Introduction
Platelets play central roles in the vascular and immune systems, including in haemostasis, thrombosis, inflammation, host defence, and carcinogenesis. Tissue injury promptly activates resting platelets, triggering profound morphological changes and granule exocytosis resulting in the release of granular proteins (releasate) that mediate injury-related response processes. Whilst previous studies have documented the importance of protein glycosylation in platelet biology, the platelet glycome remains poorly defined. This study uses quantitative glycomics to map the dynamic and heterogeneous N-glycome of the resting and thrombin-activated platelet releasate.
Methods
Primary platelets were isolated from blood of healthy donors. Platelets were left unstimulated (n=10) or were either partially (n=6) or fully (n=5) activated with α-thrombin, a potent platelet agonist. Thrombin-mediated platelet activation was documented using PAC-1- and CD62P-centric flow cytometry. Proteins released from the platelets (releasate) were collected and separated from the intracellular proteins (lysate). The glycosylation of the platelet releasate was mapped and compared using quantitative PGC-LC-MS/MS-based glycomics.
Results
In total, 40 N-glycan isomers spanning 28 glycan compositions were identified in the platelet releasate fractions that were consistently rich in sialylated (>90%) and core fucosylated (>50%) complex-type N-glycans across all samples. Oligomannose, paucimannose, and bisecting GlcNAcylation were detected in lower abundance. Excitingly, a thrombin dose-dependent elevation of sialylated and fucosylated complex-type N-glycans displaying a higher degree of branching and an overall higher protein occupancy as well as a concomitant reduction in bisecting GlcNAcylation were observed under activated conditions. Interestingly, the N-glycome remodelling of the releasate from the activated platelets was found to accurately reflect the glycosylation of proteins residing in the platelet α-granules suggesting that these compartments are readily degranulated upon thrombin activation.
Conclusions
This is the first unbiased high-definition map of the dynamic N-glycome of the platelet releasate. Our glycome map represents a useful resource for future studies of platelet glycobiology.