Preclinical Evaluation of Minigastrin Analogs and Proof-of-Concept [(68)Ga]Ga-DOTA-CCK-66 PET/CT in 2 Patients with Medullary Thyroid Cancer

迷你胃泌素类似物的临床前评估及[(68)Ga]Ga-DOTA-CCK-66 PET/CT在2例甲状腺髓样癌患者中的概念验证

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Abstract

Because of the need for radiolabeled theranostics for the detection and treatment of medullary thyroid cancer (MTC), and the yet unresolved stability issues of minigastrin analogs targeting the cholecystokinin-2 receptor (CCK-2R), our aim was to address in vivo stability, our motivation being to develop and evaluate DOTA-CCK-66 (DOTA-γ-glu-PEG(3)-Trp-(N-Me)Nle-Asp-1-Nal-NH(2), PEG: polyethylene glycol) and DOTA-CCK-66.2 (DOTA-glu-PEG(3)-Trp-(N-Me)Nle-Asp-1-Nal-NH(2)), both derived from DOTA-MGS5 (DOTA-glu-Ala-Tyr-Gly-Trp-(N-Me)Nle-Asp-1-Nal-NH(2)), and clinically translate [(68)Ga]Ga-DOTA-CCK-66. Methods: (64)Cu and (67)Ga labeling of DOTA-CCK-66, DOTA-CCK-66.2, and DOTA-MGS5 was performed at 90°C within 15 min (1.0 M NaOAc buffer, pH 5.5, and 2.5 M 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid buffer, respectively). (177)Lu labeling of these 3 compounds was performed at 90°C within 15 min (1.0 M NaOAc buffer, pH 5.5, 0.1 M sodium ascorbate). CCK-2R affinity of (nat)Ga/(nat)Cu/(nat)Lu-labeled DOTA-CCK-66, DOTA-CCK-66.2, and DOTA-MGS5 was examined on AR42J cells. The in vivo stability of (177)Lu-labeled DOTA-CCK-66 and DOTA-MGS5 was examined at 30 min after injection in CB17-SCID mice. Biodistribution studies at 1 h ([(67)Ga]Ga-DOTA-CCK-66) and 24 h ([(177)Lu]Lu-DOTA-CCK-66/DOTA-MGS5) after injection were performed on AR42J tumor-bearing CB17-SCID mice. In a translation to the human setting, [(68)Ga]Ga-DOTA-CCK-66 was administered and whole-body PET/CT was acquired at 120 min after injection in 2 MTC patients. Results: Irrespective of the metal or radiometal used (copper, gallium, lutetium), high CCK-2R affinity (half-maximal inhibitory concentration, 3.6-6.0 nM) and favorable lipophilicity were determined. In vivo, increased numbers of intact peptide were found for [(177)Lu]Lu-DOTA-CCK-66 compared with [(177)Lu]Lu-DOTA-MGS5 in murine urine (23.7% ± 9.2% vs. 77.8% ± 2.3%). Overall tumor-to-background ratios were similar for both (177)Lu-labeled analogs. [(67)Ga]Ga-DOTA-CCK-66 exhibited accumulation (percentage injected dose per gram) that was high in tumor (19.4 ± 3.5) and low in off-target areas (blood, 0.61 ± 0.07; liver, 0.31 ± 0.02; pancreas, 0.23 ± 0.07; stomach, 1.81 ± 0.19; kidney, 2.51 ± 0.49) at 1 h after injection. PET/CT examination in 2 MTC patients applying [(68)Ga]Ga-DOTA-CCK-66 confirmed multiple metastases. Conclusion: Because of the high in vivo stability and favorable overall preclinical performance of [(nat/67)Ga]Ga-/[(nat/177)Lu]Lu-DOTA-CCK-66, a proof-of-concept clinical investigation of [(68)Ga]Ga-DOTA-CCK-66 was completed. As several lesions could be identified and excellent biodistribution patterns were observed, further patient studies applying [(68)Ga]Ga- and [(177)Lu]Lu-DOTA-CCK-66 are warranted.

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