Von Willebrand factor is reversibly decreased during torpor in 13-lined ground squirrels

详细信息    查看全文

• 作者：Scott Cooper ; Shawn Sell ; Luke Nelson…
• 关键词：Factor VIII ; Factor IX ; Deep vein thrombosis ; Hibernation ; Neutrophil ; DNA NET
• 刊名：Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：186
• 期：1
• 页码：131-139
• 全文大小：548 KB
• 参考文献：Badimon L, Badimon JJ, Turitto VT, Fuster V (1989) Role of von Willebrand factor in mediating platelet-vessel wall interaction at low shear rate; the importance of perfusion conditions. Blood 73:961–967PubMed
  Bertina RM (2003) Elevated clotting factor levels and venous thrombosis. Pathophysiol Haemost Thromb 33:395–400CrossRef PubMed
  Bittar LF, de Paula EV, Mello TB, Siqueira LH, Orsi FL, Annichino-Bizzacchi JM (2010) Polymorphisms and mutations in vWF and ADAMTS13 genes and their correlation with plasma levels of FVIII and vWF in patients with deep venous thrombosis. Clin Appl Thromb Hemost 17:514–518CrossRef PubMed
  Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, Gallant M, Martinod K, Ten Cate H, Hofstra L, Crijns HJ, Wagner DD, Kietselaer BL (2013) Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 33:2032–2040CrossRef PubMed PubMedCentral
  Bouma HR, Dugbartey GJ, Boerema AS, Talaei F, Herwig A, Goris M, van Buiten A, Strijkstra AM, Carey HV, Henning RH, Kroese FG (2013) Reduction of body temperature governs neutrophil retention in hibernating and nonhibernating animals by margination. J Leukoc Biol 94:431–437CrossRef PubMed
  Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Kollnberger M, Wakefield TW, Lammle B, Massberg S, Wagner DD (2011) von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood 117:1400–1407CrossRef PubMed PubMedCentral
  Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD (2012) Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 10:136–144CrossRef PubMed PubMedCentral
  Casari C, Lenting PJ, Wohner N, Christophe OD, Denis CV (2013) Clearance of von Willebrand factor. J Thromb Haemost 11(Suppl 1):202–211CrossRef PubMed
  Chauhan AK, Kisucka J, Lamb CB, Bergmeier W, Wagner DD (2007) von Willebrand factor and factor VIII are independently required to form stable occlusive thrombi in injured veins. Blood 109:2424–2429CrossRef PubMed PubMedCentral
  Chauhan AK, Kisucka J, Brill A, Walsh MT, Scheiflinger F, Wagner DD (2008) ADAMTS13: a new link between thrombosis and inflammation. J Exp Med 205:2065–2074CrossRef PubMed PubMedCentral
  Cooper ST, Richters KE, Melin TE, Liu ZJ, Hordyk PJ, Benrud RR, Geiser LR, Cash SE, Simon Shelley C, Howard DR, Ereth MH, Sola-Visner MC (2012) The hibernating 13-lined ground squirrel as a model organism for potential cold storage of platelets. Am J Physiol Regul Integr Comp Physiol 302:R1202–1208CrossRef PubMed PubMedCentral
  de Vrij EL, Vogelaar PC, Goris M, Houwertjes MC, Herwig A, Dugbartey GJ, Boerema AS, Strijkstra AM, Bouma HR, Henning RH (2014) Platelet dynamics during natural and pharmacologically induced torpor and forced hypothermia. PLoS ne 9:e93218CrossRef
  Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, Wagner DD (1998) A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci USA 95:9524–9529CrossRef PubMed PubMedCentral
  Diaz JA, Fuchs TA, Jackson TO, Kremer Hovinga JA, Lammle B, Henke PK, Myers DD Jr., Wagner DD, Wakefield TW (2013) Plasma DNA is elevated in patients with deep vein thrombosis. J Vasc Surg Venous Lymphat Disord 1:341–348CrossRef PubMedCentral
  Diener JL, Daniel Lagasse HA, Duerschmied D, Merhi Y, Tanguay JF, Hutabarat R, Gilbert J, Wagner DD, Schaub R (2009) Inhibition of von Willebrand factor-mediated platelet activation and thrombosis by the anti-von Willebrand factor A1-domain aptamer ARC1779. J Thromb Haemost 7:1155–1162CrossRef PubMed
  Esmon CT (2009) Basic mechanisms and pathogenesis of venous thrombosis. Blood Rev 23:225–229CrossRef PubMed PubMedCentral
  Flinterman LE, van Hylckama Vlieg A, Rosendaal FR, Doggen CJ (2010) Venous thrombosis of the upper extremity: effect of blood group and coagulation factor levels on risk. Br J Haematol 149:118–123CrossRef PubMed
  Flood VH, Gill JC, Morateck PA, Christopherson PA, Friedman KD, Haberichter SL, Hoffmann RG, Montgomery RR (2011) Gain-of-function GPIb ELISA assay for VWF activity in the Zimmerman Program for the Molecular and Clinical Biology of VWD. Blood 117:e67–74CrossRef PubMed PubMedCentral
  Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD (2010) Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 107:15880–15885CrossRef PubMed PubMedCentral
  Fuchs TA, Brill A, Wagner DD (2012) Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler Thromb Vasc Biol 32:1777–1783CrossRef PubMed PubMedCentral
  Hassenpflug WA, Budde U, Obser T, Angerhaus D, Drewke E, Schneppenheim S, Schneppenheim R (2006) Impact of mutations in the von Willebrand factor A2 domain on ADAMTS13-dependent proteolysis. Blood 107:2339–2345CrossRef PubMed
  Heit JA, Silverstein MD, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ 3rd (1999) Predictors of survival after deep vein thrombosis and pulmonary embolism: a population-based, cohort study. Arch Intern Med 159:445–453CrossRef PubMed
  Heit JA, Silverstein MD, Mohr DN, Petterson TM, O’Fallon WM, Melton LJ 3rd (2000) Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case-control study. Arch Intern Med 160:809–815CrossRef PubMed
