Inflammatory cytokines differentially up-regulate human endometrial haptoglobin production in women with endometriosis

Sharpe-Timms, K. L.; Nabli, H.; Zimmer, R. L.; Birt, J. A.; Davis, J. W.

doi:10.1093/humrep/deq032

Cited by 43Endometriosis Research and TreatmentEctopic Pregnancy Diagnosis and ManagementReproductive System and Pregnancy

Inflammatory cytokines differentially up-regulate human endometrial haptoglobin production in women with endometriosis

Open access

Sharpe-Timms, K. L., Nabli, H., Zimmer, R. L., Birt, J. A., Davis, J. W.·2010·Human Reproduction

DOI 10.1093/humrep/deq032PMC PMC2902841

Open this paper in CoChat — free account Open PDF

Abstract

BACKGROUND: Evidence suggests that eutopic endometrium from women with endometriosis (US-E) has intrinsic functional anomalies compared with women without endometriosis (US-C). We hypothesized that differences in endometrial haptoglobin (eHp) mRNA and protein levels exist between eutopic endometrium from US-E and US-C and that inflammatory mediators may be involved. METHODS: Endometrial stromal cells and tissue explants from US-E (n = 18) and US-C (n = 18) were cultured (24 h/48 h for cells/explants) with interleukin (IL)-1alpha, -1beta, -6, -8 or tumor necrosis factor-alpha (TNF-alpha) at 0-100 ng/ml. eHp protein in media and mRNA levels were quantified by enzyme-linked immunosorbent assay and quantitative PCR. RESULTS: In eutopic endometrial stromal cells from US-E, IL-1beta, IL-6 and TNF-alpha (10 ng/ml) increased eHp mRNA levels (P = 0.002, P < 0.001 and P < 0.001, respectively) and eHp protein (P = 0.023, 0.031 and 0.006, respectively) versus control. In endometrial tissues from US-E, IL-1beta, IL-6 and TNF-alpha increased eHp mRNA (P < 0.001, P = 0.017 and P < 0.001, respectively) and eHp protein (P < 0.001, P = 0.007 and 0.039, respectively) versus control. IL-1alpha and IL-8 had small or no effects on isolated endometrial cells or tissues. In US-C, IL-1beta, IL-8 and TNF-alpha each reduced eHp mRNA in endometrial stromal cells (all P < 0.001) versus control; IL-1alpha and IL-6 had no effect. eHp mRNA increased in endometrial tissues from US-C in response to IL-1beta (P = 0.008), IL-6 (P = 0.015) and TNF-alpha (P = 0.031) versus control; IL-1alpha or IL-8 had no effect. CONCLUSIONS: Endometrium from US-E differentially responds to specific inflammatory cytokines by production of eHp. We propose that up-regulation of endometrial eHp by inflammatory mediators disrupts normal endometrial function and may facilitate the pathogenesis of endometriosis.

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

Crossref · 10.1093/humrep/deq032

Cites

65 of 65 references verified0 citation errors · 0 not checkable

Statistics

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?

