PET and SPECT Imaging of the EGFR Family (RTK Class I) in Oncology
Abstract
:1. Introduction
1.1. Human Epidermal Growth Factor Receptor Family in Cancer
1.2. Detection of EGFR-Family Expression for Targeted Treatment
1.3. Biopsy Based Methods
1.4. Radionuclide-Based Molecular Imaging
1.5. General Considerations for the Development of Radiotracers for PET and SPECT Imaging
2. This Review
3. HER1 Imaging
3.1. Monoclonal Antibodies for Imaging of HER1 Expression
3.2. Antibody Fragments, scFv and sdAb for Imaging of HER1 Expression
3.3. Affibody Molecules for Imaging of HER1 Expression
3.4. Small Peptides
3.5. HER1 Concluding Remarks
4. HER2 Imaging
4.1. Monoclonal Antibodies
4.2. Antibody Fragments for Imaging of HER2 Expression
4.3. scFv, Diabody, Minibody, sdAb for Imaging of HER2 Expression
4.4. ESPs for Imaging of HER2 Expression
4.5. Aptamers and Peptides
4.6. HER2 Concluding Remarks
5. HER3 Imaging
5.1. Monoclonal Antibodies and Antibody Fragments for Imaging of HER3 Expression
5.2. sdAb, Affibody Molecules and Peptides for Imaging of HER3 Expression
5.3. HER3 Concluding Remarks
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
Abbreviations
BC | Breast cancer |
ECD | Extra cellular domain |
EGFR | Epidermal growth factor receptor |
ESP | Engineered scaffold proteins |
HER | Human epidermal growth factor |
ICD | Intra cellular domain |
IHC | Immunohistochemistry |
ISH | in situ hybridizations |
mAb | Monoclonal antibody |
mBC | Metastatic breast cancer |
mCRC | Metastatic colorectal cancer |
NSCLC | Non-small cell lung cancer |
PC | Prostate cancer |
PET | Positron emission Tomography |
pi | post injection |
RTK | Receptor tyrosine kinase |
scFv | Single chain variable fragment |
sdAb | Single domain antibody |
SPECT | Single photon emission tomography |
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Tracer | PET/ SPECT | Type of Molecule | Key Points | Reference |
---|---|---|---|---|
Clinical Studies | ||||
[89Zr]Zr-cetuximab | PET | Antibody | Phase II/II Specific tumor uptake in patients Optimal imaging day six | [75,111,130] |
[89Zr]Zr-panitumumab | PET | Antibody | Tumors could not be visualized, potentially be due to location in areas with high background due metabolic tracer accumulation (liver, abdomen) | [81] |
[89Zr]Zr-nimotuzumab | PET | Antibody | Currently in Phase I/II studies Estimated absorbed was lower than dose for [89Zr]Zr-DFO-panitumumab | [123], NCT04235114 |
Preclinical Studies | ||||
[64Cu]Cu-cetuximab | PET | Antibody | Can visualize HER1 expression 48 h pi xenografts Correlation between uptake, expression and predicative power still unclear | [114,115] |
[64Cu]Cu-panitumumab | PET | Antibody | HER1 expression in three different HNSCC xenografts could be visualized Inverse relation between tumor uptake and HER1 expression, possibly related to vessel density, vascular permeability and binding site barrier | [128] |
[111In]In-panitumumab | SPECT | Antibody | [111In]In-CHX”-DTPA- panitumumab has slightly faster blood clearance compared with [89Zr]Zr-DFO-panitumumab Conjugation of an MCP with 13 DOTAs to reduce liver and spleen uptake surprisingly increased hepatic uptake significantly | [121] |
[64Cu]Cu-NOTA- panitumumab F(ab′)2 | PET | Antibody fragment | Faster clearance compared with full length panitumumab Highest uptake in xenografts 48 h pi Tumor-to-blood ratios of 5–9 at 48 h pi | [131,161] |
