Neutrophil depletion reduces endometriotic lesion formation in mice
Abstract
Problem: Neutrophils are known to be accumulated in endometriosis; however, direct evidence of the impact of neutrophils in the development of endometriosis was lacking. To clarify the importance of neutrophils, we examined the effect of neutrophil depletion on the development of endometriosis. Method of study: Ovariectomized, estradiol‐replaced, 8‐week‐old, female BALB/c mice were injected with endometrial fragments (Day 0). Neutrophils were depleted by anti‐Gr‐1 antibody, either in the early stage (from Day 1 to Day 3, group E) or late stage (from Day 8 to Day 12, group L). Control mice (group C) did not receive antibodies. On Day 14, mice were killed and the number and weight of endometriotic lesions were counted and weighed. Results: The number of endometriotic lesions was significantly less in group E in comparison with Group C and Group L. Weight per lesion did not differ between groups. Conclusion: Neutrophils are essential for the initial formation of endometriosis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Many other cells in its microenvironment. Platelets, neutrophils, macrophages, and recently nerve fibers all have been identified to be accessories to aid and abet the lesional development.
“Platelets21,23, neutrophils69, macrophages19,24, and recently nerve fibers25,26 all have been identified to be accessories to aid and abet the lesional development.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [69]
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
(1927) · PubMed Central · Cited by 1,008 · see citing works
(1984) · PubMed · Cited by 997 · see citing works
Ultraviolet-radiation-induced inflammation promotes angiotropism and metastasis in melanoma
Bald, T., Quast, T., Landsberg, J., Rogava, M., Glodde, N., Lopez-Ramos, D., Kohlmeyer, J., Riesenberg, S., van den Boorn-Konijnenberg, D., Hömig-Hölzel, C., et al. (2014) · Nature · doi:10.1038/nature13111 · Cited by 623 · see citing works
Tumor associated macrophages and neutrophils in cancer
Galdiero, M. R., Bonavita, E., Barajon, I., Garlanda, C., Mantovani, A., & Jaillon, S. (2013) · Immunobiology · doi:10.1016/j.imbio.2013.06.003 · Cited by 597 · see citing works
Bacci, M., Capobianco, A., Monno, A., Cottone, L., Di Puppo, F., Camisa, B., Mariani, M., Brignole, C., Ponzoni, M., Ferrari, S., et al. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.081011 · Cited by 458 · see citing works
Shamamian, P. E., Schwartz, J. D., Pocock, B. J. Z., Monea, S., Whiting, D., Marcus, S. G., & Mignatti, P. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.10014 · Cited by 352 · see citing works
Shen, M., Hu, P., Donskov, F. N., Wang, G., Liu, Q., & Du, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098259 · Cited by 348 · see citing works
McDonald, B., McAvoy, E. F., Lam, F., Gill, V., de la Motte, C., Savani, R., & Kubes, P. (2008) · Journal of Experimental Medicine · doi:10.1084/jem.20071765 · Cited by 345 · see citing works
Lin, Y., Lai, M.-D., Lei, H.-Y., & Wing, L.-Y. C. (2005) · Endocrinology · doi:10.1210/en.2005-0790 · Cited by 218 · see citing works
Role of CD44 and Hyaluronan in Neutrophil Recruitment
Khan, A. I., Kerfoot, S. M., Heit, B., Liu, L., Andonegui, G., Ruffell, B., Johnson, P., & Kubes, P. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.12.7594 · Cited by 195 · see citing works
Osuga, Y., Koga, K., Hirota, Y., Hirata, T., Yoshino, O., & Taketani, Y. (2010) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2010.00887.x · Cited by 189 · see citing works
Self-citationDendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis
Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep071 · Cited by 176 · see citing works
Ho, H., Chao, K., Chen, H., Wu, M., Yang, Y., & Lee, T.-Y. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135765 · Cited by 156 · see citing works
Hirata, T., Osuga, Y., Hamasaki, K., Yoshino, O., Ito, M., Hasegawa, A., Takemura, Y., Hirota, Y., Nose, E., Morimoto, C., et al. (2007) · Endocrinology · doi:10.1210/en.2007-0749 · Cited by 144 · see citing works
Self-citationMydel, P. M., Shipley, J. M., Adair-Kirk, T. L., Kelley, D. G., Broekelmann, T. J., Mecham, R. P., & Senior, R. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m706239200 · Cited by 115 · see citing works
Tabariès, S., Ouellet, V., Hsu, B. E., Annis, M., Rose, A. A. N., Meunier, L., Carmona, E., Tam, C. E., Mes-Masson, A., & Siegel, P. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0558-3 · Cited by 110 · see citing works
Nussler, A. K., Rénia, L., Pasquetto, V., Miltgen, F., Matile, H., & Mazier, D. (1993) · European Journal of Immunology · doi:10.1002/eji.1830230417 · Cited by 109 · see citing works
Neutrophil depletion retards endometrial repair in a mouse model
Kaitu’u‐Lino, T. J., Morison, N. B., & Salamonsen, L. A. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0358-2 · Cited by 103 · see citing works
Wojtasiak, M., Pickett, D. L., Tate, M. D., et al. (2010) · Journal of General Virology · doi:10.1099/vir.0.021915-0 · Cited by 95 · see citing works
Saiwai, H., Kumamaru, H., Ohkawa, Y., Kubota, K., Kobayakawa, K., Yamada, H., Yokomizo, T., Iwamoto, Y., & Okada, S. (2012) · Journal of Neurochemistry · doi:10.1111/jnc.12135 · Cited by 92 · see citing works
Defining the role of laminin-332 in carcinoma
Guess, C. M., & Quaranta, V. (2009) · Matrix Biology · doi:10.1016/j.matbio.2009.07.008 · Cited by 91 · see citing works
Milewski, Ł., Dziunycz, P., Barcz, E., Radomski, D. S., Roszkowski, P. I., Korczak-Kowalska, G., Kamiński, P., & Malejczyk, J. (2011) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2011.05.008 · Cited by 90 · see citing works
Takamura, M., Koga, K., Izumi, G., Hirata, T., Harada, M., Hirota, Y., Hiraike, O. W., Fujii, T., & Osuga, Y. (2015) · American Journal of Reproductive Immunology · doi:10.1111/aji.12426 · Cited by 85 · see citing works
Self-citationHirata, T., Osuga, Y., Yoshino, O., et al. (2005) · Human Reproduction · doi:10.1093/humrep/dei012 · Cited by 83 · see citing works
Self-citationDoi, K., Okamoto, K., Negishi, K., Suzuki, Y., Nakao, A., Fujita, T., Toda, A., Yokomizo, T., Kita, Y., Kihara, Y., et al. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.050634 · Cited by 78 · see citing works
Haber, E., Danenberg, H. D., Koroukhov, N., Ron‐El, R., Golomb, G., & Schachter, M. (2008) · Human Reproduction · doi:10.1093/humrep/den375 · Cited by 73 · see citing works
Association of neutrophil extracellular traps with endometriosis-related chronic inflammation
Berkes, E., Oehmke, F., Tinneberg, H.-R., Preissner, K. T., & Saffarzadeh, M. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.10.040 · Cited by 56 · see citing works
A potential role for colony-stimulating factor 1 in the genesis of the early endometriotic lesion
Jensen, J. R., Witz, C. A., Schenken, R. S., & TEKMAL, R. R. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.09.050 · Cited by 47 · see citing works
Itoh, H., Sashihara, T., Hosono, A., Kaminogawa, S., & Uchida, M. (2011) · Cytotechnology · doi:10.1007/s10616-010-9321-x · Cited by 47 · see citing works
Dendritic Cells Attenuate the Early Establishment of Endometriosis-Like Lesions in a Murine Model
