Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis
Open accessAbstract
Beyond its role in immunity, complement mediates a wide range of functions in the context of morphogenetic or tissue remodeling processes. Angiogenesis is crucial during tissue remodeling in multiple pathologies; however, the knowledge about the regulation of neovascularization by the complement components is scarce. Here we studied the involvement of complement in pathological angiogenesis. Strikingly, we found that mice deficient in the central complement component C3 displayed increased neovascularization in the model of retinopathy of prematurity (ROP) and in the in vivo Matrigel plug assay. In addition, antibody-mediated blockade of C5, treatment with C5aR antagonist, or C5aR deficiency in mice resulted in enhanced pathological retina angiogenesis. While complement did not directly affect angiogenesis-related endothelial cell functions, we found that macrophages mediated the antiangiogenic activity of complement. In particular, C5a-stimulated macrophages were polarized toward an angiogenesis-inhibitory phenotype, including the up-regulated secretion of the antiangiogenic soluble vascular endothelial growth factor receptor-1. Consistently, macrophage depletion in vivo reversed the increased neovascularization associated with C3- or C5aR deficiency. Taken together, complement and in particular the C5a-C5aR axes are potent inhibitors of angiogenesis.
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The anaphylatoxins C3a and C5a have been found to enhance laser-induced CNV in some cases, but may have anti-angiogenic properties in mouse models of retinal hypoxia through the stimulation of mononuclear phagocytes to secrete soluble VEGF receptor 1 that inhibits VEGF.
“For instance, the anaphylatoxins C3a and C5a have been found to enhance laser-induced CNV in some cases, but may have anti-angiogenic properties in mouse models of retinal hypoxia through the stimulation of mononuclear phagocytes to secrete soluble VEGF receptor 1 that inhibits VEGF [169,170].”
From Bruch’s Membrane: A Key Consideration with Complement-Based Therapies for Age-Related Macular Degeneration (2023) · cites this paper as [170]
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Kim, B. J., Mastellos, D. C., Li, Y., Dunaief, J. L., & Lambris, J. D. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100936 · Cited by 91 · see citing works
Self-citationComplement anaphylatoxin C3a is a potent inducer of embryonic chick retina regeneration
Haynes, T., Luz-Madrigal, A., Reis, E. S., Echeverri Ruiz, N. P., Grajales-Esquivel, E., Tzekou, A., Tsonis, P. A., Lambris, J. D., & Del Rio-Tsonis, K. (2013) · Nature Communications · doi:10.1038/ncomms3312 · Cited by 87 · see citing works
Self-citationThe role of the immune system in central nervous system plasticity after acute injury
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A Novel Function of Junctional Adhesion Molecule-C in Mediating Melanoma Cell Metastasis
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Self-citationPlatelets induce apoptosis via membrane-bound FasL
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Self-citationComplement deficiency promotes cutaneous wound healing in mice
Rafail, S., Kourtzelis, I., Foukas, P. G., Markiewski, M. M., DeAngelis, R. A., Guariento, M., Ricklin, D., Grice, E. A., & Lambris, J. D. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402354 · Cited by 72 · see citing works
“Apart from the role of complement on immune cells, recent work has also shown the involvement of complement in other key processes playing roles in wound healing, such as fibroblast migration and activation (40), angiogenesis (9, 21), and coagulation (41).”