  Herbert JM, Bernat A, Maffrand JP (1992) Importance of platelets in experimental venous thrombosis in the rat. Blood 80:2281–2286PubMed
  Jaffe EA, Hoyer LW, Nachman RL (1974) Synthesis of von Willebrand factor by cultured human endothelial cells. Proc Natl Acad Sci USA 71:1906–1909CrossRef PubMed PubMedCentral
  Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13:159–175CrossRef PubMed
  Kuipers S, Cannegieter SC, Doggen CJ, Rosendaal FR (2009) Effect of elevated levels of coagulation factors on the risk of venous thrombosis in long-distance travelers. Blood 113:2064–2069CrossRef PubMed
  Lechler E, Penick GD (1963) Blood clotting defect in hibernating ground squirrels (Citellus tridecemlineatus). Am J Physiol 205:985–988PubMed
  Lindenblatt N, Menger MD, Klar E, Vollmar B (2005) Sustained hypothermia accelerates microvascular thrombus formation in mice. Am J Physiol Heart Circ Physiol 289:H2680–2687CrossRef PubMed
  Lyman CP, O’brien RC (1960) Circulatory changes in the thirteen-lined ground squirrel during the hibernation cycle. Bull Mus Comp Zool 124:353–372
  Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenbock A, Simon D, Laimer D, Bangert C, Kammerlander AA, Mascherbauer J, Winter MP, Distelmaier K, Adlbrecht C, Preissner KT, Lang IM (2015) Coronary neutrophil extracellular trap burden and DNase activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 116:1182–1192CrossRef PubMed
  Markus HS, McCollum C, Imray C, Goulder MA, Gilbert J, King A (2011) The von Willebrand inhibitor ARC1779 reduces cerebral embolization after carotid endarterectomy: a randomized trial. Stroke 42:2149–2153CrossRef PubMed
  McArthur MD, Milsom WK (1991) Changes in ventilation and respiratory sensitivity associated with hibernation in Columbian (Spermophilus columbianus) and golden-mantled (Spermophilis lateralis) ground squirrels. Physiol Zool 64:940–959
  Michener GR (1989) Sexual differences in interyear survival and life-span of Richardson’s ground squirrels. Can J Zool 67:1827–1831CrossRef
  Nachman R, Levine R, Jaffe EA (1977) Synthesis of factor VIII antigen by cultured guinea pig megakaryocytes. J Clin Invest 60:914–921CrossRef PubMed PubMedCentral
  Pendu R, Christophe OD, Denis CV (2009) Mouse models of von Willebrand disease. J Thromb Haemost 7(Suppl 1):61–64CrossRef PubMed
  Pengelley ET, Asmundson SM (1969) Free-running periods of endogenous circadian rhythms in the golden mantled ground squirrel, Citellus lateralis. Comp Biochem Physiol 30:177–183CrossRef PubMed
  Pivorun EB, Sinnamon WB (1981) Blood coagulation studies in normothermic, hibernating, and aroused Spermophilus franklini. Cryobiology 18:515–520CrossRef PubMed
  Pruss CM, Golder M, Bryant A, Hegadorn C, Haberichter S, Lillicrap D (2012) Use of a mouse model to elucidate the phenotypic effects of the von Willebrand factor cleavage mutants, Y1605A/M1606A and R1597W. J Thromb Haemost 10:940–950CrossRef PubMed
  Reddick RL, Poole BL, Penick GD (1973) Thrombocytopenia of hibernation. Mechanism of induction and recovery. Lab Invest 28:270–278PubMed
  Ribeiro DD, Lijfering WM, Barreto SM, Rosendaal FR, Rezende SM (2012) Epidemiology of recurrent venous thrombosis. Braz J Med Biol Res 45:1–7CrossRef PubMed PubMedCentral
  Rydz N, Swystun LL, Notley C, Paterson AD, Riches JJ, Sponagle K, Boonyawat B, Montgomery RR, James PD, Lillicrap D (2013) The C-type lectin receptor CLEC4M binds, internalizes, and clears von Willebrand factor and contributes to the variation in plasma von Willebrand factor levels. Blood 121:5228–5237CrossRef PubMed PubMedCentral
  Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67:395–424CrossRef PubMed
  Sherman PW, Morton ML (1984) Demography of Belding’s Ground Squirrels. Ecology 65:1617–1628CrossRef
  Smith DE, Lewis YS, Svihla G (1954) Prolongation of clotting time in the dormant bat (Myotis lucifugus). Experientia 10:218CrossRef PubMed
  Suomalainen P, Lehto E (1952) Prolongation of clotting time in hibernation. Experientia 8:65CrossRef PubMed
  Svihla A, Bowman H, Pearson R (1952a) Prolongation of blood clotting time in the dormant hamster. Science 115:272CrossRef PubMed
  Svihla A, Bowman H, Ritenour R (1952b) Relation of prothrombin to the prolongation of clotting time in aestivating ground squirrels. Science 115:306–307CrossRef PubMed
  Svihla A, Bowman H, Ritenour R (1953) Stimuli and their effects on awakening of dormant ground squirrels. Am J Physiol 172:681–683PubMed
  Sweeney JD, Novak EK, Reddington M, Takeuchi KH, Swank RT (1990) The RIIIS/J inbred mouse strain as a model for von Willebrand disease. Blood 76:2258–2265PubMed
  von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S (2012) Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 209:819–835CrossRef
  Wagner DD, Frenette PS (2008) The vessel wall and its interactions. Blood 111:5271–5281CrossRef PubMed PubMedCentral
  Weiss HJ, Sussman II, Hoyer LW (1977) Stabilization of factor VIII in plasma by the von Willebrand factor. Studies on posttransfusion and dissociated factor VIII and in patients with von Willebrand’s disease. J Clin Invest 60:390–404CrossRef PubMed PubMedCentral
  Zatzman ML (1984) Renal and cardiovascular effects of hibernation and hypothermia. Cryobiology 21:593–614CrossRef PubMed
  
