Cited by 534Wound Healing and TreatmentsImmune cells in cancerAngiogenesis and VEGF in Cancer

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CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair

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Willenborg, Sebastian, Lucas, Tina, van Loo, Geert, Knipper, Johanna A., Krieg, Thomas, Haase, Ingo, Brachvogel, Bent, Hammerschmidt, Matthias, Nagy, Andras, Ferrara, Napoleone, Pasparakis, Manolis, Eming, Sabine A.·2012·Blood

DOI 10.1182/blood-2012-01-403386

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Abstract

Monocytes/macrophages are critical in orchestrating the tissue-repair response. However, the mechanisms that govern macrophage regenerative activities during the sequential phases of repair are largely unknown. In the present study, we examined the dynamics and functions of diverse monocyte/macrophage phenotypes during the sequential stages of skin repair. By combining the analysis of a new CCR2-eGFP reporter mouse model with conditional mouse mutants defective in myeloid cell-restricted CCR2 signaling or VEGF-A synthesis, we show herein that among the large number of inflammatory CCR2(+)Ly6C(+) macrophages that dominate the early stage of repair, only a small fraction strongly expresses VEGF-A that has nonredundant functions for the induction of vascular sprouts. The switch of macrophage-derived VEGF-A during the early stage of tissue growth toward epidermal-derived VEGF-A during the late stage of tissue maturation was critical to achieving physiologic tissue vascularization and healing progression. The results of the present study provide new mechanistic insights into CCR2-mediated recruitment of blood monocyte subsets into damaged tissue, the dynamics and functional consequences of macrophage plasticity during the sequential repair phases, and the complementary role of macrophage-derived VEGF-A in coordinating effective tissue growth and vascularization in the context of tissue-resident wound cells. Our findings may be relevant for novel monocyte-based therapies to promote tissue vascularization.

