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. Author manuscript; available in PMC: 2021 Jun 1.
Published in final edited form as: Arterioscler Thromb Vasc Biol. 2020 May 27;40(6):e138–e152. doi: 10.1161/ATVBAHA.120.314330

Table1.

Recent reports identified new evidence to support the model that endothelial cells have innate immune functions in metabolic diseases. (Part I)

Innate immune relevance Associated metabolic situlations Target and experimental model Responses on ECs Interaction between ECs and other cells Reference
Complement system Early ischemia
Late ischemia
MBL (mannose-binding lectin)-deposition (MBL−/− mice) Induces the binding of IL-1α with IL-1R1
Increases C3b and induces ICAM-1
10
Atherogenesis RGC-32 (response gene to complement 32) in resident in vascular cells, but not macrophage (RGC-32−/− mice) induces ICAM-1, VCAM-1 through directly interacting with NF-KB RGC-32 deficiency decreases TNF-α-induced monocyte-endothelial cell interaction 196
Reguatlion Of cytokines, chemokines and adipokines Diabetic macular edema BMP9/Alk1 (activin-like kinase receptor type I) (HUVECs and streptozotocin-induced mice) Prevents VEGF-induced phosphorylation of VE-cadherin, induces occludin and strengthens vascular barrier functions 9
Angiogenesis BDNF (brain-derived neurotrophic factor) /NT-3 (neurotrophin-3) (ESCs, embryonic stem cells) Promotes ESCs differentiation to ECs in a BDNF/NT3 receptors dependent way 197
Abdominal aortic aneurysm (AAA) FAM3D (Mouse Models of AAA, and FAM3D−/− mice) FAM3D is upregulated in ECs by vascular pathogenic stimuli Contributes to neutrophil recruitment via FPR-Gi Protein/β-Arrestin-Mac-1 Signaling 198
Atherogenesis IL-35 (HAECs and APOE−/− mice) Inhibits mtROS-H3K14 acetylation-activator protein 1-mediated EC activation 199
Vascualr inflammation NOTCH1 signaling (HUVECs and RbpjiΔEC, NICD (Notch intracellular domain)iEC-OE mice) Modulates the transcriptional response to inflammatory cytokines; Supports the expression of a subset of inflammatory genes at the enhancer level Increases leukocyte recruitment to the inflamed lesion 200
Endothelial regeneration Cytokine-like protein dikkopf-3 (DKK3) (Human embryonic lung fibroblasts) Drives human fibroblasts to differentiate to functional ECs via mesenchymal-to-epithelial transition and VEGF-microRNA-Stat3 pathways 201
Atherosclerosis and arterial stiffness SFRP5 (secreted frizzled-related protein 5) (HUVECs, HAECs and patients with type 2 diabetes) Restors Wnt5 (wingless-type family member 5a)-reduced NO production via eNOS 202
Part II
Innate immune relevance Associated metabolic situlations Target and experimental model Responses on ECs Interaction between ECs and other cells Reference
Receptor systems sensing (DMAPs) Erosion-associated thrombosis Neutrophil extracellular traps (HSVECs (human saphenous vein ECs) or HUVECs) Augments ICAM-1, VCAM-1 and transcription factors through concerted action of IL-1α and cathepsin G, but not IL-1β 11
Angiogenesis Posttranslational proteolytic cleavage of VEGF receptors (HUVECs) Upregulates neuropilin-1 (NRP1) species in an ADAM(a disintegrin and metalloproteinase)9/10-dependent manner resulting in inhibition of VEGF-induced EC motility and angiogenesis 203
Angiogenesis MicroRNA-199a-3p/5p (bovine aortic endothelial cells) Redundantly decreases eNOS activity and induces its degradation, thereby supporting VEGF-induced endothelial tubulogenesis 97
Atherogenesis Dislipidemia and disturbed flow (HAECs and CD36−/− mice) Increases oxLDL uptake and enhences endothelial stiffening via CD36 204
Thrombophilia Hypoxic trophoblasts derived HMGB1 (HUVECs and Pregnant mice) Stimulates the generation and release of EC-oringin microparticles and enhances blood coagulation Triggers neutrophil activation 205
Thrombotic and inflammatory disorders PolyP70 (Inorganic polyphosphate 70) (HUVECs) Amplified HMGB1-mediated VWF release via binding to RAGE and P2Y1 receptors Promotes VWF-platelet string formation on ECs 15
