Cited by 264Endometriosis Research and TreatmentReproductive System and PregnancyDiagnosis and treatment of tuberculosis

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Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis

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Rana, Nasir, Braun, Donald P., House, Robert, Gebel, Howard, Rotman, Carlos, Dmowski, W. Paul·1996·Fertility and Sterility

DOI 10.1016/s0015-0282(16)58262-4

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Abstract

Objective To evaluate basal (constitutive) and stimulated synthesis of tumor necrosis factor alpha (TNF alpha), interleukin (IL)-8, IL-10 by peritoneal macrophages (PM) in women with endometriosis.Design Peritoneal macrophages were cultured in the presence or absence of lipopolysaccharide (LPS) for 24 hours. Peritoneal fluids (PF) and PM supernatants were assayed for cytokines using ELISA.Setting Institute for the Study and Treatment of Endometriosis and university-based research laboratories.Subjects Fertile controls undergoing tubal ligation (n = 8) and women with endometriosis (n = 17).Intervention Peritoneal fluid samples were obtained at the time of diagnostic laparoscopy (endometriosis group) or laparoscopy for tubal ligation; both were performed in the midluteal phase of the cycle.Results Both basal and LPS stimulated production of TNF alpha, IL-8, and IL-10 by the PM were elevated significantly in women with endometriosis as compared with the fertile controls.Conclusions This study demonstrated that cytokines TNF alpha, IL-8, and IL-10 are synthesized at greater than normal levels by basal and stimulated PM from women with endometriosis. The levels of TNF alpha and IL-8 correlated with the levels in the PF, suggesting that PM are the principal source of these cytokines in the PF.