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A biodegradable synthetic graft for small arteries matches the performance of autologous vein in rat carotid arteries
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Biomaterials-assisted spheroid engineering for regenerative therapy
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Col6a1 Null Mice as a Model to Study Skin Phenotypes in Patients with Collagen VI Related Myopathies: Expression of Classical and Novel Collagen VI Variants during Wound Healing
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BackgroundMethod
An In Vitro Model of Angiogenesis during Wound Healing Provides Insights into the Complex Role of Cells and Factors in the Inflammatory and Proliferation Phase
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Background
Salt increases monocyte CCR2 expression and inflammatory responses in humans
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BackgroundMethod
Low‐grade inflammatory polarization of monocytes impairs wound healing
Yuan, R., Geng, S., Chen, K., Diao, N., Chu, H. W., & Li, L. (2015) · The Journal of Pathology · doi:10.1002/path.4680 · Cited by 49
“In the context of wound healing, although a causal connection between the sustained presence of pro-inflammatory monocytes and compromised wound repair is well established [5,7,27,28], the cause and mechanism responsible for the establishment and dynamic ’memory’ of low-grade inflammatory monocytes were not known.”
BackgroundInfluential
Unbiased Analysis of the Impact of Micropatterned Biomaterials on Macrophage Behavior Provides Insights beyond Predefined Polarization States
Singh, S., Awuah, D., Rostam, H. M., Emes, R. D., Kandola, N. K., Onion, D., Htwe, S. S., Rajchagool, B., Cha, B.-H., Kim, D. J., et al. (2017) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.7b00104 · Cited by 51
Recruitment of dendritic cell progenitors to foci of influenza A virus infection sustains immunity
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Dynamic trafficking patterns of IL-17-producing γδ T cells are linked to the recurrence of skin inflammation in psoriasis-like dermatitis
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Global Characteristics and Dynamics of Single Immune Cells After Myocardial Infarction
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Adipose tissue plasticity and the pleiotropic roles of BMP signaling
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Bone Healing Gone Wrong: Pathological Fracture Healing and Non-Unions—Overview of Basic and Clinical Aspects and Systematic Review of Risk Factors
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Dermal Drivers of Injury-Induced Inflammation: Contribution of Adipocytes and Fibroblasts
Cooper, P. O., Haas, M. R., Noonepalle, S. K. R., & Shook, B. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041933 · Cited by 70
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Nrg1/ErbB signaling‐mediated regulation of fibrosis after myocardial infarction
Shiraishi, M., Yamaguchi, A., & Suzuki, K. (2022) · The FASEB Journal · doi:10.1096/fj.202101428rr · Cited by 48
Placental Growth Factor Contributes to Liver Inflammation, Angiogenesis, Fibrosis in Mice by Promoting Hepatic Macrophage Recruitment and Activation
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Macrophage-Mediated Tissue Vascularization: Similarities and Differences Between Cornea and Skin
Hadrian, K., Willenborg, S., Bock, F., Cursiefen, C., Eming, S., & Hos, D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.667830 · Cited by 44
“While the role of specific macrophage populations in corneal neovascularization is not entirely resolved, blood-derived inflammatory CCR2Ly6C monocytes/macrophages were identified as the critical source of VEGF−A in skin wounds (29).”
BackgroundInfluential
Unraveling the potential of 3D bioprinted immunomodulatory materials for regulating macrophage polarization: State-of-the-art in bone and associated tissue regeneration
Dutta, S. D., Patil, T. V., Ganguly, K., Randhawa, A., & Lim, K. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.05.014 · Cited by 52
Macrophage phenotype in the epigallocatechin-3-gallate (EGCG)-modified collagen determines foreign body reaction
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“Immunofluorescence showed that the expression of iNOS in E‐Col was downregulated compared with that of Col, whereas expression of CD206 was upregulated, which indicated that EGCG‐modified collagen membrane could promote M2 macrophage polarization and inhibit M1 macrophage polarization.”
BackgroundInfluential
Monocytes as Endothelial Progenitor Cells (EPCs), Another Brick in the Wall to Disentangle Tumor Angiogenesis
Lopes‐Coelho, F., SILVA, F. A. B. N. D., Gouveia-Fernandes, S., Martins, C., Lopes, N., Domingues, G., Brito, C., Almeida, A. M., Pereira, S. A., & Serpa, J. (2020) · Cells · doi:10.3390/cells9010107 · Cited by 47
“In vivo and in vitro targeting of Tie2-monocytes decreases angiogenesis by abrogating EC proliferation [13–15] and an in vivo CCR2 (chemokine (C–C motif) receptor 2) knockout impairs monocytes recruitment and VEGFA (also named VEGF, vascular endothelial growth factor) expression, accompanied by a reduction in the angi…”
Background
On diabetic foot ulcer knowledge gaps, innovation, evaluation, prediction markers, and clinical needs
Schmidt, B. M., Holmes, C., Najarian, K., Gallagher, K. K., Haus, J. M., Shadiow, J., Ye, W., Ang, L. P., Burant, A., Baker, N., et al. (2022) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2022.108317 · Cited by 51
Pivotal role for skin transendothelial radio-resistant anti-inflammatory macrophages in tissue repair
Barreiro, O., Cibrián, D., Clemente, C., Álvarez, D., Moreno, V., Valiente, Í., Bernad, A., Vestweber, D., Arroyo, A. G., Martı́n, P., et al. (2016) · eLife · doi:10.7554/elife.15251 · Cited by 46
