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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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The release from neurons has been examined directly in brain slices and synaptosomes (56, 57). Potassium-induced depolarization caused a calcium-dependent release of CCK-8. Similarly, depolarization releases CCK peptides from the hypothalamic dopamine neurons that innervate the intermediate lobe of the pituitary (58). Cholecystokinin (CCK) is member of a family of regulatory peptides with a remarkably well preserved C-terminal sequence (1–3). The family also includes frog skin peptides (caerulein and phyllocaerulein) and the protochordean neuropeptide cionin, but in mammals, CCK and gastrin are the only family members (Figure 1). All relevant data were included in the manuscript or Supplementary information.
Cholecystokinin—From Local Gut Hormone to Ubiquitous Messenger
Accordingly, adult cardiomyocytes in mice, rats, and pigs contain substantial amounts of proCCK protein (113). The processing, however, of cardiac proCCK is unique, as the result is a long triple-sulfated and N-terminally truncated fragment 25–94 with only trace amounts of the conventionally amidated and sulfated CCK peptides (113). The tissue concentration of the long proCCK fragment is higher in atrial than ventricular myocytes. The long proCCK fragment is released to plasma and may find use as a marker of the risk of mortality in heart failure patients (113). Cholecystokinin immunoreactivity has consistently been found to be expressed in human and rat mononuclear cells in blood (106, 107).
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- In addition, most assays for measurement of CCK in plasma and elsewhere lacked specificity and sensitivity (10–12).
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In this paper, we reported four high-resolution cryo-EM structures of CCK1R and CCK2R signaling complexes. Sulfation of CCK and gastrin in the body is highly regulated by sulfotransferase (SULT) enzymes with tissue-specific expression patterns, e.g., SULT4 is predominantly expressed in the brain61. The sulfation level of CCK and gastrin is also correlated with sub-cellular and cellular distribution. Interestingly, the non-sulfated CCK is enriched in neuronal cell bodies, whereas the sulfated CCK predominantly distributes in the nerve terminals62. CCKRs differentially recognize the sulfated and non-sulfated ligands enabling subtle and precisely regulated responses to extracellular stimuli.
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