New Angiogenic Regulators Produced by TAMs: Perspective for Targeting Tumor Angiogenesis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Angiogenesis-Associated Factors Secreted by TAMs
2.1. Soluble Mediators of Cell-Cell Interactions
2.1.1. S100A Family
Factors Regulating Angiogenesis | Pro- or Anti-Angiogenic Ability | Indirect Action Mediated by TAMs | Direct Action on ECs |
---|---|---|---|
S100A family | |||
S100A4 | Pro-angiogenic | Not shown | Induces motility, migration of ECs, formation of new blood vessel in vitro [29,30,32]. |
S100A7 | Pro-angiogenic | Not shown | Induces EC proliferation, migration and tube formation in vitro [36]. |
S100A8 | Pro-angiogenic | Not shown | Induces EC proliferation and migration, and tube formation in vitro [38]. |
S100A9 | |||
S100A10 | Pro-angiogenic | Not shown | Activates ECs invasion and angiogenesis in vivo [40]. |
SEMA family | |||
SEMA3A | Anti-angiogenic | Suppresses angiogenesis via accumulation of M1-like macrophages in tumor in vivo [42]. | Suppresses adhesion and migration of human ECs in vitro [43] and decreases average number of blood vessels in vivo [44]. |
Pro-angiogenic | Induces angiogenesis by increasing TAM infiltration in hypoxic conditions in vivo [45]. | ECs involved in neo-vessel sprouting secrete SEMA3A [43]. | |
SEMA3F | Anti-angiogenic | Not shown | Inhibits EC adhesion and migration in vitro [43], decreases number of CD31+ cells in vivo [46]. |
SEMA3E | Anti-angiogenic | Induces pro-inflammatory polarization of macrophages [47]. | Impairs tumor-induced blood vessel invasion into the angioreactors [48], decreases the number of filopodium-extending tip cells, disorganized vasculature [48] and decreases newly formed blood microvessels in vivo [49]. |
SEMA4A | Anti-angiogenic | Not shown | Suppresses EC migration and tube formation in vitro and decreases newly formed blood microvessels in vivo [49,50]. Suppressed VEGF-A–induced formation of new blood vessels in CAM assay [51]. |
Pro-angiogenic | Stimulates expression and secretion of VEGF-A in macrophages [51]. SEMA4A-treated macrophages promote EC migration in vitro and increases vessel number and vessel branching in vivo [51] | Not shown | |
SEMA4D | Pro-angiogenic | TAMs are a main source of SEMA4D in breast cancer [52]. | Induces EC migration and tube formation in vitro [53] and increases vessel formation in vivo [52,53]. |
SEMA6A | Pro-angiogenic | Not shown | Increases EC viability and growth in vitro, enhances network complexity and increases the number of vesel branching in vivo [54]. |
Chitinase-like proteins | |||
YKL-39 | Pro-angiogenic | Increases monocyte recruitment. TAMs are a main source of YKL-39 in breast cancer [55]. | Induces EC tube formation in vitro [55]. |
YKL-40 | Pro-angiogenic | Not shown | Induces EC migration and spreading in vitro [56], and increases vascularisation in vivo [57,58]. |
Regulators of cell-matrix interactions | |||
OPN | Pro-angiogenic | Stimulates angiogenesis via TAM recruitment in vivo [59]. | Promotes EC junctional destabilization, actin polymerization and EC motility in vitro and increases MVD in vivo [60]. |
SPARC | Anti-angiogenic | Inhibits angiogenesis via suppression of TAM recruitment in vivo [61]. | Inhibits EC migration and vessel formation in vitro, decreases vessel number, and promotes disruption of the vascular basement membrane in vivo [62,63,64]. |
Other important angiogenesis regulators | |||
Tie2-receptor | Pro-angiogenic | TEMs induce tube formation and produce pro-angiogenic factors [65]. | Promotes EC quiescence and vascular maturation in vitro [66]. |
COX-2 | Pro-angiogenic | Enhances production of pro-angiogenic factors from TAMs [67]. | Promotes EC migration, invasion and tube formation in vitro [59,68,69]. |
2.1.2. SEMA Family
2.1.3. Chitinase-Like Proteins
2.2. Regulators of Cell-Matrix Interactions
2.2.1. Osteopontin (SPP1)
2.2.2. Anti-Angiogenic Protein SPARC (Osteonectin)
2.3. Receptors
Tie2-Positive Macrophages and Monocytes
2.4. Intracellular Enzymes
COX-2
Purified Factor | Source | Angiogenic Assay | Working Concentration | Angiogenic Effect | Reference |
---|---|---|---|---|---|
S100A4 | Retrovirus-infected CSML0 cells | Cell motility assay | 0.5 μM | Activates | [29] |