• 作者单位：Scott Cooper (1)
  Shawn Sell (1)
  Luke Nelson (1)
  Jennifer Hawes (1)
  Jacob A. Benrud (1)
  Bridget M. Kohlnhofer (1)
  Bradley R. Burmeister (1)
  Veronica H. Flood (2)
  
  1. University of Wisconsin-La Crosse, La Crosse, WI, USA
  2. Medical College of Wisconsin, Milwaukee, WI, 53226, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Biomedicine
  Human Physiology
  Zoology
  Animal Physiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-136X

文摘

During torpor in a hibernating mammal, decreased blood flow increases the risk of blood clots such as deep vein thrombi (DVT). In other animal models platelets, neutrophils, monocytes and von Willebrand factor (VWF) have been found in DVT. Previous research has shown that hibernating mammals decrease their levels of platelets and clotting factors VIII (FVIII) and IX (FIX), increasing both bleeding time and activated partial thromboplastin time. In this study, FVIII, FIX and VWF activities and mRNA levels were measured in torpid and non-hibernating ground squirrels (Ictidomys tridecemlineatus). Here, we show that VWF high molecular weight multimers, collagen-binding activity, lung mRNA and promoter activity decrease during torpor. The VWF multimers reappear in plasma within 2 h of arousal in the spring. Similarly, FIX activity and liver mRNA both dropped threefold during torpor. In contrast, FVIII liver mRNA levels increased twofold while its activity dropped threefold, consistent with a post-transcriptional decrease in FVIII stability in the plasma due to decreased VWF levels. Finally, both neutrophils and monocytes are decreased eightfold during torpor which could slow the formation of DVT. In addition to providing insight in how blood clotting can be regulated to allow mammals to survive in extreme environments, hibernating ground squirrels provide an interesting model for studying.