IL-6, IL-10, IFN, and TGF-b are implicated in immune and inflammatory responses in the pathogenesis of endometriosis.
“Interleukin (IL)-6, IL-10, interferon (IFN), and transforming growth factor (TGF-b) are implicated in the immune and inflammatory responses in the pathogenesis of endometriosis.61,64”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [64]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Applied Longitudinal Analysis
Fitzmaurice, G. M., Laird, N. M., & Ware, J. H. (2011) · Wiley Series in Probability and Statistics · doi:10.1002/9781119513469 · Cited by 4,639 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Linear Mixed Models for Longitudinal Data
Verbeke, G. (1997) · Lecture Notes in Statistics · doi:10.1007/978-1-4612-2294-1_3 · Cited by 3,506 · see citing works
Generalized, Linear, and Mixed Models
McCulloch, C. E., & Searle, S. R. (2000) · Wiley series in probability and statistics · doi:10.1002/0471722073 · Cited by 3,057 · see citing works
Dating the Endometrial Biopsy
Rw, N., Hertig, A. T., & Rock, J. A. (1950) · Fertility and Sterility · doi:10.1016/s0015-0282(16)30062-0 · Cited by 2,854 · see citing works
Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity
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
Metastatic or Embolic Endometriosis, due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation.
(1927) · PubMed Central · Cited by 1,008 · see citing works
Biological and clinical significance of haptoglobin polymorphism in humans
Langlois, M. R., & Delanghe, J. R. (1996) · Clinical Chemistry · doi:10.1093/clinchem/42.10.1589 · Cited by 942 · see citing works
Endometriosis: epidemiology and aetiological factors
Viganò, P., Parazzini, F., Somigliana, E., & Vercellini, P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.007 · Cited by 718 · see citing works
Expression Profiling of Endometrium from Women with Endometriosis Reveals Candidate Genes for Disease-Based Implantation Failure and Infertility
Kao, 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
High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners
Meuleman, C., Vandenabeele, B., Fieuws, S., Spiessens, C., Timmerman, D., & D'Hooghe, T. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.04.056 · Cited by 606 · see citing works
Role of cytokines in endometriosis
Harada, T., Iwabe, T., & Terakawa, N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01816-7 · Cited by 567 · see citing works
History of adenomyosis
Benagiano, G., & Brosens, I. A. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.007 · Cited by 536 · see citing works
Statistics notes: Transformations, means, and confidence intervals: Fig 1
Bland, J. M., & Altman, D. G. (1996) · BMJ · doi:10.1136/bmj.312.7038.1079 · Cited by 426 · see citing works
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 · see citing works
The development of the implantation theory for the origin of peritoneal endometriosis
Sampson, J. A. (1940) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(40)91238-8 · Cited by 348 · see citing works
Endometriosis and Subfertility: Is the Relationship Resolved?
D’Hooghe, T. M., Debrock, S., Hill, J. A., & Meuleman, C. (2003) · Seminars in Reproductive Medicine · doi:10.1055/s-2003-41330 · Cited by 320 · see citing works
Reprint of: Dating the Endometrial Biopsy
Rw, N., Hertig, A. T., & Rock, J. A. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.08.079 · Cited by 301 · see citing works
Statistics Notes: Transforming data
Bland, J. M., & Altman, D. G. (1996) · BMJ · doi:10.1136/bmj.312.7033.770 · Cited by 297 · see citing works
Biological functions of haptoglobin--new pieces to an old puzzle.
Dobryszycka, W. M. (1997) · PubMed · Cited by 276 · see citing works
Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis
Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., & Dmowski, W. P. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58262-4 · Cited by 264 · cited 2× · see citing works
“There are many potential sources of inflammation in the uterine cavity (Oral et al., 1996; Rana et al., 1996; Koninckx et al., 1999; D’Hooghe et al., 2001; Harada et al., 2001).”
Background
Endometriotic disease: the role of peritoneal fluid
Koninckx, P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.741 · Cited by 252 · see citing works
Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons
D'Hooghe, T. M. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.84 · Cited by 231 · see citing works
The peritoneal environment in endometriosis
Oral, E. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.385 · Cited by 201 · see citing works
Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium
Eyster, K. M., Klinkova, O. V., Kennedy, V., & Hansen, K. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.01.056 · Cited by 192 · see citing works
Endometrial 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 · see citing works
Self-citation
Embryo-maternal signalling: how the embryo starts talking to its mother to accomplish implantation
Herrler, A., von Rango, U., & Beier, H. M. (2003) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61717-8 · Cited by 178 · see citing works
Cytokine profiles in serum and peritoneal fluid from infertile women with and without endometriosis
Kalu, E., Sumar, N., Giannopoulos, T., Patel, P., Croucher, C., Sherriff, E., & Bansal, A. S. (2007) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2007.00569.x · Cited by 173 · see citing works
The 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
Endometriosis and Inflammation in Infertility
Halis, G., & Arici, A. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1335.032 · Cited by 163 · see citing works
Tumor Necrosis Factor-α-Induced Interleukin-8 (IL-8) Expression in Endometriotic Stromal Cells, Probably through Nuclear Factor-κB Activation: Gonadotropin-Releasing Hormone Agonist Treatment Reduced IL-8 Expression
Sakamoto, Y., Harada, T., Horie, S., Iba, Y., Taniguchi, F., Yoshida, S., Iwabe, T., & Terakawa, N. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020666 · Cited by 153 · see citing works
Endometriosis
Farquhar, C. M. (2007) · BMJ · doi:10.1136/bmj.39073.736829.be · Cited by 146 · see citing works
Pathogenesis of endometriosis: The role of defective ‘immunosurveillance’
Christodoulakos, G., Augoulea, A., Lambrinoudaki, I., Sioulas, V., & Creatsas, G. (2007) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625180701387266 · Cited by 133 · see citing works
The human haptoglobin gene: transcriptional regulation during development and acute phase induction
Oliviero, S., Morrone, G., & Cortese, R. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb02450.x · Cited by 123 · cited 1× · see citing works
“Endometriosis, characterized by the growth of endometrial glands and stroma outside the uterine cavity, is a gynecological disorder affecting millions of women of reproductive age worldwide (Farquhar, 2007; Meuleman et al., 2009).”
Background
Is 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