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“TNFα in peritoneal fluid of such patients (Mori et al., 1991; E-mail: calhazjorge@mailtelepac.pt Taketani et al., 1992; Overton et al., 1996; Rana et al., 1996; Harada et al., 1997) although others have found no differenceTumour necrosis factor α (TNFα) of peritoneal fluid is between women with and…”
Background
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“An increased number of activated macrophages and other immune populations, and differences in the cytokine/chemokine profile are representative of women suffering from endometriosis [42].”
Background
ORIGINAL ARTICLE: Tumor Necrosis Factor (TNF)–TNF Receptor Gene Polymorphisms and Their Serum Levels in Korean Women with Endometriosis
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Macrophage Secretory Products and Sperm Zona Pellucida Binding
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“It has been reported that both basal and lipopolysaccharide-stimulated peritoneal macrophage of women with endometriosis have elevated production of TNF-a, as well as other cytokines, when compared with macrophages from fertile controls.(24) Interestingly, the level of TNF-a produced by lipopolysaccharide-stimulated p…”
Result
Promotion of Angiogenesis by Human Endometrial Lymphocytes
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“This is accompanied by significantly increased concentrations of vasoactive inflammatory cytokines, chemokines and prostaglandins (Akoum et al., 2002; Rana et al., 1996).”
Background
The role of CXC chemokine ligand 16 in physiological and pathological pregnancies
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Genetic variation in tumour necrosis factor and lymphotoxin is not associated with endometriosis in an Australian sample
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“Elevated concentrations of TNF were found in the peritoneal fluid and granulosa cells of women with endometriosis (Rana et al., 1996; Richter et al., 1998; Barcz et al., 2000; Bedaiwy et al., 2002; Braun et al., 2002; Bullimore, 2003; Darai et al., 2003; Galo et al., 2005) suggesting that TNF may play an important rol…”
Background
Endometriotic inflammatory microenvironment induced by macrophages can be targeted by niclosamide†
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Effects of peritoneal macrophages from women with endometriosis on endometrial cellular proliferation in an in vitro coculture model
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ORIGINAL ARTICLE: Effects of Peritoneal Fluid from Endometriosis Patients on Interferon‐γ‐Induced Protein‐10 (CXCL10) and Interleukin‐8 (CXCL8) Released by Neutrophils and CD4+ T Cells
Kim, J., Lee, D., Joo, J., Jin, J., Wang, J., Hong, Y., Kwak, J., & Lee, K. S. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2009.00722.x · Cited by 28
Intraperitoneal recombinant interleukin-2 activates leukocytes in rat endometriosis
Velasco, I., Quereda, F., Bermejo, R., Campos, A., & Acién, P. (2007) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2006.12.001 · Cited by 28
“Indeed, abnormal levels of many ifferent cytokines have been described in the serum and eritoneal fluid of women with endometriosis (Odukoya t al., 1997; Rana et al., 1996; Koyama et al., 1993) hat can be implicated in the embryotoxic activity of eritoneal fluid from these patients (Gómez-Torres et al.”
Background
Involvement of CRH in fever induced by a distinct pre-formed pyrogenic factor (PFPF)
Zampronio, A. R., Melo, M. C. C., Hopkins, S. J., & de Souza, G. E. P. (2000) · Inflammation Research · doi:10.1007/s000110050619 · Cited by 28
Increased Tumor Necrosis Factor-alpha Production by Peripheral Blood Leukocytes from TCDD-Exposed Rhesus Monkeys
Rier, S. E. (2001) · Toxicological Sciences · doi:10.1093/toxsci/60.2.327 · Cited by 28
“, 1990, 1992 ) and the pathogenesis of endometriosis (Braun et al., 1996; Halme, 1989; Rana et al., 1996).”
Background
Intraperitoneal inflammation decreases endometriosis in a mouse model
Nowak, N. M., Fischer, O. M., Gust, T. C., Fuhrmann, U., Habenicht, U. ‐., & Schmidt, A. (2008) · Human Reproduction · doi:10.1093/humrep/den189 · Cited by 27
“…2466 Advance Access publication on July 24, 2008 these macrophages produce higher levels of IL-1ß, IL-6, IL-8, IL-10 and tumour necrosis factor-alpha (TNF-a) under basal and stimulated conditions in vitro compared with PMs of healthy women (Rana et al., 1996; Montagna et al., 2007).”
Background
Fas-Related Apoptosis of Peritoneal Fluid Macrophages in Endometriosis Patients: Understanding the Disease
Gogacz, M., Gałczyński, K., Wojtas, M., Winkler, I., Adamiak, A., Romanek-Piva, K., Rechberger, T., & Kotarski, J. (2017) · Journal of Immunology Research · doi:10.1155/2017/3175394 · Cited by 26
Luteolin Promotes Apoptosis of Endometriotic Cells and Inhibits the Alternative Activation of Endometriosis-Associated Macrophages
Woo, J., Jang, D. S., & Choi, J. (2021) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2021.045 · Cited by 25
“IL-10 is highly expressed in activated macrophages (Wu and Ho, 2003) and is known to suppress T-cell function (e.g., downregulation of the T helper 1 type immune response) in the peritoneal fluid of patients with endometriosis (Rana et al., 1996).”
Background
Protective effects of polydatin on LPS-induced endometritis in mice
Li, R., Maimai, T., Yao, H., Liu, X., He, Z., Xiao, C., Wang, Y., & Xie, G. (2019) · Microbial Pathogenesis · doi:10.1016/j.micpath.2019.103720 · Cited by 25
Role of Estradiol Receptor-α in Differential Expression of 2,3,7,8-Tetrachlorodibenzo-p-dioxin-Inducible Genes in the RL95-2 and KLE Human Endometrial Cancer Cell Lines
Jana, N. R., Sarkar, S., Ishizuka, M., Yonemoto, J., Tohyama, C., & Sone, H. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1288 · Cited by 25
The Peritoneal Fluid Levels of Interleukin‐12 in Women with Endometriosis
Zeyneloğlu, H. B., Senturk, L. M., Seli, E. U., Bahtiyar, M. O., Olive, D. L., & Arici, A. M. (1998) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1998.tb00347.x · Cited by 25
Re-evaluation of mouse models of endometriosis for pathological and immunological research
He, Y., Liang, B., Hung, S. W., Zhang, R., Xu, H., Chung, J. P. W., & Wang, C. C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.986202 · Cited by 24
“A decrease in NK cell cytotoxicity (40) and enhanced activation of peritoneal macrophages (41) also appear in women with endometriosis.”
Background
Cytolysis of Eutopic and Ectopic Endometrial Cells by Peripheral Blood Monocytes and Peritoneal Macrophages in Women with Endometriosis
Braun, D. P., Gebel, H. M., Rana, N., & Dmowski, W. P. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00062-4 · Cited by 24