BackgroundMethodResultSelf-citationComplement links platelets to innate immunity
Nording, H., & Langer, H. F. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2018.01.003 · Cited by 75 · see citing works
Self-citationBurwick, R. M., & Feinberg, B. B. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.038 · Cited by 77 · see citing works
Abnormal Complement Activation and Inflammation in the Pathogenesis of Retinopathy of Prematurity
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Implications of genetic variation in the complement system in age-related macular degeneration
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Targeting complement-mediated immunoregulation for cancer immunotherapy
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Complement activation in animal and human pregnancies as a model for immunological recognition
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A Novel Role of Complement in Retinal Degeneration
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The Complement System Is Critical in Maintaining Retinal Integrity during Aging
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Complement activation in the context of stem cells and tissue repair
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Wang, C., Lee, Y., Chang, C., Lin, Y., Liou, Y.-A., Hsu, P.-C., Chang, C.-C., Sai, A., Wang, C., & Chao, T. (2022) · Cancers · doi:10.3390/cancers14071651 · Cited by 57 · see citing works
Obesity “complements” preeclampsia
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The Complement System in Inflammatory Bowel Disease
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Complement factor C5a as mast cell activator mediates vascular remodelling in vein graft disease
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Terminal Complement Activation in Preeclampsia
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Complement regulation in the eye: implications for age-related macular degeneration
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Anaphylatoxins coordinate innate and adaptive immune responses in allergic asthma
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The C5a/C5a receptor 1 axis controls tissue neovascularization through CXCL4 release from platelets
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The dual role of complement in cancer and its implication in anti-tumor therapy
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Complement 5a‐mediated trophoblasts dysfunction is involved in the development of pre‐eclampsia
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Self-citationExpression of anaphylatoxin receptors on platelets in patients with coronary heart disease
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Self-citationInhibition of the alternative complement pathway preserves photoreceptors after retinal injury
Sweigard, J. H., Matsumoto, H., Smith, K. E., Kim, L. A., Paschalis, E. I., Okonuki, Y., Castillejos, A. G., Kataoka, K., Hasegawa, E., Yanai, R., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aab1482 · Cited by 48 · see citing works
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Angiogenic and Antiangiogenic Chemokines
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The non-inflammatory role of C1q during Her2/neu-driven mammary carcinogenesis
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Elevated Soluble Flt1 Inhibits Endothelial Repair in PR3-ANCA–Associated Vasculitis
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C5L2 receptor disruption enhances the development of diet-induced insulin resistance in mice
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Self-citationCharacterization of the LPS-induced inflammation of the adrenal gland in mice
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Self-citationThe Role of Chemoattractant Receptors in Shaping the Tumor Microenvironment
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Urinary Excretion of C5b‐9 is Associated With the Anti‐Angiogenic State in Severe Preeclampsia
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The alternative complement pathway regulates pathological angiogenesis in the retina
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Assessment of blood-brain barrier integrity and neuroinflammation in preeclampsia
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Complement C3a promotes proliferation, migration and stemness in cutaneous squamous cell carcinoma
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The Role of Complement in Angiogenesis
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Complement Involvement in Neovascular Ocular Diseases
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Self-citationRole of NOD- like Receptors in Glioma Angiogenesis: Insights into future therapeutic interventions
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Thiol pathways in the regulation of tissue factor prothrombotic activity
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Complement involvement in kidney diseases: From physiopathology to therapeutical targeting
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The role of complement in the tumor microenvironment
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Complement Activation in Placental Malaria
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- Authors
- Langer, H. F., Chung, K.-J., Orlova, V. V., Choi, E. Y., Kaul, S., Kruhlak, M. J., Alatsatianos, M., DeAngelis, R. A., Roche, P. A., Magotti, P., Li, X., Economopoulou, M., Rafail, S., Lambris, J. D., & Chavakis, T.
- Affiliations
- National Institutes of Health (US)
- University of Pennsylvania (US)
- Corresponding author
- Lambris, John D.
- Chavakis, Triantafyllos
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2010-11-25
- Volume
- 116
- Issue
- 22
- Pages
- 4395-4403
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC2996109
- OpenAlex
- W2165915271
- Cited by
- 176
- References
- 58
- Citations by year
- 2025: 8 · 2024: 8 · 2023: 9 · 2022: 9 · 2021: 8 · 2020: 9 · 2019: 13 · 2018: 15 · 2017: 8 · 2016: 13 · 2015: 16 · 2014: 12 · 2013: 16 · 2012: 14
- FWCI
- 6.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Blood (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Site cant be reached (submittedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (R01CA112162, CA-112162)
- National Institute of Allergy and Infectious Diseases (AI 068730, P01AI068730)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Complement system in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- complement system, neovascularization, pathological angiogenesis, complement C3, C5a, C5a receptor, retinopathy of prematurity, macrophages, macrophage polarization, soluble VEGFR1, antiangiogenic activity, innate immunity, tissue remodeling
- MeSH terms
- Animals, Cell Line, Complement C3, Complement C5, Humans, Immunity, Innate, Infant, Newborn, Macrophages, Mice, Inbred C57BL, Neovascularization, Pathologic, Retina, Retinopathy of Prematurity, Complement C5a, Gene Deletion, Cell Culture Techniques, Vascular Endothelial Growth Factors, Receptor, Anaphylatoxin C5a, Mice
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