Platelet Dynamics during Natural and Pharmacologically Induced Torpor and Forced Hypothermia
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{"title"=>"Platelet dynamics during natural and pharmacologically induced torpor and forced hypothermia", "type"=>"journal", "authors"=>[{"first_name"=>"Edwin L.", "last_name"=>"De Vrij", "scopus_author_id"=>"55581208100"}, {"first_name"=>"Pieter C.", "last_name"=>"Vogelaar", "scopus_author_id"=>"56134799000"}, {"first_name"=>"Maaike", "last_name"=>"Goris", "scopus_author_id"=>"25521656500"}, {"first_name"=>"Martin C.", "last_name"=>"Houwertjes", "scopus_author_id"=>"6603557204"}, {"first_name"=>"Annika", "last_name"=>"Herwig", "scopus_author_id"=>"23004983800"}, {"first_name"=>"George J.", "last_name"=>"Dugbartey", "scopus_author_id"=>"55361824500"}, {"first_name"=>"Ate S.", "last_name"=>"Boerema", "scopus_author_id"=>"8552484900"}, {"first_name"=>"Arjen M.", "last_name"=>"Strijkstra", "scopus_author_id"=>"6603831786"}, {"first_name"=>"Hjalmar R.", "last_name"=>"Bouma", "scopus_author_id"=>"35789891200"}, {"first_name"=>"Robert H.", "last_name"=>"Henning", "scopus_author_id"=>"35426186600"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84899503513", "sgr"=>"84899503513", "pui"=>"372974702", "pmid"=>"24722364", "doi"=>"10.1371/journal.pone.0093218"}, "id"=>"191d56fc-4e9c-33ad-981b-cc1f471531dd", "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.", "link"=>"http://www.mendeley.com/research/platelet-dynamics-during-natural-pharmacologically-induced-torpor-forced-hypothermia", "reader_count"=>38, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>7, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>7, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>7, "Medicine and Dentistry"=>13, "Agricultural and Biological Sciences"=>7, "Neuroscience"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>13}, "Neuroscience"=>{"Neuroscience"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>2, "Belgium"=>1, "Japan"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1459657"], "description"=>"<p>A) Pharmacologically induced torpor by 5′-AMP in mice does not decrease platelet count during torpor and shows an increase upon arousal. Body temperature drops during torpor and restores during arousal. B) Leukocyte level decreases with falling body temperature. C) The correlation of decreased body temperature and reduced platelet count is prominent in deep hibernating hamster (n = 31), daily hibernating hamster (n = 15), forced-cooled hamster (n = 8, multiple sampling), forced-cooled rat (n = 25), and forced-cooled mouse (n = 15), but absent in 5′-AMP induced torpor in mice (n = 10). Bars represent mean ± SEM of 5 to 6 animals per group. *P<0.05, **P<0.01.</p>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "induced", "torpor", "platelet"], "article_id"=>995145, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093218.g003", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pharmacologically_induced_torpor_by_5_8242_AMP_does_not_decrease_platelet_count_despite_decreased_body_temperature_/995145", "title"=>"Pharmacologically induced torpor by 5′-AMP does not decrease platelet count despite decreased body temperature.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 03:48:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1459663", "https://ndownloader.figshare.com/files/1459664", "https://ndownloader.figshare.com/files/1459665", "https://ndownloader.figshare.com/files/1459666"], "description"=>"<div><p>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.</p></div>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "pharmacologically", "induced", "torpor", "forced"], "article_id"=>995151, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0093218.s001", "https://dx.doi.org/10.1371/journal.pone.0093218.s002", "https://dx.doi.org/10.1371/journal.pone.0093218.s003", "https://dx.doi.org/10.1371/journal.pone.0093218.s004"], "stats"=>{"downloads"=>8, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Platelet_Dynamics_during_Natural_and_Pharmacologically_Induced_Torpor_and_Forced_Hypothermia_/995151", "title"=>"Platelet Dynamics during Natural and Pharmacologically Induced Torpor and Forced Hypothermia", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-04-10 03:48:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1459661"], "description"=>"<p>Velocity and max amplitude of aggregation of rat platelets in response to 20 μM of ADP is not significantly different between anesthetized, cooled and rewarmed rats. Values are mean ± SEM of 10 rats per group.</p>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "forced-cooled"], "article_id"=>995150, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093218.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Aggregation_of_platelets_from_forced_cooled_rats_/995150", "title"=>"Aggregation of platelets from forced-cooled rats.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-04-10 03:48:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1459659"], "description"=>"<p>A) Immature platelet fraction (IPF) is increased in torpor, but decreases in arousal toward normal euthermic percentage in Syrian hamster. B) In rat, IPF decreases during cooling and rewarming. C) In mice IPF only increases during arousal. D) Splenectomy prior to hibernation does not inhibit induction of thrombocytopenia in torpor. E) Splenectomy during torpor does not prevent restoration of platelet count during the subsequent arousal. Bars represent mean ± SEM of 4 to 12 animals per group. *P<0.05, **P<0.01.