Immunological aspects of endometriosis
Vinatier, D. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.371 · Cited by 113 · see citing works
Peritoneal fluid environment in endometriosis. Clinicopathological implications.
Bedaiwy, M. A., & Falcone, T. (2003) · PubMed · Cited by 108 · see citing works
Peritoneal fluid-mediated enhancement of eutopic and ectopic endometrial cell proliferation is dependent on tumor necrosis factor-α in women with endometriosis
Braun, D. P., Ding, J., & Dmowski, W. P. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03318-6 · Cited by 105 · see citing works
Interaction of cytokine- and glucocorticoid-response elements of acute-phase plasma protein genes. Importance of glucocorticoid receptor level and cell type for regulation of the elements from rat alpha 1-acid glycoprotein and beta-fibrinogen genes.
Baumann, H., Jahreis, G. P., & Morella, K. K. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45700-6 · Cited by 100 · see citing works
Endometriosis and human infertility: a new investigation into the role of eutopic endometrium
Minici, F., Tiberi, F., Tropea, A., Orlando, M., Gangalè, M. F., Romani, F., Campo, S., Bompiani, A., Lanzone, A., & Apa, R. (2007) · Human Reproduction · doi:10.1093/humrep/dem399 · Cited by 89 · see citing works
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 · see citing works
Statistics Notes: Logarithms
Bland, J. M., & Altman, D. G. (1996) · BMJ · doi:10.1136/bmj.312.7032.700 · Cited by 78 · see citing works
Endometriotic haptoglobin binds to peritoneal macrophages and alters their function in women with endometriosis
Sharpe-Timms, K. L., Zimmer, R. L., Ricke, E. A., Piva, M. A., & Horowitz, G. M. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03317-4 · Cited by 77 · see citing works
Self-citation
Pathogenesis of Endometriosis
Witz, C. A. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000049425 · Cited by 73 · see citing works
Tumor necrosis factor-α induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-κB and mitogen-activated protein kinase pathways
Yamauchi, N., Harada, T., Taniguchi, F., Yoshida, S., Iwabe, T., & Terakawa, N. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.02.134 · Cited by 73 · see citing works
Pain and endometriosis
Evans, S., Moalem‐Taylor, G., & Tracey, D. J. (2007) · Pain · doi:10.1016/j.pain.2007.07.006 · Cited by 68 · see citing works
Endometriotic Lesions Synthesize and Secrete a Haptoglobin-Like Protein1
Sharpe-Timms, K. L., Piva, M. A., Ricke, E. A., Surewicz, K. A., Zhang, Y. L., & Zimmer, R. L. (1998) · Biology of Reproduction · doi:10.1095/biolreprod58.4.988 · Cited by 61 · see citing works
Self-citation
Cytokines Regulate Matrix Metalloproteinases in Human Uterine Endometrial Fibroblast Cells Through a Mechanism That Does Not Involve Increases in Extracellular Matrix Metalloproteinase Inducer
Braundmeier, A. G., & Nowak, R. A. (2006) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2006.00418.x · Cited by 60 · see citing works
Haptoglobin is present in human endometrium and shows elevated levels in the decidua during pregnancy
Berkova, N. (2001) · Molecular Human Reproduction · doi:10.1093/molehr/7.8.747 · Cited by 60 · see citing works
Effect of menstruation and intrapelvic injection of endometrium on inflammatory parameters of peritoneal fluid in the baboon (Papio anubis and Papio cynocephalus )
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
Differential expression and localization of de-novo synthesized endometriotic haptoglobin in endometrium and endometriotic lesions
Sharpe-Timms, K. L. (2000) · Human Reproduction · doi:10.1093/humrep/15.10.2180 · Cited by 59 · see citing works
Self-citation
Polypeptides synthesized and released by human endometriosis differ from those of the uterine endometrium in cell and tissue explant culture
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
Self-citation
Interleukin-6 Differentially Stimulates Haptoglobin Production by Peritoneal and Endometriotic Cells in Vitro: A Model for Endometrial-Peritoneal Interaction in Endometriosis
Piva, M. A., Horowitz, G. M., & Sharpe-Timms, K. L. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7613 · Cited by 57 · see citing works
Peritoneal fluid as an unrecognised vector between female reproductive tissues
Hunter, R. H. F., Cicinelli, E., & Einer‐Jensen, N. (2007) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340601155098 · Cited by 44 · see citing works
The endometrium and hormonal contraceptives
Benagiano, G., Pera, A., & Primiero, F. M. (2000) · Human Reproduction · doi:10.1093/humrep/15.suppl_1.101 · Cited by 39 · see citing works
Polypeptides Synthesized and Released by Rat Ectopic Uterine Implants Differ from those of the Uterus in Culture1
Sharpe-Timms, K. L., & Vernon, M. W. (1993) · Biology of Reproduction · doi:10.1095/biolreprod48.6.1334 · Cited by 35 · see citing works
Self-citation
A Haptoglobin-Like Glycoprotein is Produced by Implantation-Stage Rabbit Endometrium1
Hoffman, L. H., Winfrey, V. P., Blaeuer, G. L., & Olson, G. E. (1996) · Biology of Reproduction · doi:10.1095/biolreprod55.1.176 · Cited by 34 · see citing works
Peritoneal endometriotic lesions differentially express a haptoglobin-like gene*
Piva, M. A. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.1.71 · Cited by 34 · see citing works
Specific expression of haptoglobin mRNA in implantation-stage rabbit uterine epithelium
Olson, G. E., Winfrey, V. P., Matrisian, P. E., Melner, M. H., & Hoffman, L. H. (1997) · Journal of Endocrinology · doi:10.1677/joe.0.1520069 · Cited by 32 · see citing works
Glycosylation and over-expression of endometriosis-associated peritoneal haptoglobin
Piva, M. A., Moreno, J. I., & Sharpe-Timms, K. L. (2002) · Glycoconjugate Journal · doi:10.1023/a:1022580813870 · Cited by 29 · see citing works
Self-citation
Haptoglobin expression by shed endometrial tissue fragments found in peritoneal fluid
Sharpe-Timms, K. L. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.02.014 · Cited by 22 · see citing works
Self-citation
Haptoglobin expression and release by rabbit oviduct and endometrium, its localization in blastocyst extra-embryonic matrix and fluid during preimplantation time
Herrler, A., Krusche, C. A., Müller-Schöttle, F., & Beier, H. M. (2004) · Human Reproduction · doi:10.1093/humrep/deh517 · Cited by 19 · see citing works
SHORT COMMUNICATION: Increased Expression of Glutathione by Estradiol, Tumor Necrosis Factor‐Alpha, and Interleukin 1‐Beta in Endometrial Stromal Cells
Lee, S. R., Kim, S. H., Lee, H. W., Kim, Y., Chae, H. D., Kim, C., & Kang, B. M. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2009.00760.x · Cited by 18 · see citing works
Ectopic, autologous eutopic and normal endometrial stromal cells have altered expression and chemotactic activity of RANTES
Fang, C.-L., Han, S., Fu, S., Wang, W., Kong, N., & Wang, X.-L. (2009) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2008.12.001 · Cited by 12 · see citing works