“…nature of STREAMs to deplete skin radio-sensitive macrophages by lethal g-irradiation and prevented their replenishment by limiting the affluence of peripheral blood monocytes after reconstitution with Ccr2-/- hematopoietic progenitors (Willenborg et al., 2012) (Figure 10—figure supplement 1E).”
BackgroundInfluential
Macrophages Regulate Unilateral Ureteral Obstruction-Induced Renal Lymphangiogenesis through C-C Motif Chemokine Receptor 2–Dependent Phosphatidylinositol 3-Kinase-AKT–Mechanistic Target of Rapamycin Signaling and Hypoxia-Inducible Factor-1α/Vascular Endothelial Growth Factor-C Expression
Guo, Y., Zhang, M., Wang, F., Pei, G., Sun, F., Zhang, Y., He, X., Wang, Y., Song, J., Zhu, F., et al. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.04.007 · Cited by 45
The regenerative potential of skin and the immune system
Tsepkolenko, A., Цепколенко, В. О., Dash, S., Mishra, A., Bader, A., Melerzanov, A., & Giri, S. (2019) · Clinical Cosmetic and Investigational Dermatology · doi:10.2147/ccid.s196364 · Cited by 47
“For instance, macrophages induce VEGF-mediated neoangiogenesismediating formation of neoepithelium at the site of wound bed formation as observed in reporter mice.(41) Taken together, these findings demonstrate the critical role of macrophages and their interplay with monocytes”
Background
Regulation of Macrophage Foam Cell Formation During Nitrogen Mustard (NM)-Induced Pulmonary Fibrosis by Lung Lipids
Venosa, A., Smith, L. C., Murray, A., Banota, T., Gow, A. J., Laskin, J. D., & Laskin, D. L. (2019) · Toxicological Sciences · doi:10.1093/toxsci/kfz187 · Cited by 46
“A number of reports have described a subset of anti-inflammatory M2 macrophages that coexpresses CCR2 and CX3CR1 and exhibits enhanced mobilization from the periphery to inflammatory sites (Kohno et al., 2015; Schmall et al., 2015; Willenborg et al., 2012).”
Background
Epigenetic Regulation of TLR4 in Diabetic Macrophages Modulates Immunometabolism and Wound Repair
Davis, F. M., denDekker, A. D., Kimball, A., Joshi, A., Azzouny, M. E., Wolf, S., Andrea, T., Lipinski, J. H., Gudjonsson, J. E., Xing, X., et al. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901263 · Cited by 49
“the mandatory drive for acute inflammation, recruiting additional leukocytes, and promoting tissue/pathogen destruction (4, 6, 9, 10).”
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Tibial cortex transverse transport promotes ischemic diabetic foot ulcer healing via enhanced angiogenesis and inflammation modulation in a novel rat model
Qin, W., Liu, K., Su, H., Hou, J., Yang, S., Pan, K., Yang, S., Liu, J., Zhou, P., Lin, Z., et al. (2024) · European journal of medical research · doi:10.1186/s40001-024-01752-4 · Cited by 45
A modified collagen gel dressing promotes angiogenesis in a preclinical swine model of chronic ischemic wounds
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“Macrophages secrete pro-angiogeneic factors such as VEGF.(37) Signaling between endothelial cellsurface receptors and ECM molecules, such as collagen, stimulates migration and proliferation of endothelial cells.”
Background
The diversity of myeloid immune cells shaping wound repair and fibrosis in the lung
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“…tissue in two waves: the first wave involves an influx of classical Ly6Chi CCR2+ monocytes contributing to inflammation and angiogenesis followed by a later influx of nonclassical Ly6Clow CX3CR1+monocytes that contribute to scar formation (Ishida, Gao, & Murphy, 2008; Willenborg et al., 2012).”
Background
Titanium or Biodegradable Osteosynthesis in Maxillofacial Surgery? In Vitro and In Vivo Performances
Gareb, B., van Bakelen, N. B., Vissink, A., Bos, R. R. M., & van Minnen, B. (2022) · Polymers · doi:10.3390/polym14142782 · Cited by 48
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Human adipose tissue-resident monocytes exhibit an endothelial-like phenotype and display angiogenic properties
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Synergistic interactions of blood-borne immune cells, fibroblasts and extracellular matrix drive repair in an in vitro peri-implant wound healing model
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“VEGF is released from polymorphonuclear cells (PMNs, such as neutrophils) and macrophages 15 during the early tissue maturation phase 50 , and mediates the recruitment of endothelial progenitor cells, endothelial cell proliferation, survival, migration and differentiation 51,52 .”
Cryptosporidium parvumincreases intestinal permeability through interaction with epithelial cells and IL-1β and TNFα released by inflammatory monocytes
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Background
The Vitamin D Receptor Regulates Tissue Resident Macrophage Response to Injury.
Song, L.-G., Papaioannou, G., Zhao, H., Luderer, H. F., Miller, C. M., Dall’Osso, C., Nazarian, R., Wagers, A., & Demay, M. (2016) · Endocrinology · doi:10.1210/en.2016-1474 · Cited by 40
lncRNA-H19 in Fibroblasts Promotes Wound Healing in Diabetes
Yu, P., Guo, J., Li, J., Xiao Hua, S. H. I., Xu, N., Jiang, Y., Chen, W., & Hu, Q. (2022) · Diabetes · doi:10.2337/db21-0724 · Cited by 49
The potential role of platelets in the consensus molecular subtypes of colorectal cancer
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CC Chemokine Family Members’ Modulation as a Novel Approach for Treating Central Nervous System and Peripheral Nervous System Injury—A Review of Clinical and Experimental Findings
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“Importantly, CCR2 activation promotes angiogenesis [247] and fracture healing [248] and decreases amyloid plaque formation in Alzheimer’s disease models through macrophage-mediated phagocytosis [249,250].”
Background

