Local preconditioning by thermal stress accelerates microvascular thrombus formation

Shock

Volumn 31, Issue 6, 2009, Pages 627-633

  Rücker, Martin ^a,b,d   Laschke, Matthias W ^a   Stamm, Alexander ^a   Harder, Yves ^a   Vollmar, Brigitte ^c   Menger, Michael D ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

^d Department of Oral and Maxillofacial Surgery   (Germany)

Author keywords

Heat shock protein 32; Hyperthermia; Hypothermia; Preconditioning; Thrombomodulin; Thrombosis; Thrombospondin 1; Von Willebrand factor

Indexed keywords

ANTICOAGULANT AGENT; FLUORESCENT DYE; HEME OXYGENASE 1; THROMBOMODULIN; THROMBOSPONDIN 1; VON WILLEBRAND FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; CONDITIONING; CONTROLLED STUDY; COOLING; ENDOTHELIUM CELL; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; HINDLIMB; HYPERTHERMIA; IMMUNOHISTOCHEMISTRY; KINETICS; LIGHT EXPOSURE; NONHUMAN; PERIOSTEUM; PHOTOCHEMISTRY; RAT; SHAM PROCEDURE; SPRAGUE DAWLEY RAT; STRESS; TEMPERATURE STRESS; THROMBOGENESIS; THROMBOGENICITY; THROMBOSIS; THROMBUS; UPREGULATION;

ANIMALS; HEME OXYGENASE-1; HEMODYNAMICS; HINDLIMB; HYPERTHERMIA, INDUCED; HYPOTHERMIA; IMMUNOHISTOCHEMISTRY; MICROCIRCULATION; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROVESSELS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PHYSIOLOGICAL; THROMBOMODULIN; THROMBOSIS; THROMBOSPONDIN 1; VON WILLEBRAND FACTOR;

EID: 68049104311     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e318188f815     Document Type: Article

References (49)

