran, K. L., & Osteen, K. G. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.09.017 · Cited by 38 · see citing works
Self-citationCurrent Knowledge on Endometriosis Etiology: A Systematic Review of Literature
Михалева, Л. М., Radzinsky, V. E., Orazov, M. R., Николаевна, Х. Т., Sorokina, A. V., Александрович, М. С., Владимировна, В. С., Shustova, V. B., & Sinelnikov, M. Y. (2021) · International Journal of Women s Health · doi:10.2147/ijwh.s306135 · Cited by 37 · see citing works
The role of progestins in treating the pain of endometriosis
Surrey, E. S. (2006) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2006.06.008 · Cited by 36 · see citing works
Treatment of endometriosis in different ethnic populations: a meta-analysis of two clinical trials
Gerlinger, C., Faustmann, T. A., Hassall, J. J., & Seitz, C. (2012) · BMC Women s Health · doi:10.1186/1472-6874-12-9 · Cited by 35 · see citing works
Cutting SRC-1 down to size in endometriosis
Dyson, M. T., & Bulun, S. E. (2012) · Nature Medicine · doi:10.1038/nm.2855 · Cited by 34 · see citing works
Theories on the Pathogenesis of Endometriosis
Nap, A. W. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch5 · Cited by 33 · see citing works
The Levonorgestrel Intrauterine System: Long-Term Contraception and Therapeutic Effects
Sitruk-Ware, R. L., & Inki, P. (2005) · Women s Health · doi:10.2217/17455057.1.2.171 · Cited by 32 · see citing works
P27Kip1 is down-regulated in the endometrium of women with endometriosis
Schor, E., Silva, I. D. C. G., Sato, H., Baracat, E. C., Girão, M. J. B. C., & de Freitas, V. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.12.070 · Cited by 31 · see citing works
Wang, C., Mavrogianis, P. A., & Fazleabas, A. T. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.072496 · Cited by 30 · see citing works
Kim, S. H., Lee, H. W., Kim, Y. H., Koo, Y. H., Chae, H., Kim, C. H., Lee, P. R., & Kang, B.-M. (2009) · Human Reproduction · doi:10.1093/humrep/den484 · Cited by 28 · see citing works
Antisperm antibodies in infertile men and their correlation with seminal parameters
Garcia, P. C., Rúbio, E. M., & Pereira, O. C. M. (2007) · Reproductive Medicine and Biology · doi:10.1111/j.1447-0578.2007.00162.x · Cited by 28 · see citing works
Tanaka, K., Mayne, L., Khalil, A., Baartz, D., Eriksson, L., Mortlock, S., Montgomery, G. W., McKinnon, B. D., & Amoako, A. A. (2019) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2019.11.012 · Cited by 27 · see citing works
Karita, M., Yamashita, Y., Hayashi, A., Yoshida, Y., Hayashi, M., Yamamoto, H., Tanabe, A., Terai, Y., & Ohmichi, M. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.12.026 · Cited by 27 · see citing works
Chae, U., Min, J. Y., Kim, S. H., Ihm, H. J., Oh, Y. S., Park, S. Y., Chae, H. D., Kim, C.-H., & Kang, B. M. (2016) · Yonsei Medical Journal · doi:10.3349/ymj.2016.57.6.1468 · Cited by 27 · see citing works
Influence of inguinal hernia mesh repair on testicular flow and sperm autoimmunity
Štula, I., Družijanić, N., Sršen, D., Čapkun, V., Perko, Z., Sapunar, A., Kraljević, D., Bošnjak, N., & Pogorelić, Z. (2012) · Hernia · doi:10.1007/s10029-012-0918-1 · Cited by 27 · see citing works
Endometrial biology and the etiology of endometriosis
Osteen, K. G., Bruner‐Tran, K. L., & Eisenberg, E. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.01.124 · Cited by 26 · see citing works
Self-citationPeluso, C., Christofolini, D. M., Goldman, C., Mafra, F., Cavalcanti, V., Barbosa, C. P., & Bianco, B. A. V. (2012) · Human Immunology · doi:10.1016/j.humimm.2012.09.007 · Cited by 25 · see citing works
Bruner‐Tran, K. L., Resuehr, D., Ding, T., Lucas, J. A., & Osteen, K. G. (2012) · Current Obstetrics and Gynecology Reports · doi:10.1007/s13669-012-0014-7 · Cited by 25 · see citing works
Self-citationEffects of Prenatal Environmental Exposures on the Development of Endometriosis in Female Offspring
Wei, M., Chen, X., Zhao, Y., Cao, B., & Zhao, W. (2016) · Reproductive Sciences · doi:10.1177/1933719116630418 · Cited by 21 · see citing works
Experimental endometriosis in immunocompromised mice after adoptive transfer of human leukocytes
Bruner‐Tran, K. L., Carvalho-Macedo, A. C., Dulęba, A. J., Crispens, M. A., & Osteen, K. G. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.05.076 · Cited by 22 · see citing works
Self-citationShen, F., Yan, C.-Y., Liu, M., Feng, Y.-H., & Chen, Y. (2014) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-014-3419-x · Cited by 19 · see citing works
Choi, J., Jo, M., Lee, E., Lee, D., & Choi, D. (2019) · Molecular Human Reproduction · doi:10.1093/molehr/gaz064 · Cited by 19 · see citing works
Tiberi, F., Tropea, A., Romani, F., Apa, R., Marana, R., & Lanzone, A. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.03.006 · Cited by 20 · see citing works
Matsuzaki, S., Canis, M. J., Darcha, C., Déchelotte, P. J., Pouly, J. L., & Mage, G. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.02.101 · Cited by 19 · see citing works
Kim, S. H., Kim, S. R., Ihm, H. J., Oh, Y. S., Chae, H. D., Kim, C., & Kang, B. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2969 · Cited by 17 · see citing works