Flagged first, then by citations

1 of the 66 references couldn’t be matched to a known paper.

Research works printed but not linked: 15

Baumann H, Jahreis GP, Morella KK. Interaction of cytokine-and glucocorticoid-response elements of acute-phase plasma protein genes. J Biol Chem 1990;265:22275-22281.
Review.
Review.
Bland JM, Altman DG. Logarithms. BMJ 1996a;312:700.
Bland JM, Altman DG. Transforming data. BMJ 1996b;312:770.
Bland JM, Altman DG. Transformations, means, and confidence intervals. BMJ 1996c;12:1079.
Bowman BH. Haptoglobin. In: Bowman BH (ed). Hepatic Plasma Proteins. San Diego: Academic Press, 1993, 159 -167.
D'Hooghe TM, Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation. Hum Reprod Update 2002;8:84-88.
D'Hooghe TM, Bambra CS, Xiao L, Hill JA. The effect of menstruation and intrapelvic injection of endometrium on peritoneal fluid parameters in the baboon. Am J Obstet Gynecol 2001;184:917 -925.
Review.
Review.
Review.
Sharpe-Timms KL, Ricke EA, Piva M, Horowitz GM. Differential in vivo expression and localization of endometriosis protein-I (ENDO-I), a haptoglobin homologue, in endometrium and endometriotic lesions. Hum Reprod 2000;15:101 -105.
Sharpe-Timms KL, Zimmer RL, Ricke EA, Piva MA, Horowitz GM. Endometriotic haptoglobin binds peritoneal macrophages and alters their function in endometriosis. Fertil Steril 2002;78: 810 -819.
Review.