1. Delano FA, Balete R, Schmid-Schonbein GW: Control of oxidative stress in microcirculation of spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 288:H805-H812, 2005.
2. Maytin M, Leopold J, Loscalzo J: Oxidant stress in the vasculature. Curr Atheroscler Rep 1:156-164, 1999.
3. Maack C, Kartes T, Kilter H, Schafers HJ, Nickenig G, Bohm M, Laufs U: Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation 108:1567-1574, 2003.
4. Lee YH, Wei FC, Lee J, Su MS, Chang YC: Effect of postischemic reperfusion on microcirculation and lipid metabolism of skeletal muscle. Microsurgery 16:522-527, 1995.
5. Yokoyama I, Negita M, Liu DG, Nagasaka T, Kobayashi T, Hayakawa A, Hayashi S, Nakao A: Prevention of free-radical induced apoptosis by induction of human recombinant Cu, Zn-SOD in pig endothelial cells. Transpl Int 15:220-225, 2002.
6. Ambrosio G, Tritto I, Golino P: Reactive oxygen metabolites and arterial thrombosis. Cardiovasc Res 34:445-452, 1997.
7. Weinzweig N, Gonzalez M: Free tissue failure is not an all-or-none phenomenon. Plast Reconstr Surg 96:648-660, 1995.
8. Lindenblatt N, Bordel R, Schareck W, Menger MD, Vollmar B: Vascular heme oxygenase-1 induction suppresses microvascular thrombus formation in vivo. Arterioscler Thromb Vasc Biol 24:601-606, 2004.
9. De Maio A: The heat-shock response. New Horiz 3:198-207, 1995.
10. Rücker M, Schäfer T, Roesken F, Spitzer WJ, Bauer M, Menger MD: Local heat-shock priming-induced improvement in microvascular perfusion in osteomyocutaneous flaps is mediated by heat-shock protein 32. Br J Surg 88:450-457, 2001.
11. Rücker M, Schäfer T, Roesken F, Spitzer WJ, Bauer M, Menger MD: Reduction of inflammatory response in composite flap transfer by local stress 8conditioning-induced heat-shock protein 32. Surgery 129:292-301, 2001.
12. Rücker M, Kadirogullari B, Vollmar B, Spitzer WJ, Menger MD: Improvement of nutritive perfusion after free tissue transfer by local heat shock-priming-induced preservation of capillary flowmotion. J Surg Res 123:102-108, 2005.
13. Maines MD: Heme oxygenase: function, multiplicity, regulatory mechanism, and clinical application. FASEB J 2:2557-2568, 1988.
14. Stocker R, Glazer AN, Ames BN: Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci 84:5918-5922, 1987.
15. Conway EM, Liu L, Nowakowski B, Steiner-Mosonyi M, Jackman RW: Heat shock of vascular endothelial cells induces an up-regulatory transcriptional response of the thrombomodulin gene that is delayed in onset and does not attenuate. J Biol Chem 269:22804-22810, 1994.
16. Ketis NV, Lawler J, Hoover RL, Karnovsky MJ: Effects of heat shock on the expression of thrombospondin by endothelial cells in culture. J Cell Biol 106:893-904, 1988.
17. Xie L, Chesterman CN, Hogg PJ: Control of von Willebrand factor multimer size by thrombospondin-1. J Exp Med 193:1341-1349, 2001.
18. Holland DB, Roberts SG, Wood EJ, Cunliffe WJ: Cold shock induces the synthesis of stress proteins in human keratinocytes. J Invest Dermatol 101:196-199, 1993.
19. Cullen KE, Sarge KD: Characterization of hypothermia-induced cellular stress response in mouse tissues. J Biol Chem 272:1742-1746, 1997.
20. Matz JM, LaVoi KP, Moen RJ, Blake MJ: Cold-induced heat shock protein expression in rat aorta and brown adipose tissue. Physiol Behav 60:1369-1374, 1996.
21. Rücker M, Roesken F, Vollmar B, Menger MD: A novel approach for comparative study of periosteum, muscle, subcutis, and skin microcirculation by intravital fluorescence microscopy. Microvasc Res 56:30-42, 1998.
22. Vollmar B, Schmits R, Kunz D, Menger MD: Lack of in vivo function of CD31 in vascular thrombosis. Thromb Haemost 85:160-164, 2001.
23. Baker M, Wayland H: On-line volume flow rate and velocity profile measurement for blood in microvessels. Microvasc Res 7:131-143, 1974.
24. Kubulus D, Amon M, Roesken F, Rücker M, Bauer I, Menger MD: Experimental cooling-induced preconditioning attenuates skin flap failure. Br J Surg 92:1432-1438, 2005.
25. Evers P, Uylings HBM: Microwave-stimulated antigen retrieval is pH and temperature dependent. J Histochem Cytochem 42:1555-1563, 1994.
26. Page C, Rose M, Yacoub M, Pigott R: Antigenic heterogeneity of vascular endothelium. Am J Pathol 141:673-683, 1992.
27. Jourdan A, Aguejouf O, Imbault P, Doutremepuich F, Inamo J, Doutremepuich C: Experimental thrombosis model induced by free radicals. Application to aspirin and other different substances. Thromb Res 79:109-123, 1995.
28. Laux V, Seiffge D: Platelet function in the dorsal skin fold chamber of the rat. In Vivo 7:45-51, 1993.
29. Roesken F, Ruecker M, Vollmar B, Boeckel N, Morgenstern E, Menger MD: A new model for quantitative in vivo microscopic analysis of thrombus formation and vascular recanalisation: the ear of the hairless (hr/hr) mouse. Thromb Haemost 78:1408-1414, 1997.
30. Herrmann KS: Platelet aggregation induced in the hamster cheek pouch by a photochemical process with excited fluorescein isothiocyanate-dextran. Microvasc Res 26:238-249, 1983.
31. Siegel JM, Markou CP, Ku DN, Hanson SR: A scaling law for wall shear rate through an arterial stenosis. J Biomech Eng 116:446-451, 1994.
32. Roesken F, Vollmar B, Rucker M, Seiffge D, Menger MD: In vivo analysis of antithrombotic effectiveness of recombinant hirudin on microvascular thrombus formation and recanalization. J Vasc Surg 28:498-505, 1998.
33. Sato M, Ohshima N: Effect of wall shear rate on thrombogenesis in microvessels of the rat mesentery. Circ Res 66:941-949, 1990.
34. Rosenblum WI: Aspects of endothelial malfunction and function in cerebral microvessels. Lab Invest 55:252-268, 1986.
35. Kubulus D, Roesken F, Amon M, Rucker M, Bauer M, Bauer I, Menger MD: Mechanism of the delay phenomenon: tissue protection is mediated by heme oxygenase-1. Am J Physiol Heart Circ Physiol 287:H2332-H2340, 2004.
36. Kinnunen I, Laurikainen E, Schrey A, Laippala P, Aitasalo K: Effect of acute ischemic preconditioning on blood-flow response in the epigastric pedicled rat flap. J Reconstr Microsurg 18:61-68, 2002.
37. Keyse SM, Tyrrell RM: Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A 86:99-103, 1989.
38. Furchgott RF, Jothianandan D: Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels 28:52-61, 1991.
39. Suematsu M, Goda N, Sano T, Kashiwagi S, Egawa T, Shinoda Y, Ishimura Y: Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J Clin Invest 96:2431-2437, 1995.
40. Brüne B, Ullrich V: Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 32:497-504, 1987.
41. Esmon CT: Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J 9:946-955, 1995.
42. Goto S, Ikeda Y, Saldivar E, Ruggeri ZM: Distinct mechanisms of platelet aggregation as a consequence of different shearing flow conditions. J Clin Invest 101:479-486, 1998.
43. Koller A, Dornyei G, Kaley G: Flow-induced responses in skeletal muscle venules: modulation by nitric oxide and prostaglandins. Am J Physiol 275:H831-H836, 1998.
44. Federici AB: The factor VIII/von Willebrand factor complex: basic and clinical issues. Haematologica 88:EREP02, 2003.
45. Chauhan AK, Kisucka J, Lamb CB, Bergmeier W, Wagner DD: von Willebrand factor and factor VIII are independently required to form stable occlusive thrombi in injured veins. Blood 109:2424-2429, 2007.
46. Furlan M: von Willebrand factor: molecular size and functional activity. Ann Hematol 72:341-348, 1996.
47. Rajagopalan S, Mascha E, Na J, Sessler DI: The effects of mild perioperative hypothermia on blood loss and transfusion requirement. Anesthesiology 108:71-77, 2008.
48. Lindenblatt N, Menger MD, Klar E, Vollmar B: Systemic hypothermia increases PAI-1 expression and accelerates microvascular thrombus formation in endotoxemic mice. Crit Care 10:R148, 2006.
49. Lindenblatt N, Menger MD, Klar E, Vollmar B: Sustained hypothermia accelerates microvascular thrombus formation in mice. Am J Physiol Heart Circ Physiol 289:H2680-H2687, 2005.