Authors: Willenborg, S., Lucas, T., van Loo, G., Knipper, J. A., Krieg, T., Haase, I., Brachvogel, B., Hammerschmidt, M., Nagy, A., Ferrara, N., Pasparakis, M., & Eming, S. A.
Affiliations: University of Cologne (DE)
Department for Molecular Biomedical Research, Vlaams Instituut voor Biotechnologie, Ghent, Belgium;
Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, ON;
Genentech (US)
Corresponding author: Willenborg, Sebastian
Lucas, Tina
ORCID: Willenborg, Sebastian
Knipper, Johanna A.
Krieg, Thomas
Haase, Ingo
Brachvogel, Bent
Hammerschmidt, Matthias
Pasparakis, Manolis
Eming, Sabine A.
Venue: Blood
Publisher: American Society of Hematology
Published: 2012-07-19
Volume: 120
Issue: 3
Pages: 613-625
ISSN: 0006-4971 (ISSN-L)
1528-0020
DOI: 10.1182/blood-2012-01-403386
OpenAlex: W2065145765
Cited by: 534
References: 40
Citations by year: 2026: 29 · 2025: 43 · 2024: 38 · 2023: 55 · 2022: 46 · 2021: 40 · 2020: 40 · 2019: 34 · 2018: 38 · 2017: 43 · 2016: 32 · 2015: 29 · 2014: 37 · 2013: 24 · 2012: 5
FWCI: 32.15
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Blood (publishedVersion)
PubMed (publishedVersion)
Ghent University Academic Bibliography (Ghent University) (submittedVersion)
Funders: European Commission (2007–2013, 214402)
Deutsche Forschungsgemeinschaft
Universiteit Gent
Topics: Health Sciences › Medicine › Surgery › Wound Healing and Treatments
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: CCR2, macrophage plasticity, VEGF-A, angiogenesis, skin wound healing, tissue repair, monocyte recruitment, vascular sprouting, tissue vascularization
MeSH terms: Animals, Cells, Cultured, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Monocytes, Regeneration, Skin, Wound Healing, Signal Transduction, Macrophages, Peritoneal, Neovascularization, Physiologic, Gene Expression Profiling, Myeloid Cells, Vascular Endothelial Growth Factor A, Green Fluorescent Proteins, Mice, Receptors, CCR2

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CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair

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