Stanic, A. K., Kim, M., Styer, A. K., & Rueda, B. R. (2014) · Reproductive Sciences · doi:10.1177/1933719114525267 · Cited by 46 · see citing works
Yang, M., Jiang, C., Chen, H., Nian, Y., Zhimiao, B., & Ha, C. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0090-4 · Cited by 43 · see citing works
Takamura, M., Osuga, Y., Izumi, G., Yoshino, O., Koga, K., Saito, A., Hirata, T., Hirota, Y., Harada, M., Hasegawa, A., et al. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.07.1117 · Cited by 39 · see citing works
Self-citationUmezawa, M., Saito, Y., Tanaka-Hattori, N., et al. (2012) · Reproductive Sciences · doi:10.1177/1933719112450340 · Cited by 23 · see citing works
Cathepsin Protease Inhibition Reduces Endometriosis Lesion Establishment
Porter, K. M., Wieser, F. A., Wilder, C. L., Sidell, N., & Platt, M. O. (2015) · Reproductive Sciences · doi:10.1177/1933719115611752 · Cited by 20 · see citing works
Upregulation of gamma‐2 laminin‐332 in the mouse ear vesicant wound model
Chang, Y., Sabourin, C. L. K., Lu, S., Sasaki, T., Svoboda, K. K. H., Gordon, M. K., Riley, D. J., Casillas, R. P., & Gerecke, D. R. (2009) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.20275 · Cited by 19 · see citing works
Impaired Development of Early Endometriotic Lesions in CD44 Knockout Mice
Knudtson, J. F., TEKMAL, R. R., Santos, M. T., et al. (2015) · Reproductive Sciences · doi:10.1177/1933719115594022 · Cited by 18 · see citing works
Hyaluronic acid reagent suppressed endometriotic lesion formation in a mouse model
Hasegawa, A., Yoshino, O., Osuga, Y., et al. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.02.053 · Cited by 10 · see citing works
Self-citationStimulation of neutrophil production in CSF-1-responsive clones
Rothstein, G., Rhondeau, S., Peters, C., et al. (1988) · Blood · doi:10.1182/blood.v72.3.898.bloodjournal723898 · Cited by 10 · see citing works
Stimulation of neutrophil production in CSF-1-responsive clones
Rothstein, G., Rhondeau, S., Peters, C., et al. (1988) · Blood · doi:10.1182/blood.v72.3.898.898 · Cited by 9 · see citing works
Change profiles in matrix metalloproteinase-2 and -9 in induced endometriosis in mice
Chen, Q., Qiu, N., Pu, D., Zhou, Y., Li, T., & Yang, H. (2010) · Journal of Huazhong University of Science and Technology [Medical Sciences] · doi:10.1007/s11596-010-0211-4 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Main Theories on the Pathogenesis of Endometriosis
Lamceva, J., Uljanovs, R., & Strumfa, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054254 · Cited by 324 · see citing works
Qi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
- Authors
- Takamura, M., Koga, K., Izumi, G., Urata, Y., Nagai, M., Hasegawa, A., Harada, M., Hirata, T., Hirota, Y., Wada‐Hiraike, O., Fujii, T., & Osuga, Y.
- Affiliations
- The University of Tokyo (JP)
- Corresponding author
- Koga, Kaori
- ORCID
- Venue
- American Journal of Reproductive Immunology
- Publisher
- Wiley
- Published
- 2016-07-19
- Volume
- 76
- Issue
- 3
- Pages
- 193-198
- ISSN
- 0271-7352 (ISSN-L)
- 1046-7408
- 1600-0897
- OpenAlex
- W2498683695
- Cited by
- 53
- References
- 41
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 7 · 2023: 11 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 3 · 2018: 2 · 2017: 1 · 2016: 1 · 2014: 1
- FWCI
- 3.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Reproductive Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Health, Labour and Welfare
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, neutrophils, neutrophil depletion, neutrophil recruitment
- MeSH terms
- Animals, Antibodies, Endometriosis, Female, Mice, Inbred BALB C, Neutrophils, Mice
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