Sorted by citations

Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France
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
Risks of adverse pregnancy outcome in endometriosis
Brosens, I., Brosens, J. J., Fusi, L., Al-Sabbagh, M., Kuroda, K., & Benagiano, G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.02.024 · Cited by 132 · see citing works
Abnormal peritoneal regulation of chemokine activation—The role of IL ‐8 in pathogenesis of endometriosis
Sikora, J., Smycz‐Kubańska, M., Mielczarek‐Palacz, A., & Kondera‐Anasz, Z. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12622 · Cited by 118 · see citing works
Functional endometrial polyps in infertile asymptomatic patients: a possible evolution of vascular changes secondary to endometritis
Carvalho, F. M., Aguiar, F. N., Tomioka, R. B., de Oliveira, R. M., Frantz, N., & Ueno, J. (2013) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2013.05.012 · Cited by 105 · see citing works
Visceral hypersensitivity in endometriosis: a new target for treatment?
Issa, B., Onon, T. S., Agrawal, A., Shekhar, C., Morris, J., Hamdy, S., & Whorwell, P. J. (2012) · Gut · doi:10.1136/gutjnl-2011-300306 · Cited by 90 · see citing works
Time-dependent behavioral, neurochemical, and metabolic dysregulation in female C57BL/6 mice caused by chronic high-fat diet intake
Krishna, S., Lin, Z., Serre, C. B. D. L., Wagner, J. J., Harn, D. A., Pepples, L. M., Djani, D. M., Weber, M., Srivastava, L., & Filipov, N. M. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.02.007 · Cited by 77 · see citing works
Endometriosis, a modern syndrome.
Brosens, I. A., & Benagiano, G. (2011) · PubMed Central · Cited by 68 · see citing works
The Complementary and Alternative Medicine for Endometriosis: A Review of Utilization and Mechanism
Kong, S., Zhang, Y., Liu, C., Tsui, I. K., Guo, Y., Ai, B.-B., & Han, F. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/146383 · Cited by 68 · see citing works
Interleukin‐6, intracellular adhesion molecule‐1, and glycodelin A levels in serum and peritoneal fluid as biomarkers for endometriosis
Mosbah, A., Nabiel, Y., & Khashaba, E. O. (2016) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2016.01.018 · Cited by 61 · see citing works
Glycyrrhizin inhibits LPS-induced inflammatory mediator production in endometrial epithelial cells
Wang, X., Hao, H.-G., & Chu, L. (2017) · Microbial Pathogenesis · doi:10.1016/j.micpath.2017.05.032 · Cited by 61 · see citing works
Endometriosis, especially mild disease: a risk factor for miscarriages
Kohl Schwartz, A. S., Wölfler, M. M., Mitter, V., Rauchfuss, M., Haeberlin, F., Eberhard, M., von Orelli, S., Imthurn, B., Imesch, P., Fink, D., et al. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.025 · Cited by 63 · see citing works
Types of acute phase reactants and their importance in vaccination (Review)
Khalil, R., & Al-Humadi, N. H. (2020) · Biomedical Reports · doi:10.3892/br.2020.1276 · Cited by 55 · see citing works
Potential scenarios leading to ovarian cancer arising from endometriosis
Kobayashi, H. (2015) · Redox Report · doi:10.1179/1351000215y.0000000038 · Cited by 52 · see citing works
Progress on haptoglobin and metabolic diseases
Wan, B.-N., Zhou, S., Wang, M., Zhang, X., & Ji, G. (2021) · World Journal of Diabetes · doi:10.4239/wjd.v12.i3.206 · Cited by 43 · see citing works
Overexpression of TGF‑β enhances the migration and invasive ability of ectopic endometrial cells via ERK/MAPK signaling pathway
Liu, Z., Yi, L., Du, M., Gong, G., & Zhu, Y. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7522 · Cited by 41 · see citing works
Retracted
Systematic review of genome-wide association studies on susceptibility to endometriosis
Cardoso, J. V., Perini, J. A., Machado, D. E., Pinto, R., & Medeiros, R. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.10.017 · Cited by 36 · see citing works
TGF- 1 induces proteinase-activated receptor 2 (PAR2) expression in endometriotic stromal cells and stimulates PAR2 activation-induced secretion of IL-6
Saito, A., Osuga, Y., Yoshino, O., Takamura, M., Hirata, T., Hirota, Y., Koga, K., Harada, M., Takemura, Y., Yano, T., et al. (2011) · Human Reproduction · doi:10.1093/humrep/der125 · Cited by 36 · see citing works
Genetic Variation at Chromosome 2q13 and Its Potential Influence on Endometriosis Susceptibility Through Effects on the IL-1 Family
Gajbhiye, R., McKinnon, B. D., Mortlock, S., Mueller, M. D., & Montgomery, G. W. (2018) · Reproductive Sciences · doi:10.1177/1933719118768688 · Cited by 31 · see citing works
Sphingosine I Phosphate (S1P) Increased IL-6 Expression and Cell Growth in Endometriotic Cells
Yoshino, O., Yamada‐Nomoto, K., Kano, K., Ono, Y., Kobayashi, M., Ito, M., Yoneda, S., Nakashima, A., Shima, T., Onda, T., et al. (2019) · Reproductive Sciences · doi:10.1177/1933719119828112 · Cited by 29 · see citing works
Hp: an Inflammatory Indicator in Cardiovascular Disease
Graves, K. L., & Vigerust, D. J. (2016) · Future Cardiology · doi:10.2217/fca-2016-0008 · Cited by 29 · see citing works
The Risk of Endometrial Cancer and Uterine Sarcoma Following Endometriosis or Pelvic Inflammatory Disease
Huang, J., Sheng‐Kai, K., Wang, L., Chiang, C., Yang, S., Wang, C., & Wang, P.-H. (2023) · Cancers · doi:10.3390/cancers15030833 · Cited by 19 · see citing works
Proteolytic tailoring of the heat shock protein 70 and its implications in the pathogenesis of endometriosis
Chehna-Patel, N., Warty, N. R., Sachdeva, G., & Khole, V. V. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.01.122 · Cited by 16 · see citing works
Dietary Inflammatory Index score and risk of developing endometriosis: A case–control study