[111In]In-cetuximab F(ab′)2 | SPECT | Antibody fragment | Provides significantly better tumor-to-blood ratios than cetuximab at early time points Highest uptake in xenografts 24 h pi Correlation between uptake and expression in xenografts Therapy response in mice correlated with tracer uptake | [87,132,162] |
[99mTc]Tc-Pm-Fab-His6 | SPECT | Antibody fragment | Tumor uptake and tumor-to-blood ratios similar to those of [64Cu]Cu-NOTA-panitumumab-F(ab′)2 24 h and 48 h pi Clear visualization of a panel of HER1 expressing xenografts using SPECT | [134] |
[99mTc]Tc-D10 | SPECT | sdAb | Detection of HER1 expressing lesions 45 min pi Tumor-to-blood ratio comparable to that of F(ab′)2 fragments of cetuximab and panitumumab | [135] |
[68Ga]Ga/[89Zr]Zr-Df-Bz-NCS-7D12 | PET | sdAb | Higher tumor uptake than uptake of [ 99m Tc]Tc-D10 Good visualization on PET 1h pi | [137] |
[89Zr]Zr-DFO-ZEGFR:2377 | PET | Affibody | Tumor uptake 3 h pi exceeded uptake of [89 Zr]Zr-DFO-cetuximab at 48 h pi Tumor-to-tissue contrast at 3 h and 24 h was higher than [89 Zr]Zr-DFO-cetuximab except from tumor-to-kidney | [140] |
[55/57Co]Co-DOTA- ZEGFR:2377 | PET | Affibody | Highest tumor-to-tissue contrast compared with all other studied affibody-based tracers | [105] |
[68Ga]Ga-DFO-ZEGFR:2377 | PET | Affibody | For imaging at 3 h pi Compared with other affibody molecules against HER1 the imaging contrast was inferior only to the radiocobalt conjugate, but 68Ga is more available than 55Co | [142] |
[64Cu]Cu-FnEI3.4.3′ | PET | Fibronectin binding domain | Good tumor visualization on PET 1h pi No cross-reactivity with mErbB1 | [149] |
Tracer | PET/ SPECT | Type of Molecule | Key Points | Reference |
---|---|---|---|---|
Clinical Studies | ||||
[64Cu]Cu-trastuzumab [89Zr]Zr-trastuzumab | PET | Antibody | [89Zr]Zr-trastuzumab was the first clinically studied PET-tracer for imaging of HER2 Successful visualization of HER2 positive lesions in patients with BC and esophagogastric cancer Optimal imaging 4–6 d pi (89Zr) or 48 h pi (64Cu) | [74,179,180,181,185,187] |
[89Zr]Zr-pertuzumab | PET | Antibody | Successful visualization of HER2 positive primary tumor and metastases in BC patients [89Zr]Zr-pertuzumab appeared to have slightly higher uptake than [89Zr]Zr-trastuzumab in liver, kidney, spleen, and lung | [182,184] |
[111In]In-CHX-A″-DTPA trastuzumab | SPECT | Antibody | Phase 0 demonstrated safety No data on tumor targeting available | [177] |
[68Ga]Ga-DOTA-F(ab′)2- trastuzumab | PET | Antibody fragment | HER2-positive lesion were detected in only half the patients with known HER2-positive disease In xenografted mice, the tumor uptake was proportional to HER2 expression | [206,209] |
[68Ga]Ga-HER2-Nanobody (also 2Rs15d) | PET | sdAb | Well tolerated administration Imaging of HER2 expression 60–90 min pi 90 min pi was suggested as more suitable time point for imaging | [223] |
[131I]I-GMIB-Anti-HER2- VHH1 (also GMIB-2Rs15d) | SPECT | sdAb | Phase I trial showed uptake in patients with lesions >3 cm Visualization of smaller lesions was difficult, supposedly due to PVE | [219] |
[68Ga]Ga-DOTA-ABY025 | PET | Affibody | Primary tumors and metastases (even hepatic) could be visualized Correlation between SUV in lesions with confirmed HER2 IHC scores Multicenter Phase II/III study currently underway (NCT03655353) | [78,233] |
[68Ga]Ga-NOTA-MAL-Cys-MZHER2:342 | PET | Affibody | Optimal imaging contrast was achieved 2 h pi Reporting 100% specificity, 55% sensitivity at an SUV cutoff at 6.6 | [237] |
