Macrophages Are Alternatively Activated in Patients with Endometriosis and Required for Growth and Vascularization of Lesions in a Mouse Model of Disease
Open accessAbstract
The mechanisms that sustain endometrial tissues at ectopic sites in patients with endometriosis are poorly understood. Various leukocytes, including macrophages, infiltrate endometriotic lesions. In this study, we depleted mouse macrophages by means of either clodronate liposomes or monoclonal antibodies before the injection of syngeneic endometrial tissue. In the absence of macrophages, tissue fragments adhered and implanted into the peritoneal wall, but endometriotic lesions failed to organize and develop. When we depleted macrophages after the establishment of endometriotic lesions, blood vessels failed to reach the inner layers of the lesions, which stopped growing. Macrophages from patients with endometriosis and experimental mice, but not nonendometriotic patients who underwent surgery for uterine leiomyomas or control mice, expressed markers of alternative activation. These markers included high levels of scavenger receptors, CD163 and CD206, which are involved in both the scavenging of hemoglobin with iron transfer into macrophages and the silent clearance of inflammatory molecules. Macrophages in both inflammatory liquid and ectopic lesions were equally polarized, suggesting a critical role of environmental cues in the peritoneal cavity. Adoptively transferred, alternatively activated macrophages dramatically enhanced endometriotic lesion growth in mice. Inflammatory macrophages effectively protected mice from endometriosis. Therefore, endogenous macrophages involved in tissue remodeling appear as players in the natural history of endometriosis, required for effective vascularization and ectopic lesion growth.
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Many non-endometriotic cells in the lesional microenvironment, such as platelets, macrophages, and nerve fibers, are actively involved in facilitating lesional development.
“many non-endometriotic cells in the lesional microenvironment, such as platelets21,23, macrophages19,24, and now nerve fibers25,26, are actively involved in facilitating 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 [24]
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 [24]
SP can directly induce M2 polarization of inflammatory macrophages, which participate in tissue repair and promote lesion growth and fibrogenesis in endometriosis.
“SP can also directly induce M2 polarization of inflammatory macrophages, which participate in tissue repair75 and are involved in promoting lesion growth and fibrogenesis in endometriosis76,77.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [76]
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- Authors
- Bacci, M., Capobianco, A., Monno, A., Cottone, L., Di Puppo, F., Camisa, B., Mariani, M., Brignole, C., Ponzoni, M., Ferrari, S., Panina-Bordignon, P., Manfredi, A. A., & Rovere-Querini, P.
- Affiliations
- Vita-Salute San Raffaele University (IT)
- Istituto Giannina Gaslini (IT)
- ORCID
- Venue
- The American Journal of Pathology
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 175
- Issue
- 2
- Pages
- 547-556
- ISSN
- 0002-9440 (ISSN-L)
- PMC
- PMC2716955
- OpenAlex
- W1998696411
- Cited by
- 458
- References
- 50
- Citations by year
- 2026: 33 · 2025: 48 · 2024: 42 · 2023: 34 · 2022: 35 · 2021: 61 · 2020: 33 · 2019: 26 · 2018: 30 · 2017: 15 · 2016: 20 · 2015: 17 · 2014: 24 · 2013: 10 · 2012: 9
- FWCI
- 11.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal Of Pathology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- Funders
- Ministero della Salute
- Ministero dell’Istruzione, dell’Università e della Ricerca
- Associazione Italiana per la Ricerca sul Cancro
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, macrophages, alternative macrophage activation, macrophage depletion, clodronate liposomes, CD163, CD206, scavenger receptors, ectopic endometrium, adoptive transfer, peritonitis, tissue remodeling
- MeSH terms
- Animals, Disease Models, Animal, Endometriosis, Female, Macrophage Activation, Mice, Inbred BALB C, Neovascularization, Pathologic, Macrophages, Peritoneal, Mice
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