Expression of Allograft Inflammatory Factor-1 in Human Eutopic Endometrium and Endometriosis: Possible Association with Progression of Endometriosis
Koshiba, H., Kitawaki, J., Teramoto, M., Kitaoka, Y., Ishihara, H., Obayashi, H., Ohta, M., Hara, H., Adachi, T., & Honjo, H. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0871 · Cited by 24
Decreased Expression of HOXA10 May Activate the Autophagic Process in Ovarian Endometriosis
Zheng, J., Luo, X., Bao, J., Huang, X., Jin, Y., Chen, L., & Zheng, F. (2018) · Reproductive Sciences · doi:10.1177/1933719118768704 · Cited by 23
Review: Immunodepression in sepsis and SIRS assessed by ex vivo cytokine production is not a generalized phenomenon: a review
Cavaillon, J., Adib‐Conquy, M., Cloëz-Tayarani, I., & Fitting, C. (2001) · Journal of Endotoxin Research · doi:10.1177/09680519010070020201 · Cited by 23
Effect of Lignocaine on IL-6, IL-8, and MCP-1 in Peritoneal Macrophages and Endometriotic Stromal Cells
Wickström, K., Stavreus-Evers, A. C., Vercauteren, O., Olovsson, M., & Edelstam, G. A. B. (2016) · Reproductive Sciences · doi:10.1177/1933719116657188 · Cited by 22
Use of immunomodulators to treat endometriosis
Kotlyar, A. M., Taylor, H. S., & D’Hooghe, T. M. (2019) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2019.06.006 · Cited by 22
2-Methoxyestradiol in the Pathophysiology of Endometriosis: Focus on Angiogenesis and Therapeutic Potential
Machado-Linde, F., Pelegrín, P., Sanchez-Ferrer, M., León, J., Cascales, P., & Parrilla, J. (2012) · Reproductive Sciences · doi:10.1177/1933719112446080 · Cited by 22
Macrophages are activated by 17b-estradiol: possible permission role in endometriosis
Hong, M., & Quan, Z. (2004) · Experimental and Toxicologic Pathology · doi:10.1078/0940-2993-00335 · Cited by 22
Peritoneal fluid cytokines and sICAM-1 in minimal endometriosis: search for discriminating factors between infertility and/or endometriosis
Skrzypczak, J., Szczepańska, M., Puk, E., Kamieniczna, M., & Kurpisz, M. K. (2005) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2004.11.044 · Cited by 22
“1e) supported the previous reports on elevated (statistically significant) IL-8 levels in peritoneal fluid of women with endometriosis [11–13,16,30].”
BackgroundResult
Soluble interleukin-1 receptor type II blocks monocyte chemotactic protein-1 secretion by u937 cells in response to peripheral blood serum of women with endometriosis
Kharfi, A., & Akoum, A. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03335-6 · Cited by 21
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
Leptin Stimulates Endometriosis Development in Mouse Models
Kim, T. H., Bae, N., Kim, T., Hsu, A. L., Hunter, M. I., Shin, J., & Jeong, J. (2022) · Biomedicines · doi:10.3390/biomedicines10092160 · Cited by 21
Do Environmental Contaminants Adversely Affect Human Reproductive Physiology?
Foster, W. G., & Holloway, A. C. (2003) · Journal of Obstetrics and Gynaecology Canada · doi:10.1016/s1701-2163(16)31080-5 · Cited by 20
Mechanisms of Immunodysregulation in Sepsis
Cavaillon, J., Fitting, C., & Adib‐Conquy, M. (2004) · KARGER eBooks · doi:10.1159/000078879 · Cited by 19
The CCL 17‐ CCR 4 axis between endometrial stromal cells and macrophages contributes to the high levels of IL ‐6 in ectopic milieu
Zhou, W., Hou, X., Wang, X., & Li, D. (2017) · American Journal of Reproductive Immunology · doi:10.1111/aji.12644 · Cited by 19
Differential interleukin-6 messenger ribonucleic acid expression and its distribution pattern in eutopic and ectopic endometrium
Salmassi, A., Açil, Y., Schmutzler, A. G., Koch, K., Jonat, W., & Mettler, L. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.060 · Cited by 19
Pentoxifylline versus medical therapies for subfertile women with endometriosis
Lu, D., Song, H., Li, Y., Clarke, J., & Shi, G. (2009) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007677.pub2 · Cited by 19
Role of some biomarkers in chronic pelvic pain for early detection of endometriosis in infertile women
Foda, A. A., & Aal, I. A. A. (2012) · Middle East Fertility Society Journal · doi:10.1016/j.mefs.2012.06.002 · Cited by 18
Expression of secretory leukocyte protease inhibitor in women with endometriosis
Suzumori, N., Sato, M., Yoneda, T., Ozaki, Y., Takagi, H., & Suzumori, K. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00381-7 · Cited by 18
Understanding endometriosis is the key to successful therapeutic management
Sharpe-Timms, K. L., & Young, S. L. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.09.072 · Cited by 18
Expression of angiopoietin 1 and 2 in ectopic endometrium on the chicken chorioallantoic membrane
Drenkhahn, M., Gescher, D. M., Wolber, E., Meyhöfer-Malik, A., & Malik, E. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.09.040 · Cited by 17
Possible Role of the Posterior Compartment Peritonectomy, as a Part of the Complex Surgery, Regarding Recurrence Rate, Improvement of Symptoms and Fertility Rate in Patients with Endometriosis, Long-Term Follow-Up
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Efficacy of niclosamide on the intra-abdominal inflammatory environment in endometriosis
Shi, M.-X., Sekulovski, N., Whorton, A. E., MacLean, J., Greaves, E., & Hayashi, K. (2021) · The FASEB Journal · doi:10.1096/fj.202002541rrr · Cited by 13
Concentration of Interleukin‐12 in the peritoneal fluid is not influenced by the presence of endometriosis, its stage or the phase of the menstrual cycle
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Polymorphisms in Exons 1B and 1C of the Type I Interleukin‐1 Receptor Gene in Patients with Endometriosis
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High-fat diets promote peritoneal inflammation and augment endometriosis-associated abdominal hyperalgesia
Herup-Wheeler, T., Shi, M., Harvey, M. E., Talwar, C., Kommagani, R., MacLean, J. A., & Hayashi, K. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1336496 · Cited by 15
“These M F populations establish an in ﬂ ammatory environment in the pelvic cavity by secreting cytokines and chemokines, which encourage lesion growth and progression (24, 28, 29, 32, 33) and contribute to endometriosis-associated pelvic pain (32, 34, 35).”
Background
Molecular Basis of Impaired Decidualization in the Eutopic Endometrium of Endometriosis Patients
Retis-Resendiz, A. M., Gómez-Suárez, S. K., García-Gómez, E., & Vázquez-Martínez, E. R. (2025) · Cells · doi:10.3390/cells14050326 · Cited by 18
“…resistance and altered PKA signaling, may contribute to endometriosis-associated infertility through multiple mechanisms: impaired decidualization, defective implantation, compromised placentation, altered Natural Killer cell differentiation, and decreased decidual cell survival [75–81].”

