Microvascular Experimentation in the Chick Chorioallantoic Membrane as a Model for Screening Angiogenic Agents including from Gene-Modified Cells
Abstract
:1. Introduction
2. CAM and Chick Development
3. CAM Assay Procedures
4. CAM Experimental Treatments
4.1. Scaffolds and Delivery Methods
4.2. Drugs, Metabolites, miRNAs and Other Treatments
4.3. Cell and Gene Modified Cell On-Plants
5. CAM Analyses
5.1. Sectioning and Staining Techniques
5.2. Image Quantification Techniques
5.3. Vascular Casting
5.4. Live Blood-Flow Observation
5.5. Molecular Analysis
6. Advantages and Limitations of the CAM to Study Microcirculation
7. Concluding Remarks
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Scaffold/Delivery Method | Reference |
---|---|
Collagen | [54,55,56,57] |
Filter disc | [58,59,60,61,62,63,64,65] |
Gelatin sponge | [66,67,68,69,70,71] |
Glass discs | [72,73] |
Hydrogel | [41,74,75,76,77] |
Injected | [78,79,80,81,82,83,84] |
Matrigel | [16,85,86,87,88,89,90] |
Methylcellulose disc | [15,91,92,93,94] |
Microspheres | [95,96] |
Pipetted onto surface | [97,98,99,100,101,102,103] |
Plastic ring | [75,104,105,106,107,108,109,110,111] |
Scaffold | [108,112,113,114,115,116,117] |
Thermanox coverslip | [118,119,120,121,122] |
Tumour | [5,123,124,125,126] |
Pellet | [127,128,129] |
Treatment | Delivery Method | Angiogenic Outcome | Ref. |
---|---|---|---|
Connective tissue growth factor (CTGF) | Scaffold | Significant increase in blood vessel number and diameter following software quantification | [137] |
Thermanox Coverslips | A dose dependent increase seen by appearance of spoke wheel pattern of blood vessels radiating from on-plants | [138] | |
Platelet-derived growth factor (PDGF) | Thermanox Coverslips | Macroscopic observations indicated thickening of CAM, but no vascular response | [139] |
Scaffold | An increased blood vessel density converging towards on-plant observed along with thickening of CAM membrane | [140] | |
Basic Fibroblast Growth Factor (bFGF/FGF-2) | Scaffold | ||
Plastic ring | Significant increase in number of blood vessels converging towards on-plant | [110] | |
Filter disc | Significant increase in mean fluorescent vascular density, measured by pixel intensity | [141] | |
Increased number of branch points in a region around on-plants | [142] | ||
Transforming growth factor-β (TGF-β) | Filter disc | Radial formation of new vessels seen in area around on-plants | [143] |
TNFα | Filter disc | Significant increase in tube length and size as measured by angiogenic software | [144] |
VEGF-165 | Filter disc | A dose responsive increase in blood vessels in defined area observed | [145] |
Hydrogel | A time-dependent increase in blood vessel diameter and branching points, measured using angiogenic software | [146] | |
Thermanox Coverslips | Macroscopic observations saw a dose dependent increase in angiogenesis | [139] | |
VEGF-121 | Thermanox Coverslips | Macroscopic observations noticed a change in vascular pattern under the treatment area | [147] |
Filter disc | Software quantified a dose responsive increase in total blood vessel network length | [148] | |
VEGF-A | Filter disc | Significant increase in sprouting blood vessels within a defined area | [149] |
Scaffold | Increased blood vessel density observed within a defined area | [140] | |
Matrigel | Microvascular mapping of the blood vessel network following FITC injection resulted in increased blood vessel density | [150] | |
Glass fibre filter disc | Significant increase in vessels number quantified in a random square areas of CAM surface | [151] | |
Plastic ring | Angiogenic software indicated a significant increase in number of branchpoints and average vessel length | [111] | |
Hydrogel | Significant increase in vessel length, number and vasculogenic index | [74] | |
Significant increase in vessel number in a region around on-plant | [152] | ||
VEGF-C | Hydrogel | Significant increase in vessel number in a region around on-plant | [152] |
Methylcellulose disc | Increase in sprouting blood vessels present within a defined area | [153] | |
Thyroxine | Hydrogel | Significant increase in vascular penetration of on-plants | [154] |
Heparin | Hydrogel | Significant increase in vessel number in a region around on-plant | [40] |
VEGF-D | Hydrogel | Significant increase in sprouting blood vessels present within a defined area | [152] |
Estradiol | Plastic ring | Calculation of percentage of CAM surface covered by endothelial cells resulted in a significant increase in the mean vessels count | [49] |
Angiogenic software quantified a significant increase in number of branchpoints and average vessel length | [111] | ||
Scaffold | Increase in angiogenic response seen by measurement of vasculogenic index | [117] | |