da Silva, C. V. D., Felipe, V. A. D. A., Shivappa, N., Hébert, J. R., Perini, J. A., de Brito, P. D., Cardoso, J. V., Ferrari, R., & Filho, G. L. D. A. (2020) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026520967599 · Cited by 16 · see citing works
Short communication: Assessment of biomarkers of inflammation in the vaginal discharge of postpartum dairy cows diagnosed with clinical metritis
Barragan, A. A., Lakritz, J., Carman, M. K., Bas, S., Hovingh, E., & Schuenemann, G. M. (2019) · Journal of Dairy Science · doi:10.3168/jds.2018-15854 · Cited by 15 · see citing works
Molecular evaluation of proliferative-phase endometrium may provide insight about the underlying causes of infertility in women with endometriosis
Hurst, B. S., Shimp, K. E., Elliot, M. C., Marshburn, P. B., Parsons, J., & Bahrani-Mostafavi, Z. (2013) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-013-3103-6 · Cited by 14 · see citing works
Evaluation of IL-3, IL-5, and IL-6 concentration in the follicular fluid of women with endometriosis: A cross-sectional study
Ghodsi, M., Hojati, V., Attaranzadeh, A., & Saifi, B. (2022) · International Journal of Reproductive BioMedicine (IJRM) · doi:10.18502/ijrm.v20i3.10713 · Cited by 13 · see citing works
rhTNFR: Fc Suppresses the Development of Endometriosis in a Mouse Model by Downregulating Cell Proliferation and Invasiveness
Liu, Y., Sun, L., Hou, Z., Mao, Y., Cui, Y., & Liu, J. (2015) · Reproductive Sciences · doi:10.1177/1933719115620495 · Cited by 13 · see citing works
Feeding rumen-protected lysine altered immune and metabolic biomarkers in dairy cows during the transition period
Fehlberg, L. K., Guadagnin, A. R., Thomas, B. L., Ballou, M., Loor, J. J., Sugimoto, Y., Shinzato, I., & Cardoso, F. C. (2023) · Journal of Dairy Science · doi:10.3168/jds.2022-22349 · Cited by 12 · see citing works
Molecular Mechanisms of Endometriosis Revealed Using Omics Data
Cho, S. B. (2023) · Biomedicines · doi:10.3390/biomedicines11082210 · Cited by 10 · see citing works
Biomarkers of endometriosis
Arsalan, H. M., Mumtaz, H., & Laganà, A. S. (2025) · Advances in clinical chemistry · doi:10.1016/bs.acc.2025.01.004 · Cited by 8 · see citing works
Haptoglobin gene polymorphisms in peri‐implantitis and chronic periodontitis
Ebadian, A. R., Kadkhodazadeh, M., Naghavi, S. H. H., Torshabi, M., & Tamizi, M. (2013) · Journal of Investigative and Clinical Dentistry · doi:10.1111/jicd.12028 · Cited by 8 · see citing works
Molecular mechanisms in IL-1β-mediated decorin production by decidual cells
Halari, C. D., Renaud, S. J., & Lala, P. K. (2021) · Molecular Human Reproduction · doi:10.1093/molehr/gaab068 · Cited by 7 · see citing works
The pathogenesis of endometriosis: clues from the immunological evidence
Villanacci, R., Bandini, V., Ottolina, J., Pagliardini, L., Candiani, M., & Viganò, P. (2021) · Minerva Obstetrics and Gynecology · doi:10.23736/s2724-606x.21.04768-7 · Cited by 7 · see citing works
Serum Proteomic Analysis of Cannabis Use Disorder in Male Patients
Alasmari, F. F., Alsanea, S., Alfadda, A. A., Alanazi, I. O., Musambil, M., Masood, A., Alqahtani, F., Fantoukh, O. I., Alasmari, A. F., & Benabdelkamel, H. (2021) · Molecules · doi:10.3390/molecules26175311 · Cited by 5 · see citing works
TNFα and IL1β Stimulate Differential Gene Expression in Endometrial Stromal Cells
Chalpe, A. J., Law, C. D., Dumdie, J. N., Hansen, K. A., & Eyster, K. M. (2015) · Advances in Biological Chemistry · doi:10.4236/abc.2015.52010 · Cited by 4 · see citing works
Metabolomics Analysis Reveals Gut Microbiota-Associated Sakuranin Modulates Endometrial Stem Cell Differentiation and Inflammation to Alleviate Pain in Endometriosis
Shi, W., Wang, M., Jin, Z., Chen, X., Li, J., Lai, H., Li, X. F., Zhong, Q., Chen, Y., & Chen, S. (2026) · Journal of Pain Research · doi:10.2147/jpr.s557430 · Cited by 1 · see citing works
Chemokine CCL21 promotes the pathological progression of endometriosis by regulating inflammatory cytokine expression and activating the NF-κB signaling pathway
Wang, N., Liu, B., Zhang, Y., Man, X.-H., Jiang, R., Yao, L., Dong, X., Guo, M., Sun, J., & Bi, J. (2026) · International Immunopharmacology · doi:10.1016/j.intimp.2026.117079 · Cited by 1 · see citing works
Tumor Necrosis Factor-α and Interleukin-1β Treatment of Endometrial Stromal Cells Does not Promote Their Adhesion to Peritoneal Mesothelial Cells in an in Vitro Model of Early-Stage Endometriosis
Lousse, J., Defrère, S., Colette, S., Langendonckt, A. V., & Donnez, J. (2011) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.2011.8524
Atypical Expression of COX-2, StAR, CYP19A1 and Apoptotic Regulators in CD90 Positive Endometrial Stromal Cells from Women with Endometriosis
Kadalmani, B., Taylor, H. S., Krikun, G., & Palanivel, K. (2013) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.5000149
MODERN CONCEPTS OF PELVIC ADHESIONS’ ETIOLOGY AND PATHOGENESIS AT REPRODUCTIVE AGE WOMEN
Alekseev, A. A., & Sulima, A. N. (2016) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.21886/2219-8075-2016-1-4-14
Phase-dependent cytokine dynamics in multicellular in vitro models of the human endometrium
Gavriel, M., Jaffa, A. J., Elad, D., & Grisaru, D. (2025) · F&S Science · doi:10.1016/j.xfss.2025.12.001
Fertility restoration in women with infertility associated with ovarian endometriomas: a retrospective study
Kiselev, M. A., Репина, Н. Б., Nikiforov, А. А., Николаевна, Д. М., & Kiselev, A. M. (2026) · Perm Medical Journal · doi:10.17816/pmj431111-123
Diagnostic accuracy of intraoperative haptoglobin point-of-care testing in ovarian tumor fluid versus frozen section for epithelial ovarian cancer
Titaley, B. R., Salima, S., Kurniadi, A., Suardi, D., Harsono, A. B., Winarno, G. N. A., Agustiansyah, P., & Nisa, A. S. (2026) · BMC Research Notes · doi:10.1186/s13104-026-07866-8