Authors: Rana, N., Braun, D. P., House, R., Gebel, H., Rotman, C., & Dmowski, W. P.
Affiliations: Rush University Medical Center (US)
ORCID: Gebel, Howard
Venue: Fertility and Sterility
Publisher: Elsevier BV
Published: 1996-05
Volume: 65
Issue: 5
Pages: 925-930
ISSN: 0015-0282 (ISSN-L)
DOI: 10.1016/s0015-0282(16)58262-4
OpenAlex: W98713221
Cited by: 264
References: 27
Citations by year: 2026: 2 · 2025: 8 · 2024: 12 · 2023: 9 · 2022: 5 · 2021: 8 · 2020: 6 · 2019: 5 · 2018: 6 · 2017: 9 · 2016: 6 · 2015: 4 · 2014: 4 · 2013: 8 · 2012: 9
FWCI: 11.33
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 9522 d)
Locations: Fertility and Sterility (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01ca058922-03)
National Cancer Institute (CA 58922)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Health Sciences › Medicine › Infectious Diseases › Diagnosis and treatment of tuberculosis
Keywords: endometriosis, peritoneal macrophages, cytokine production, TNF-α, interleukin-8, IL-10, lipopolysaccharide stimulation, peritoneal fluid
MeSH terms: Ascitic Fluid, Cells, Cultured, Endometriosis, Female, Humans, Lipopolysaccharides, Tumor Necrosis Factor-alpha, Cytokines, Interleukin-8, Interleukin-10, Macrophages, Peritoneal

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Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis

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