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Meanwhile, various CCKR-targeted drugs have been developed, yet most of them were ultimately removed from the market due to questionable efficacy, lack of target specificity, or severe adverse effects28,29. This highlights the need for investigation of the structure of CCK1R and CCK2R to understand agonist binding, receptor activation and thus promote structure-based drug discovery. The biochemical concept of CCK as a single hormonal peptide from the small intestine has also changed considerably. Now CCK is known to be synthetized and released in multiple molecular forms. And the CCK gene is expressed at peptide level in a cell-specific manner in neurons, endocrine cells, and epithelial cells outside the gastrointestinal tract (Table 1).
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Step 2
CCK-8 predominates in the brain, and gastrin-17 accounts for 90% of gastrin in the human body, inducing acid release30. Notably, posttranslational modifications (PTMs) are critical for CCK and gastrin activity, including sulfation of the tyrosine (TYS) at position 7 from the C-terminus in CCK and at position 6 in gastrin (Fig. 1a). Intriguingly, CCK2R binds sulfated and non-sulfated ligands equally well, whereas CCK1R exclusively responds to sulfated CCK.
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In the CCK2R–Gq complex, Gq undergoes an anticlockwise rotation relative to the receptor compared to Gs (except for EP4R–Gs) (Supplementary Fig. S5a, f). This difference makes the α5 helix of Gq moving closer to the TM2–TM3–TM4 half (Supplementary Fig. S5h, i). It remains mysterious that the CCKRs with highly conserved orthosteric binding pocket display distinct affinity and potency on various endogenous ligands, according to previous homology modeling and mutagenesis studies45.
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Therefore, we attribute the fact that CCK2R recognizes non-sulfated and sulfated CCK-8 equally well to the lack of polar interactions between the endogenous ligands and CCK2R. CCK1R was co-expressed with human Gs protein in Sf9 insect cells to form the CCK1R–Gs complexes and activated by CCK-8 and by CCK1R-selective agonist SR146131, respectively. All complexes were purified to homogeneity for single-particle cryo-EM analysis (Supplementary Fig. S2). G protein activation was measured by a NanoBiT–G protein dissociation assay in which GPCR-induced G protein dissociation is monitored by a NanoBiT system. A large fragment (LgBiT) of the NanoBiT luciferase was inserted into the helical domain (between the αA and the αB helices) of a Gα subunit with 15-amino acid flexible linkers.