S100A4 | HCT-116 cell line | Migration assay | 3 µM | Activates | [30] |
S100A7 | Abnova, catalog number is not specified | Proliferation, migration and tube formation assay | 1 μg/mL | Activates | [36] |
S100A8 | Cyclex Co. Ltd., catalog number is not specified | Tube formation, proliferation and migration assay | 10 μg/mL | Activates | [38] |
S100A9 | Cyclex Co. Ltd., catalog number is not specified | Tube formation, proliferation and migration assay | 10 μg/mL | Activates | [38] |
SEMA3A | R&D systems, catalog number is not specified | Adhesion and migration assay | 200–700 ng/mL | Inhibits | [43] |
SEMA3A | R&D systems, catalog number is not specified | CAM assay | 50 μg/mL | Inhibits | [43] |
SEMA3E | R&D systems, catalog number is not specified | DIVAA | 100 ng/mL | Inhibits | [48] |
SEMA3E | COS-7 cells | CAM assay | 100 nmol/L | Inhibits | [49] |
SEMA4A | COS-7 cells | CAM assay | 100 nmol/L | Inhibits | [49] |
YKL-39 | Sino Biological Inc, catalog number is not specified | Tube formation assay | 100 ng/mL | Activates | [55,87] |
YKL-40 | E. coli | Migration and tube formation assay | 100 ng/mL | Activates | [58] |
SPP1 | Not indicated | Vascular permeability assays | 10−10 M | Activates | [60] |
SPARC peptides FSEN and FSEC | Chemically synthesized | Migration assay and matrigel plug assay | 10 μM | Inhibits | [120] |
CCL18 | Not indicated | Tube formation assay | 20 ng/mL | Activates | [155] |
2.5. Other Pro-Angiogenic Factors Produced by Macrophages
2.5.1. Hypoxia-Induced Factors
2.5.2. Chemokines and Cytokines
2.5.3. Non-Coding RNA
3. Genetic and Posttranscriptional Alterations in Angiogenic Factors in Cancer
4. Perspectives for Anti-Angiogenic Therapy: Single and Combination Therapeutic Approaches
4.1. The Effect of Direct Inhibitors on TAM Amount and Repolarization
4.2. Indirect Inhibitors of Angiogenesis and TAMs
4.2.1. Bevacizumab
4.2.2. Receptor Tyrosine Kinase (RTK) Inhibitors
4.2.3. Celecoxib (Anti-COX2)
Therapeutic Drug/Combination | Targets | Macrophage Activity | Experimental Model |
---|---|---|---|
Bevacizumab | mAb against VEGF | Increases amount of M2-like TAMs after treatment | Breast cancer and glioblastoma model, patients with glioblastoma [229,231,232] |
CrossMab, A2V | mAb against Ang-2/VEGF | Diminishes MVD and tumor growth, and induces prolonged survival, induces re-programming of pro-tumor M2 TAMs to M1-like TAMs | Mice bearing orthotopic syngeneic (Gl261) or human (MGG8) gioblastoma xenografts [233] |
Bevacizumab plus CCL2 inhibitor (mNOX-E36) | mAb against VEGF+CCL2 inhibitor | Decreases the recruitment of TAMs, tumor volume and blood volume | CCL2-expressing rat glioblastoma multiforme model [236] |
Bevacizumab plus OLA-PEG | mAb against VEGF+CXCL-12 inhibitor | Reduces accumulation of CD68+ TAMs and increases the survival of tumor-bearing mice | Orthotopic G12 human glioblastoma model [237] |
Bevacizumab plus Altiratinib | mAb against VEGF+inhibitor of MET/TIE2/VEGFR2 | Reduces tumor volume, invasiveness, MVD, and Tie2+/F4/80+ macrophage infiltration | Glioblastoma mouse model [238] |
Triple inhibition (anti-CD40, anti-VEGF-A and anti-Ang2) | anti-CD40, anti-VEGF-A and anti-Ang2 | Promotes pro-inflammatory macrophage skewing, decreasing the proportion of CD206hiCD11clow M2-like TAMs and increasing the M1/M2 ratio, and facilitates tumor rejection | Murine tumor models of colon cancer and melanoma [239] |
Axitinib | TKR inhibitor | Reduces tumor growth, decreases number of TAMs | Subcutaneous MC38 and LLC mouse models [240] |
Cediranib plus MEDI3617 (an anti-Ang-2–neutralizing antibody) | VEGFR inhibitor+anti-Ang2 | Reduces tumor growth, induces morphological normalization and TAM-mediated improved survival | Murine glioblastoma models [234] |
Cetuximab | mAb against EGFR | Reduces the number of CD206+F4/80+ TAMs, increases expression of M1-like markers and decreases expression of M2-like markers | AOM/DSS-induced colorectal cancer mouse model [241], modeled TAMs, treated with conditioned medium of colon cancer cells in vitro [241,242] |
Cetuximab-targeted gold nanorods (CTX-AuNR) plus NIR irradiation | mAb against EGFR | Enhances ROS generation, and re-programms TAMs to the anti-tumor M1 phenotype | TAM-embedded breast cancer BT-20 spheroids [243] |