</p>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "circulating", "platelet", "numbers", "arousal", "rewarming", "originate", "spleen"], "article_id"=>995147, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093218.g004", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Restoration_of_circulating_platelet_numbers_during_arousal_and_rewarming_does_not_originate_from_spleen_or_bone_marrow_/995147", "title"=>"Restoration of circulating platelet numbers during arousal and rewarming does not originate from spleen or bone marrow.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 03:48:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1459642"], "description"=>"<p>A) During spontaneous entrance into torpor body temperature gradually declines from 35°C to 8°C in a matter of hours. B) Increase in body temperature during a spontaneous arousal, demonstrating the rapid increase to euthermic level. Line represents one of thirty-one Syrian hamsters, measured with an intraperitoneal implanted Thermochron iButton. C) Normal platelet count in summer-euthermic Syrian hamster (n = 5, open dots; n = 7, black dots). D) Platelet count decreases with lower body temperature from euthermic stage to deep torpor in the Syrian hamster (n = 31), both during natural hibernation as well as during forced hypothermia (n = 8, multiple sampling). Curves from D) and E) are fitted to a polynomial quadratic curve with equation y = y<sub>0</sub>+ax+bx<sup>2</sup> and constraints of y<sub>0</sub>>0 and y<sub>0</sub>≤ lowest platelet count for torpor. Black dots (•) are natural hibernating hamsters, open dots (°) are forced-cooled hamsters. E) Platelet number increases rapidly to a normal level during arousal (n = 42) or rewarming from forced hypothermia (n = 7, multiple sampling). F) P-selectin positive platelets are absent in torpid hamsters. G) The platelets are activatible following addition of ADP and the subsequent percentage of P-selectin positive platelets is similar to euthermic and aroused animals. H) The P-selectin expression level per platelet was significantly decreased in non-activated platelets from torpor compared to euthermia and arousal hamsters. I) Upon activation with ADP, P-selectin expression reaches similar levels in euthermia (eu), torpor (trp) and arousal (arsl). Please note that F-I are n = 2 per group. J) Circulating platelet count is reduced during daily torpor in the Djungarian hamster, and restored upon arousal. Bars represent mean ± SEM of 5 to 9 animals per group. *P<0.05, **P<0.01.</p>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "platelet", "torpor", "arousal", "hibernating", "syrian", "hamster", "ambient"], "article_id"=>995127, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093218.g001", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Body_temperature_dependent_platelet_count_of_functional_platelets_during_torpor_and_arousal_in_natural_hibernating_Syrian_hamster_at_5_176_C_ambient_temperature_/995127", "title"=>"Body temperature dependent platelet count of functional platelets during torpor and arousal in natural hibernating Syrian hamster at 5°C ambient temperature.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 03:48:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/1459654"], "description"=>"<p>A) Rats forced to hypothermia of 15°C have a decreased amount of platelets, which partially restores during rewarming. B) No difference in amount of activatable platelets from anestethized euthermic, cooled or rewarmed rats. C) Unchanged P-selectin expression at all time points in both non-activated and activated whole blood samples. D) Unchanged aggregometry at all time points upon addition of ADP. E) Mathematical approach for velocity and max amplitude of platelet aggregation. ν, velocity of aggregation; Δ%, change in percentage light transmission; Δt, timespan over which velocity is determined; MA, maximum aggregation in % light transmission. F) Mice forced to hypothermia of 20°C have a decreased amount of platelets, which partially restores during rewarming. Panels G) and H) show unchanged platelet P-selectin expression between time points in non-activated and activated whole blood samples. Bars represent mean ± SEM of 7 to 27 rats per group and 3 to 9 mice per group. *P<0.05, **P<0.01.</p>", "links"=>[], "tags"=>["anatomy", "Body fluids", "blood", "platelets", "Cardiovascular anatomy", "Biochemistry", "metabolism", "Energy metabolism", "cell biology", "Cellular types", "Animal cells", "Immune cells", "Chronobiology", "Cryobiology", "immunology", "Immune system", "bone marrow", "physiology", "Cardiovascular physiology", "Blood circulation", "Physiological processes", "homeostasis", "sleep", "Veterinary science", "Animal types", "Laboratory animals", "Zoology", "Animal behavior", "anesthesiology", "anesthesia", "cardiology", "Myocardial infarction", "hematology", "Blood coagulation", "Coagulation disorders", "hemostasis", "Perioperative hemostasis", "hemodynamics", "thrombocytopenia", "Surgical and invasive medical procedures", "Vascular medicine", "thromboembolism", "Venous thromboembolism", "stroke", "platelet", "preserved", "forced"], "article_id"=>995141, "categories"=>["Biological Sciences"], "users"=>["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"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0093218.g002", "stats"=>{"downloads"=>5, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Decreased_platelet_count_with_preserved_function_during_forced_hypothermia_/995141", "title"=>"Decreased platelet count with preserved function during forced hypothermia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 03:48:26"}

PMC Usage Stats | Further Information

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