Estradiol | Filter disc | Increased vascular branching observed within a defined area | [155] |
L-Arginine | Filter disc | The number of primary, secondary, tertiary, and quaternary blood vessels counted with a significant increase in number of quaternary blood vessels | [3] |
TGF-β induced miR-29a upregulation | Pipetted | Significant increase in number of blood vessels around on-plant observed | [130] |
Fibroblast growth factor-1 expression plasmid | Pipetted | Significant increase in number of blood vessels in a region around on-plant observed | [135] |
VEGF-GFP LV | Microgels | Increased blood vessel development quantified | [136] |
MSCs-exomes | Not mentioned | Significant promotion of new blood vessel formation | [133] |
miR-21-5p OE exomes | |||
Transthyretin | Plastic ring | Significant increase in number of blood vessels growing towards on-plants | [110] |
Terbutaline | Plastic disc | Counting blood vessels which intersected a concentric circle projected around on-plants observed a significant increase in number of blood vessels | [64] |
β2AR antagonist | Coverslip | Increased number of blood vessel branch points observed within on-plants | [156] |
Angiogenin | Thermonox discs | Visibly increased number of blood vessel spoke wheel pattern seen radiating from on-plants | [157] |
Adenosine | Elvax Polymer pellet | Dose dependent increase in vascular density observed in a region around on-plant | [158] |
Observation of spoke wheel pattern of blood vessels radiating from on-plants, with a positive result observed in majority of samples | [127] | ||
ADP | |||
ATP | |||
Lactic Acid | |||
Malate | |||
Exosomes derived from chronic myeloid leukaemia cells (K562) | Plastic ring | Treatment with a higher concentration resulted in an increase in neovasculature | [134] |
2-deoxy-D-ribose | Plastic ring | Angiogenic software calculated a significant increase in number of branchpoints and average vessel length | [111] |
Sclerostin | Gelatin sponge | Increased number of blood vessels converging towards on-plants observed | [159] |
Roxarsone | Gelatin sponge | Increased number of neovessels and blood vessel length | [160] |
Leptin | Gelatin sponge | Software measured significantly increased blood vessel tube length and size | [71] |
Arsenic | Filter disc | Dose dependent increase in blood vessel number observed, however higher doses resulted in negative effects | [161] |
Y2O3 nanoparticles | Scaffold | Improved blood vessel formation, vascular branching and blood vessel diameter within the area around scaffolds | [162] |
Treatment | Delivery Method | Angiogenic Outcome | Ref. |
---|---|---|---|
Nicotinamide adenine dinucleotide (NAD) | 10% EVA copolymer Pellet | No spoke wheel pattern was observed radiating from on-plants | [127] |
Pyruvate | |||
Succinate Fumarate citrate | |||
Avastin (Bevacizumab) | Injected | Significantly less vascular nodes and branches were quantified within a defined area | [80] |
EG-VEGF Antibodies | No significant differences in vessel density observed, but dilated medium and large vessels observed | [168] | |
Methyl blue | Microspheres | No spoke wheel pattern was observed radiating from on-plants | [96] |
Chloroquine & Doxorubicin | Agarose pellet | Combination of doxorubicin and chloroquine resulted in strong anti-angiogenic effect on capillaries near on-plants | [129] |
Avastin (Bevacizumab) | Pipetted | Significant decrease in percentage of surface area occupied by microvessels | [165] |
Vitamin C | Pipetted | The number of primary, secondary, tertiary, and quaternary blood vessels was counted, with decrease in quaternary blood vessels quantified | [3] |
MART-10 (Vitamin D analog) | Pipetted | Reduced vessel branch point numbers observed within a defined area | [172] |
Green nanoparticles | Gelatin sponge | Decrease in vessels length and branch number within a defined area | [166] |
Rhaponticin | Filter disc | Software determined a significant reduction in total blood vessel length | [173] |
Thalidomide derivatives | Filter disc | Reduction in vessel number, branch points, neovascularization and total length of vessels | [59] |
High affinity PGF-specific Nanobody | Filter disc | Significant inhibition of angiogenesis within a defined area | [170] |
Antithrombin | Filter disc | Potent antiangiogenic activity in blood vessel tubules, networks and branching points | [174] |
Zinc tungstate nanoparticles | Filter disc | A dose dependent reduction in percentage of surface area occupied by blood vessels was calculated | [61] |
Gold nanoparticles | Filter disc | Software determined a dose dependent reduction in blood vessel size, length and branch points | [60] |
Injected | Software determined a significant reduction in vessel length and number of junctions and complexes | [84] | |