Flow-dependent vascular remodeling Lack of cystathionine γ-lyase (CSE−/− mice) limits disturbed flow-induced ICAM-1, VCAM-1 through altering NO availability Decreases monocyte infiltration 206
Pulmonary Hypertension (PH) HIMF Signaling (human pulmonary microvascular ECs and pulmonary arteries of patients with idiopathic PH and PH Models in mice and rats) Triggers the HMGB1 pathway and RAGE EC-derived HMGB1 induces an autophagic response, BMPR2 defects, and subsequent apoptosis-resistant proliferation in smooth muscle cells 126
Pulmonary Hypertension EC-specific caveolin-1 (Cav-1) depletion (EC-Cav1−/− mice) exhibits a non-EC phenotype and contributes to vascular remodeling via TGF-β/pSmad2/3 signaling With Increasing Cav-1+ extracellular vesicle shedding into the circulation and decreasing circulating monocytes 207
Pulmonary Hypertension Cigarette Smoke Exposure (PAECs and rats model) Increases endothelial extracellular vesicles (eEV) generation and the spermine content in eEV Triggers eEV migration into SMCs, and contributes to pulmonary artery smooth muscle constriction and proliferation via CaSR 208
Vascular aging and acute myocardial infarction (AMI) Switch in Lamb2 to Lamb1 (HUVECs and Mouse models of AMI) Impaires the functional properties and phenotype of endothelial cell via integrin receptors 209
ECs Dysfunction Nine flavors added to tobacco products (HEACs) Iimpairs eNOS agonist-stimulated NO production and triggers inflammation, even cell death, such as vanillin and eugenol. 5
ECs Dysfunction Exposure to fine particulate matter (PM2.5) (Endothelial progenitor cells, EPCs) Impairs EPC abundance and function and prevents EPC-mediated vascular recovery after hindlimb ischemia via vascular VEGF resistance and a decrement in NO bioavailability 210
Hypertension GLP-1 (glucagon-like peptide-1) analogs (Global, EC-and myelomonocytic-specific Glp1r −/− mice) Reduces blood pressure and protects endothelial function through endothelial but not myeloid cell GLP-1 receptor Prevents Ly6G−Ly6C+ and Ly6G+ Ly6C+ cell infiltration to the vessel wall 211
Part III
Innate immune relevance Associated metabolic situlations Target and experimental model Responses on ECs Interaction between ECs and other cells Reference
Receptor systems sensing (HAMPs) Organ specificity Cardiac ECs (transcriptome) Highly expresses key regulators in fatty acid uptake, such as Meox2/Tcf15, Fabp4, and Cd36 212
Pathological angiogenesis EC-specific Atg5 deletion (HUVECs, HRMECs (human retinal microvascular ECs), MLECs (murine lung ECs) and Mice with EC-specific inactivation of Atg5) Impairs mitochondrial function, diminishes production of mtROS, decreased oxidative inactivation of PTPs (phospho-tyrosine phosphatases)and hence, decreasing phosphorylation of the VEGFR2 167
Atherogenesis Atheroprotective pulsatile shear stress (HUVECs) Activates ITPR3 transcription via KLF4-regulated H3K27ac (acetylation of histone 3 lysine 27) enrichment and chromatin accessibility, contributes to the Ca2+ - dependent eNOS activation and EC homeostasis. 168
Atherogenesis and CAD (coronary artery disease) JCAD, CAD-associated variants at 10p11.23, knockdown (HUVECs) Decreases ICAM-1, VCAM-1 and Selectin E by negatively regulates YAP activity and Hippo signaling Reduces monocyte adhesion 26
Abdominal aortic aneurysm Cilostazol, a selective inhibitor of phosphodiesterase III (PDEIII) (MAECs and APOE−/− mice) Reduces MCP-1 and ICAM-1 via increasing intracellular cAMP Reduces medial disruption and macrophage infiltration in angiotensin II-Induced AAA, but no effect on atherosclerosis 213
Pulmonary hypertension Hypoxia (HPMEC) Induces SENP1 (sentrin-specific protease 1)and deprivates KLF15 by SUMOylation, lossing repression on arginase 2 promoter and impairing NO production 169
Inflammation/Stress A shift from AIP1A to AIP1B isoform (HUVECs) Localizes to the mitochondria and augments TNFα-induced mtROS generation and EC activation 170
Hypertension Knockdown of SIRT3 (sirtuin 3) (EPCs) Contributes to the decline in reendothelialization capacity Results in mitochondrial oxidative damage, hyperacetylation of SOD2 (superoxide dismutase 2) in EPCs 171