Interleukin-6 Differentially Stimulates Haptoglobin Production by Peritoneal and Endometriotic Cells in Vitro: A Model for Endometrial-Peritoneal Interaction in Endometriosis
Piva, M. A., Horowitz, G. M., & Sharpe-Timms, K. L. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7613 · Cited by 57 · see citing works
Self-citation
Regulation of Interleukin-8 Expression in Human Endometrial Endothelial Cells: A Potential Mechanism for the Pathogenesis of Endometriosis
Luk, J., Seval, Y., Kayisli, U. A., Ulukuş, M., Ulukuş, Ç., & Arici, A. M. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1813 · Cited by 47 · see citing works
Intense focal expression of de novo synthesized haptoglobin by subluminal endometrial stroma correlates with the window of implantation in women with endometriosis
Sharpe-Timms, K. L., Zimmer, R. L., & Ricke, E. A. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03612-9
Self-citation
Interleukin-6 secretion in vitro is up-regulated in ectopic and eutopic endometrial stromal cells from women with endometriosis
Tseng, J. F., Ryan, I., Milam, T. D., Murai, J. T., Schriock, E. D., LANDERS, D. V., & Taylor, R. N. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.3.8772585 · Cited by 291 · see citing works
Inflammatory pathway in eutopic endometrium of women with endometriosis
Scillitani, G., Serviddio, G., Cantatore, S., Rosario, F. D., Scutiero, G., Altomare, E., Matteo, M., NERI, M., & GRECO, P. (2012) · Institutional Research Information System University of Ferrara (University of Ferrara)