miR-7 mimics | Nitrocellulose rings | A reduction in vascular density within a defined area was visible | [175] |
Sunitinib (receptor tyrosine kinase inhibitor) | Nitrocellulose rings | A reduction in vascular density within a defined area was visible | [175] |
Vasohibin Adenovirus | Matrigel | Macroscopic observations saw inhibition of blood vessel growth | [16] |
Chitosan derivatives nanoparticles | Methylcellulose disc | Reduction in number of blood vessels in contact with on-plants observed | [94] |
Anti-VEGF Antibody | Methylcellulose disc | Visible anti-angiogenic activity observed through semi-quantitative evaluation | [169] |
Anti-laminin antibody | Methylcellulose disc | Macroscopic observations saw a delay in capillary network development | [171] |
Anginex | Plastic ring | Significant decrease in intersections of blood vessels with concentric rings projected onto images | [176,177] |
Angiotensinogen | Plastic ring | First and second order centripetal blood vessels around on-plants were counted, with inhibition of smaller blood vessels observed | [178] |
Following FITC injection, blood vessel density, length and number of branch points were quantified highlighting inhibition of smaller blood vessels | [29] | ||
Obtustatin (α1β1 inhibitor) | Decrease in the number of small new vessels growing towards on-plants | [179] |
Response | Treatment | Delivery Method | Angiogenic Outcome | Ref. |
---|---|---|---|---|
Pro-angiogenic | Glioblastoma cancer stem cells | Alginate scaffold | Increased blood vessel number converging towards on-plants | [114] |
Human umbilical vein endothelial cells (HUVECs) | Cylindrical scaffold | Increased number of blood vessels and blood vessel penetration into on-plant | [115] | |
Adipose derived stem cells | Cylindrical scaffold | Increased number of blood vessels and blood vessel penetration into on-plant | [115] | |
Hydrogel | Significant increase in vessel number, vessel length and vasculogenic index | [74] | ||
Seeded on a scaffold | Increased number of blood vessels converging towards on-plants | [108] | ||
Matrigel | Following von Willebrand factor staining and semi quantitative scoring, a significant increase in angiogenesis | [184] | ||
Burkitt’s Lymphoma cell lines (BL2B95 and BL74) | Matrigel | Following tissue sectioning increase in blood vessel diameter determined | [183] | |
Human Liver Cancer (HepG2) cells | Matrigel | Increased number of blood vessels converging towards on-plants | [86] | |
Prostate Cancer Cells (LNCaP) | Matrigel | A change in blood vessel number within a defined area observed | [185] | |
Colon carcinoma (SW620) | Matrigel | Increase in angiogenic index was observed | [54] | |
Neuroblastoma (NB15/FOXO3 cells) | Matrigel | Following desmin staining, increased micro-vessel formation was observed | [56] | |
Glioblastoma (U87 MG) Cell lines | Matrigel | Increased observation of spoke wheel pattern of blood vessels radiating from on-plants | [55] | |
Human Cardiopoietic Stem Cells | Scaffold | Blood vessel density within a defined area was increased | [186] | |
Multiple myeloma plasma cells | Gelatin sponge | Induction of an increased vasculogenic index was calculated | [66] | |
Mouse Melanoma (B-16) | Plastic ring | Development of visible spoke wheel pattern of blood vessels converging towards on-plants | [187] | |
Human Melanoma (C8161) | Plastic ring | Significant increase in area occupied by endothelial cells observed within a defined area | [75] | |
Hydrogel | ||||
Human Prostate Cancer (PC3) | ||||
Plastic ring | ||||
Skin graft | Plastic ring | Photobiomodulation along with cell application resulted in increased number of vascular junctions within a defined area | [104] | |
Human Ovarian Tissue | Plastic ring | Visual estimation of area occupied by blood vessels compared to total surface area resulted increased angiogenesis and neovascularisation | [188] | |
Melanoma Tumour Tissue | Tumour | Spoke wheel pattern of capillaries converging towards on-plants observed | [189] | |
Recurrent respiratory papilloma tissue (RRP) | Tumour | Increase in blood vessel number within a defined area observed | [125] | |
Hepatocellular Carcinoma Tumour tissue | Tumour | Increased micro vessel density within a defined area observed | [190] | |
Human Malignant Ovarian tumours | Tumour | Increase in the pattern, density, and size of the CAM blood vessels near the tumour implants visible | [191] | |
Adenocarcinoma Tumour Tissue | Tumour | Increase in the pattern, density, and size of the CAM blood vessels near the tumour implants visible | [191] | |
Glioma cells (C6) | Injected | Macroscopic observations indicated tumours became vascularised by CAM blood vessels | [78] | |