[99mTc]Tc-ADAPT6 | SPECT | ADAPT | First ever clinical study with ADAPT Well-tolerated administration An optimal injected protein dose (500 µg) was able to differentiate between positive and negative lesions | [169] |
[99mTc]Tc-(HE)3-G3 | SPECT | DARPin | First clinical trial with HER2 targeting DARPin to assess safety, distribution, and dosimetry in patients with primary breast cancer is currently ongoing | NCT04277338 |
Preclinical Studies | ||||
[64Cu]Cu-NOTA-pertuzumab F(ab′)2 | PET | Antibody fragment | Trastuzumab-induced changes in HER2 could be detected Sensitivity increased from 24 to 48 h pi | [205] |
[89Zr]Zr-Df-Fab-PAS200 [124I]I-Df-Fab-PAS200 | PET | Antibody fragment | Despite lower tumor uptake of the 124I-labeled variant both tracers showed comparable contrast and good visualization of xenografts 24 h pi Administration of 89Zr-labeled variant in one patient could detect lesions 24 h pi | [207,208] |
[123/124/125I]I-PIB-G3-(HE)3 | PET/ SPECT | DARPin | Indirect iodination using SPIB and introduction of (HE)3-tag improved tumor-to-tissue ratios Another promising variant for clinical translation among the explored DARPin variants | [86,224,239] |
[111In]In-DTPA-AHNP-PEG | SPECT | Peptide | Showed higher tumor uptake, retention and tumor-to-tissue ratios than other reported HER2 targeting peptides Good visualization of gastric cancer xenografts up to 48 h pi | [242] |
Tracer | PET/ SPECT | Type of Molecule | Key Points | Reference |
---|---|---|---|---|
Clinical Studies | ||||
[64Cu]Cu-patritumab (also AMG-888 or U3-1287) | PET | Antibody | Clinical/Phase 1 terminated after 11 patients due to low uptake in HER3 expressing lesions | [249] |
[89Zr]Zr-GSK 2849330 | PET | Antibody | Tumor uptake was dependent on the injected mass thus indicating good potential for assessment of target occupancy and as a tool for dose selection | [251] |
[89Zr]Zr-lumretuzumab (also RG-7116) | PET | Antibody | Detected 67.6% of lesions larger than 10 mm No liver metastases could be detected due to high uptake in healthy liver tissue | [73] |
Preclinical Studies | ||||
[89Zr]Zr-MSB0010853 | PET | Biparatopic sdAb construct | Maximum tumor uptake 96 h pi was comparable with that of affibody molecules 3–24 h piHigher tumor-to-blood ratios compared with preclinical data on [89Zr]Zr-lumretuzumab and [64Cu]Cu-patritumab | [259] |
[55/57Co]Co-(HE)3- ZHER3:08698-DOTA | PET/ SPECT | Affibody | Reported best tumor-to-liver contrast among radiometal labeled anti-HER3 affibody molecules | [265] |
[89Zr]Zr-DFO-ZHER3:08698 | PET | Affibody | Could image changes in HER3 expression induced by HSP90 therapy | [258] |
[68Ga]Ga-HER3P1 | PET | Peptide | Uptake in xenografts <1 %ID/g due to rapid wash out and low affinity | [269] |
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Rinne, S.S.; Orlova, A.; Tolmachev, V. PET and SPECT Imaging of the EGFR Family (RTK Class I) in Oncology. Int. J. Mol. Sci. 2021, 22, 3663. https://doi.org/10.3390/ijms22073663
Rinne SS, Orlova A, Tolmachev V. PET and SPECT Imaging of the EGFR Family (RTK Class I) in Oncology. International Journal of Molecular Sciences. 2021; 22(7):3663. https://doi.org/10.3390/ijms22073663
Chicago/Turabian StyleRinne, Sara S., Anna Orlova, and Vladimir Tolmachev. 2021. "PET and SPECT Imaging of the EGFR Family (RTK Class I) in Oncology" International Journal of Molecular Sciences 22, no. 7: 3663. https://doi.org/10.3390/ijms22073663