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All known biological effects of CCK peptides reside in the conserved C-terminal heptapeptide sequence (Figure 1). Modification of this sequence grossly reduces or abolishes receptor binding and biological effects (13–15). The N-terminal extensions of the common C-terminus increase the biological potency and the specificity for receptor binding.
- Cerebral gliomas, astrocytomas, and acoustic neuromas also express CCK (119–121).
- The tissue concentration of the long proCCK fragment is higher in atrial than ventricular myocytes.
- Also, thyroid C-cells produce CCK, but mainly as non-sulfated but amidated CCK-8 (17).
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Ligand recognition and G-protein coupling selectivity of cholecystokinin A receptor
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The plasma forms are CCK-58, -33, -22, and -8, whereas the small CCK-8 and -5 are potent neurotransmitters. Over the last decades, CCK expression has also been encountered in tumors (neuroendocrine tumors, cerebral astrocytomas, gliomas, acoustic neuromas, and specific pediatric tumors). Recently, a metastastic islet cell tumor was found to cause a specific CCKoma syndrome, suggesting that circulating CCK may be a useful tumor marker.
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Moreover, CCK-8 (sulfated as well as non-sulfated) has been reported to exert a wide specter of stimulation and inhibition on lymphocytes, macrophages, and cytokine release, with ensuing anti-inflammatory effects (108–111). The field is complex due to the many players; but the clinical impact of CCK in inflammatory diseases and endotoxin shock may be significant. The distal part of the gut is as mentioned abundantly innervated with CCK neurons (42, 90). It is therefore likely that an increase of intestinal motor activity by exogenous CCK (91) reflects neuronal control of intestinal muscles by CCK peptide transmission. Neuronal CCK acts both indirectly via acetylcholine release from postganglionic parasympathetic nerves and directly on muscle cells (49). The observation that CCK peptides stimulate intestinal blood flow is in harmony with the occurrence of CCK nerve terminals around blood vessels in the basal lamina propria and the submucosa (42).
We compared the CCK1R–Gs complex with other GPCR–Gs protein complexes. In each panel (Supplementary Fig. S5a, f), the complexes were aligned by the receptor, thus showing differences in the orientation of the Gs protein relative to the receptor. The αN orientation of CCK1R–Gs is closest to that of A2AR–Gs and β2AR–Gs, whereas the conformation of the α5 helix shows marked differences when compared to that in other GPCR–Gs complexes. Owning to the unique transducer–pocket conformation, the extreme C-terminus of Gs-α5 helix unexpectedly inserts into the cleft between TM6 and the TM7–H8 hinge (Supplementary Fig. S5b).
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According to the two CCK-8-bound structures, the interfaces between CCK-8 and CCKRs and the overall shape of the orthostatic pockets are conserved, consistent with previous prediction45. However, the sub-pocket for the TYS of CCK-8 is more positively charged in CCK1R attributed to N982.61, and R197ECL2 contributes to a beneficial charge–charge interaction with TYS of CCK-8 (Fig. 3a). Site-directed mutations R197ECL2M/A or N982.61A in CCK1R almost abolished CCK-8-triggered activation, implying the critical role of ECL2 in sulfated endogenous ligand recognition (Fig. 3b). The substitution of Q204ECL2A, the closest polar residue in CCK2R compared to CCK-8, does not affect CCK-8-induced Gq signaling of CCK2R measured by NanoBiT assay (Fig. 3d).