Bioprotective role of platelet-derived microvesicles in hypothermia: Insight into the differential characteristics of peripheral and splenic platelets. Issue 223 (March 2023)

• Record Type: Journal Article
• Authors: Horioka, Kie; Tanaka, Hiroki; Okaba, Keisuke; Yamada, Shinnosuke; Hayakawa, Akira; Ishii, Namiko; Motomura, Ayumi; Inoue, Hiroyuki; Takauji, Shuhei; Isozaki, Shotaro; Ogawa, Katsuhiro; Yajima, Daisuke; Druid, Henrik; Pakanen, Lasse; Porvari, Katja
• Is Part Of: Thrombosis research. Issue 223(2023)
• Page Start: 155
• Page End: 167
• Publication Date: 2023-03
• Subjects: Hypothermia -- Platelet -- Spleen -- Platelet-derived microvesicles -- Shivering -- Muscle repair; Thrombosis -- Periodicals; 616.135
• DOI: 10.1016/j.thromres.2023.01.006
• Languages: English
• ISSNs: 0049-3848

Abstract

Abstract: Background: Most platelets are present in peripheral blood, but some are stored in the spleen. Because the tissue environments of peripheral blood vessels and the spleen are quite distinct, the properties of platelets present in each may also differ. However, no studies have addressed this difference. We previously reported that hypothermia activates splenic platelets, but not peripheral blood platelets, whose biological significance remains unknown. In this study, we focused on platelet-derived microvesicles (PDMVs) and analyzed their biological significance connected to intrasplenic platelet activation during hypothermia. Methods: C57Bl/6 mice were placed in an environment of −20 °C, and their rectal temperature was decreased to 15 °C to model hypothermia. Platelets and skeletal muscle tissue were collected and analyzed for their interactions. Results: Transcriptomic changes between splenic and peripheral platelets were greater in hypothermic mice than in normal mice. Electron microscopy and real-time RT-PCR analysis revealed that platelets activated in the spleen by hypothermia internalized transcripts, encoding tissue repairing proteins, into PDMVs and released them into the plasma. Plasma microvesicles from hypothermic mice promoted wound healing in the mouse myoblast cell line C2C12. Skeletal muscles in hypothermic mice were damaged but recovered within 24 h after rewarming. However, splenectomy delayed recovery from skeletal muscle injury after the mice were rewarmed. Conclusions: These results indicate that PDMVs released from activated platelets in the spleen play an important role in the repair of skeletal muscle damaged by hypothermia. Graphical abstract: Unlabelled Image Highlights: Platelets in the spleen and peripheral blood may have different properties. The splenic platelets were activated by hypothermia. Hypothermia induces release of PDMVs containing tissue repair transcripts from splenic platelets. PDMVs facilitate skeletal muscle recovery from damage caused by hypothermia.