Inside the granulosa transcriptome
D’Aurora, M., Sperduti, S., Emidio, G. D., Stuppia, L., Artini, P. G., & Gatta, V. (2016) · Gynecological Endocrinology · doi:10.1080/09513590.2016.1223288 · Cited by 16 · see citing works
Broi, M. G. D., Rocha, C. V., Meola, J., Martins, W. P., Carvalho, F. M., Ferriani, R. A., & Navarro, P. A. (2017) · JBRA · doi:10.5935/1518-0557.20170038 · Cited by 16 · see citing works
Paradowska, A., Bohring, C., Krause, E., & Krause, W. K. H. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2006.00367.x · Cited by 16 · see citing works
Endometriosis: A general review and rationale for surgical therapy
Barton‐Smith, P., Ballard, K., & Kent, A. S. H. (2006) · Reviews in Gynaecological and Perinatal Practice · doi:10.1016/j.rigapp.2006.05.005 · Cited by 16 · see citing works
Syrcle, S. M., Pelch, K. E., Schroder, A. L., Nichols, B. M., Mills, M. P., Barrier, B., Havey, A. D., & Nagel, S. C. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000320736 · Cited by 13 · see citing works
Bulun, S. E. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00025-1 · Cited by 13 · see citing works
Moreira, L., de Carvalho, E. C. Q., & Caldas-Bussiere, M. C. (2011) · Veterinary Research Communications · doi:10.1007/s11259-011-9470-1 · Cited by 11 · see citing works
Malec‐Milewska, M., Horosz, B., Sękowska, A., Kolęda, I., Kosson, D., & Jakiel, G. (2015) · Annals of Agricultural and Environmental Medicine · doi:10.5604/12321966.1152094 · Cited by 11 · see citing works
Wong, Y. S., Mançanares, A. C. F., Navarrete, F. I., Poblete, P. M., Mendez, L., Ferreira-Dias, G. M., Rodriguez-Alvarez, L., & Castro, F. O. (2023) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.1271240 · Cited by 10 · see citing works
Analysis of CARD10 and CARD11 somatic mutations in patients with ovarian endometriosis
Zou, Y., Zhou, J., Wang, F., Zhang, Z., Liu, F., Luo, Y., Tan, J., Zeng, X., Wan, X., & Huang, O. (2018) · Oncology Letters · doi:10.3892/ol.2018.8659 · Cited by 10 · see citing works
Szukiewicz, D. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2022.11.005 · Cited by 10 · see citing works
Tanha, M., Bozorgmehr, M., Shokri, M.-R., Edalatkhah, H., Tanha, M., Zarnani, A., & Nikoo, S. (2021) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2021.103439 · Cited by 8 · see citing works
Unique Sensitivity of Uterine Tissue and the Immune System for Endometriotic Lesion Formation
Morris, S. A., Korach, K., & Burns, K. A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.805784 · Cited by 6 · see citing works
Liu, F., Zhou, J., Zhang, X., Fang, S.-F., Liu, R., Chen, G., Luo, Y., Zhang, Z., Cheng, Y., Wang, L., et al. (2022) · Human Molecular Genetics · doi:10.1093/hmg/ddac062 · Cited by 5 · see citing works
Progestins for the Treatment of Endometriosis: An Update
Lazzeri, L., Luisi, S. V., & Petraglia, F. (2010) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/228402651000200401 · Cited by 5 · see citing works
Models of Endometriosis: Animal Models I – Rodent‐Based Chimeric Models
Bruner‐Tran, K. L., McConaha, M. E., & Osteen, K. G. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch26 · Cited by 4 · see citing works
Self-citationWahab, M., Taylor, A. H., Pringle, J. H., Thompson, J. R., & Al‐Azzawi, F. (2006) · Molecular Human Reproduction · doi:10.1093/molehr/gal014 · Cited by 4 · see citing works
O papel dos desreguladores endócrinos na fisiopatologia da endometriose: revisão da literatura
Bianco, B. A. V., Christofolini, D. M., de Souza, Â. M. B., & Barbosa, C. P. (2010) · Arquivos Brasileiros de Ciências da Saúde · doi:10.7322/abcs.v35i2.95 · Cited by 3 · see citing works
Hamilton, M., Turpin, V., Ayoub, A., Reihani, A., Arredondo, J., Ask, K., Clark, D. A., & Foster, W. G. (2022) · American Journal of Reproductive Immunology · doi:10.1111/aji.13655 · Cited by 3 · see citing works
Ruiz-Magaña, M. J., Puerta, J. M., Llorca, T., Méndez-Malagón, C., Martínez-Aguilar, R., Abadía‐Molina, A. C., Olivares, E. G., & Ruiz‐Ruiz, C. (2022) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2022.12.005 · Cited by 3 · see citing works
Endometriosis and ovarian cancer
Brown, D., Pejovic, T. B., & Nezhat, F. R. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139003254.015 · Cited by 3 · see citing works
An Investigation into the Surgical Treatment of Endometriosis.
Barton‐Smith, P. (2010) · Surrey Research Insight Open Access (The University of Surrey) · Cited by 3 · see citing works
Sharpe-Timms, K. L., Barrier, B. F., & Nagel, S. C. (2008) · Reproductive medicine and assisted reproductive techniques series · doi:10.3109/9780203091500.038 · Cited by 2 · see citing works
Nataraja, S. G., Kagan, D., Clark, A., & Palmer, S. S. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.04.021 · Cited by 1 · see citing works
- 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 › Public Health, Environmental and Occupational Health › 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
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