Platelet dynamics during natural and pharmacologically induced torpor and forced hypothermia

Edwin L. de Vrij*, Pieter C. Vogelaar, Maaike Goris, Martin C. Houwertjes, Annika Herwig, George J. Dugbartey, Ate S. Boerema, Arjen M. Strijkstra, Hjalmar R. Bouma, Robert H. Henning

*Corresponding author for this work

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Abstract

Hibernation is an energy-conserving behavior in winter characterized by two phases: torpor and arousal. During torpor, markedly reduced metabolic activity results in inactivity and decreased body temperature. Arousal periods intersperse the torpor bouts and feature increased metabolism and euthermic body temperature. Alterations in physiological parameters, such as suppression of hemostasis, are thought to allow hibernators to survive periods of torpor and arousal without organ injury. While the state of torpor is potentially procoagulant, due to low blood flow, increased viscosity, immobility, hypoxia, and low body temperature, organ injury due to thromboembolism is absent. To investigate platelet dynamics during hibernation, we measured platelet count and function during and after natural torpor, pharmacologically induced torpor and forced hypothermia. Splenectomies were performed to unravel potential storage sites of platelets during torpor. Here we show that decreasing body temperature drives thrombocytopenia during torpor in hamster with maintained functionality of circulating platelets. Interestingly, hamster platelets during torpor do not express P-selectin, but expression is induced by treatment with ADP. Platelet count rapidly restores during arousal and rewarming. Platelet dynamics in hibernation are not affected by splenectomy before or during torpor. Reversible thrombocytopenia was also induced by forced hypothermia in both hibernating (hamster) and non-hibernating (rat and mouse) species without changing platelet function. Pharmacological torpor induced by injection of 5'-AMP in mice did not induce thrombocytopenia, possibly because 5'-AMP inhibits platelet function. The rapidness of changes in the numbers of circulating platelets, as well as marginal changes in immature platelet fractions upon arousal, strongly suggest that storage-and-release underlies the reversible thrombocytopenia during natural torpor. Possibly, margination of platelets, dependent on intrinsic platelet functionality, governs clearance of circulating platelets during torpor.

Original languageEnglish
Article numbere93218
Number of pages12
JournalPLoS ONE
Volume9
Issue number4
DOIs
Publication statusPublished - 10-Apr-2014

Keywords

  • HIBERNATING GROUND-SQUIRRELS
  • ISCHEMIA-REPERFUSION INJURY
  • LOW-TEMPERATURE
  • SYRIAN-HAMSTER
  • COLD-STORAGE
  • BLOOD-FLOW
  • ACTIVATION
  • MECHANISM
  • AGGREGATION
  • COAGULATION

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