Pancreatic carcinoma (10AS) | Injectí | Macroscopic observations indicated tumours became vascularised by CAM blood vessels | [78] | |
Anti-angiogenic | Colon carcinoma (SW480) | Collagen | No Induction of angiogenesis or increased angiogenic index | [54] |
Burkitt’s Lymphoma cell lines (BL2) | Matrigel | Following tissue sectioning reduced blood vessel diameter observed | [183] |
Gene Modification | Cell Type | Delivery Method | Angiogenic Response | Ref. | |
---|---|---|---|---|---|
Pro-angiogenic | FGF-1 expression plasmid | Bovine Endothelial Cells | Gelatin sponge | Following tissue sectioning, and staining for von Willebrand Factor, a twofold increase in capillary number was quantified | [135] |
LV miR-205 inhibition | Endothelial colony-forming cell CM | Not mentioned | Software quantified significant increase in blood vessel density within a defined area | [192] | |
Sphingosine-1-phosphate treated | Osteoblast cell (MG-63) CM | Increase in blood vessel number within a defined area was quantified | [193] | ||
miR-338-3p inhibition plasmid | Hepatocellular carcinoma (HCC) CM | Filter disc | Visual inspection of second and third order blood vessels inferred increased blood vessel formation | [194] | |
AGO2 expression plasmid | Myeloma cell CM | Significant increase in on-plant infiltrating blood vessels observed | [195] | ||
IFN-γ treated | Mesenchymal stem cell CM | Pipetted | A significant increase in number of small blood vessels (diameter less than 1 mm) | [196] | |
TNF-α treated | |||||
IFN-γ and TNF-α treated | A significant increase in both small and large blood vessels | ||||
Anti-angiogenic | AAV-Timp1- transduced | Chinese hamster ovary cells | Gelatin sponge | No spoke wheel pattern of blood vessels radiating from on-plants | [197] |
LV mediated Angiopoietin-2 shRNA | Pancreatic carcinoma cells | Pipetted | Decrease in number of blood vessel branch points | [198] | |
Connective tissue growth factor (CTGF)-shRNA | OASF cell CM | Pipetted | Significant reduction in blood vessel count | [199] | |
Endostatin expression plasmid | COS-1 cell CM | Pipetted | Significant reduction in blood vessel branch points | [200] | |
LV VEGF shRNA | Hypertriploid renal cell carcinoma CM | Pipetted | Significant decrease in blood vessel counts and total blood vessel length | [201] | |
CCL5-shRNA | Chondrosarcoma cells (JJ012) | Matrigel | Significant decrease in blood vessel branches | [202] | |
Sema3C transfected | Glioblastoma cell line (U87 MG) | Collagen | Diminished observation of a spoke wheel pattern of blood vessels radiating from on-plants | [55] | |
AGO2-shRNA | Myeloma cell CM | Filter disc | Lower blood vessel densities infiltrating the on-plants observed | [195] | |
Vascular endothelial cell growth inhibitor (VEGI) expression plasmid | HeLa cell CM | Filter disc | Significant inhibition of neovascularization | [203] | |
Novel immunotoxin (VEGF165-PE38) expression plasmid | HEK293 cell CM | Not mentioned | Inhibition in growth of capillary-like structures | [204] | |
LV miR-205 OE | Endothelial colony-forming cell CM | Visual inspection saw reduced blood vessel formation | [192] | ||
miR-181a-5p expression plasmid | Fibrosarcoma (HT1080) cell CM | Gelatin sponge | Impairment of new blood vessel formation observed | [205] | |
Nuclear Factor-Erythroid 2 (NRF2) shRNA | Human colon cancer cell CM | Matrigel | Significant reduction in blood vessel branch points in circular region around on-plants | [206] | |
P53 Isoform (Δ133p53) deletion | Human Glioblastoma (U87) cell CM | Silicon ring | Following tissue sectioning and staining, reduced blood vessels quantified | [207] | |
LV miR-542-5p | Non-small cell lung cancer CM | Silicon ring | Significant reduction in percentage vascular density | [109] |
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Kennedy, D.C.; Coen, B.; Wheatley, A.M.; McCullagh, K.J.A. Microvascular Experimentation in the Chick Chorioallantoic Membrane as a Model for Screening Angiogenic Agents including from Gene-Modified Cells. Int. J. Mol. Sci. 2022, 23, 452. https://doi.org/10.3390/ijms23010452
Kennedy DC, Coen B, Wheatley AM, McCullagh KJA. Microvascular Experimentation in the Chick Chorioallantoic Membrane as a Model for Screening Angiogenic Agents including from Gene-Modified Cells. International Journal of Molecular Sciences. 2022; 23(1):452. https://doi.org/10.3390/ijms23010452
Chicago/Turabian StyleKennedy, Donna C., Barbara Coen, Antony M. Wheatley, and Karl J. A. McCullagh. 2022. "Microvascular Experimentation in the Chick Chorioallantoic Membrane as a Model for Screening Angiogenic Agents including from Gene-Modified Cells" International Journal of Molecular Sciences 23, no. 1: 452. https://doi.org/10.3390/ijms23010452