Celecoxib | COX-2 inhibitor | Changes TAM phenotype from M2 to M1 | ApcMin/+ mouse polyps [272] |
Celecoxib plus IFNγ | COX-2 inhibitor | Decreases MVD, increases amount of CD68+iNOS+ M1 macrophages and decreases amount of CD68+ARG1+ M2 macrophages | Mouse model of LLC [273] |
Dasatinib | TKR inhibitor | Inhibites M2 polarization of TAMs | In vitro [244,245] |
Mannosylated mixed micelles delivered dasatinib (DAS-MMic) | TKR inhibitor | Eliminates F4/80+ TAMs, decreases CD31+ angiogenesis | 4T1 breast cancer model [246] |
Etoricoxib | COX-2 inhibitor | Suppresses MVD and the infiltration of macrophages | Mouse model of melanoma [59] |
Erlotinib plus bevacizumab/IFN (BVZ/IFN/ERLO) | EGFR inhibitor+anti-VEGF | Inhibites tumor growth, promotes blood vessel normalization, reduces lymphatic network, and inhibites M2 polarization | Mouse xenografts of RCC [247] |
Erlotinib derivative, TD-92 | EGFR inhibitor | Reduces the number of pro-tumorigenic CD11b+F4/80+ TAMs | LLC tumor model [248] |
Imatinib | TKR inhibitor | Prevents M2-like polarization of BMDMs, reduces amount of M2-polarized TAMs | LLC mouse model [249] |
Imatinib plus anti-CD40 antibody | TKR inhibitor+anti-CD40 | Redirects TAMs to antitumor M1 phenotype | Mouse model of GIST [250] |
Lenvatinib | RTK inhibitor | Decreases the number of CD31+ tumor blood vessels, diminishes the amount of CD11b+F4/80+ TAMs and increases the percentage of activated CD8+ T cells | CT26 colon cancer mouse model [252] |
Lenvatinib plus golvatinib | RTK inhibitor+c-Met, Tie2, and EphB4 inhibitor | Disrupts pericyte-mediated vessel stabilization, reduces angiogenesis, decreases the amount of F4/80+MRC1+ macrophages | Thyroid and endometrial cancer models [253] |
Regorafenib | TKR inhibitor | Decreases tumor angiogenesis, the total number of TAMs, and increases M1/M2 ratio and infiltration of tumor by CD4+ and CD8+ T cell | Mouse model of HCC [254], mouse model of CRC [255] |
Sorafenib | small molecule, RTK inhibitor | Reduces the number of CD68+ TAMs, induces pro-inflammatory activity in TAMs | Patients with HCC [257], mouse model of HCC [258,259] |
Sorafenib plus compound Kushen injection (CKI) | RTK inhibitor+natural compound | Increases M1/M2 ratio, decreased M2, activates cytotoxic ability of CD8+ T cells | HCC mouse model [260] |
Sorafenib plus IRD-αCD206 | RTK inhibitor+anti-CD206 | Suppresses tumor growth and inhibites lung metastasis | Mouse model of 4T1 tumor [261] |
Sorafenib plus zoledronic acid | RTK inhibitor+TAM-depleting agent | Suppresses tumor growth and inhibites lung metastasis | Orthotopic HCC model [262] |
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
TAMs | Tumor-associated macrophages |
BMDM | Bone marrow-derived macrophage |
DC | Dendritic cell |
PFS | Progression-free survival |
LLC | Lewis lung carcinoma |
RCC | Renal cell carcinoma |
OSCC | Oral squamous cell carcinoma |
mAb | monoclonal antibody |
MVD | Microvessel density |
CM | Conditioned medium |
EC | Endothelial cell |
CAM | Chick chorioallantoic membrane |
CLP | Chitinase-like protein |
OPN | Osteopontin (SPP1) |
OSN | Osteonectin, Secreted protein acidic and rich in cysteine (SPARC) |
NSCLC | Non-small cell lung cancer |
TME | Tumor microenvironment |
SMA | Smooth muscle actin |
HUVEC | Human umbilical vein endothelial cell |
PDAC | Pancreatic ductal adenocarcinoma cell |
WT | Wild type |
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Larionova, I.; Kazakova, E.; Gerashchenko, T.; Kzhyshkowska, J. New Angiogenic Regulators Produced by TAMs: Perspective for Targeting Tumor Angiogenesis. Cancers 2021, 13, 3253. https://doi.org/10.3390/cancers13133253
Larionova I, Kazakova E, Gerashchenko T, Kzhyshkowska J. New Angiogenic Regulators Produced by TAMs: Perspective for Targeting Tumor Angiogenesis. Cancers. 2021; 13(13):3253. https://doi.org/10.3390/cancers13133253
Chicago/Turabian StyleLarionova, Irina, Elena Kazakova, Tatiana Gerashchenko, and Julia Kzhyshkowska. 2021. "New Angiogenic Regulators Produced by TAMs: Perspective for Targeting Tumor Angiogenesis" Cancers 13, no. 13: 3253. https://doi.org/10.3390/cancers13133253