Authors: Sharpe-Timms, K. L., Nabli, H., Zimmer, R. L., Birt, J. A., & Davis, J. W.
Affiliations: University of Missouri (US)
Corresponding author: Sharpe-Timms, K. L.
ORCID: Sharpe-Timms, K. L.
Birt, J. A.
Davis, J. W.
Venue: Human Reproduction
Publisher: Oxford University Press (OUP)
Published: 2010-02-22
Volume: 25
Issue: 5
Pages: 1241-1250
ISSN: 0268-1161 (ISSN-L)
1460-2350
DOI: 10.1093/humrep/deq032
PMC: PMC2902841
OpenAlex: W2149000495
Cited by: 43
References: 66
Citations by year: 2026: 4 · 2025: 2 · 2023: 3 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 1 · 2017: 3 · 2016: 4 · 2015: 3 · 2014: 1 · 2013: 5 · 2012: 1
FWCI: 4.19
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Human Reproduction (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01hd040849-04)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD040849)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Keywords: endometriosis, inflammatory cytokines, endometrial stromal cells, IL-1β, interleukin-6, TNF-α, interleukin-8, interleukin-1 alpha, eutopic endometrium, gene expression regulation, endometritis
MeSH terms: Endometriosis, Endometrium, Female, Haptoglobins, Humans, RNA, Messenger, Tumor Necrosis Factor-alpha, Interleukin-6, Up-Regulation, Cytokines, Interleukin-8, Stromal Cells, Inflammation Mediators, Interleukin-1alpha, Interleukin-1beta, In Vitro Techniques

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

Inflammatory cytokines differentially up-regulate human endometrial haptoglobin production in women with endometriosis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks