Mechanism of the delay phenomenon: Tissue protection is mediated by heme oxygenase-1

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 287, Issue 5 56-5, 2004, Pages

  Kubulus, Darius ^a   Roesken, Frank ^a   Amon, Michaela ^a   Rücker, Martin ^a   Bauer, Michael ^a   Bauer, Inge ^a   Menger, Michael D ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Carbon monoxide; Heat shock protein 32; Microcirculation; Mouse ear; Skin flap; Tissue necrosis; Vitamin E analog

Indexed keywords

HEAT SHOCK PROTEIN 32; HEME OXYGENASE 1; TROLOX C;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ISCHEMIA; MICROCIRCULATION; MOUSE; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; SKIN FLAP; SKIN FLAP SURVIVAL; TISSUE NECROSIS; VASODILATATION;

ANIMALS; ANTIOXIDANTS; BILIVERDINE; CARBON MONOXIDE; CONDITIONING (PSYCHOLOGY); CYTOPROTECTION; EAR; FEMALE; GENE EXPRESSION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; ISCHEMIA; MALE; MEMBRANE PROTEINS; MICE; MICE, NUDE; MICROCIRCULATION; NECROSIS; SKIN; SURGICAL FLAPS; TIME FACTORS; VASODILATION;

EID: 7244226472     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.01109.2003     Document Type: Article

References (47)

1. Adanali G, Ozer K, and Siemionow M. Early and late effects of ischemic preconditioning on microcirculation of skeletal muscle flaps. Plast Reconstr Surg 109: 1344-1351, 2002.
2. Amon M, Menger MD, and Vollmar B. Heme oxygenase and nitric oxide synthase mediate cooling-associated protection against TNF-α-induced microcirculatory dysfunction and apoptotic cell death. FASEB J 17: 175-185, 2003.
3. Barker JH, Frank J, Bidiwala SB, Stengel CK, Carroll SM, Carroll CM, van Aalst V, and Anderson GL. An animal model to study microcirculatory changes associated with vascular delay. Br J Plast Surg 52: 133-142, 2002.
4. Barker JH, Hammersen F, Bondar I, Galla TJ, Menger MD, Gross W, and Messmer K. Direct monitoring of nutritive blood flow in a failing skin flap: the hairless mouse ear skin-flap model. Plast Reconstr Surg 84: 303-313, 1989.
5. Barker JH, Hammersen F, Bondar I, Uhl E, Galla TJ, Menger MD, and Messmer K. The hairless mouse ear for in vivo studies of skin microcirculation. Plast Reconstr Surg 83: 948-959, 1989.
6. Barthe Garcia P, Suarez Nieto C, and Rojo Ortega JM. Morphological changes in the vascularization of delayed flaps in rabbits. Br J Plast Surg 44: 285-290, 1991.
7. Bauer I, Wanner GA, Rensing H, Alte C, Miescher EA, Wolf B, Pannen BHJ, Clemens MG, and Bauer M. Expression pattern of heme oxygenase isoenzymes 1 and 2 in normal and stress exposed rat liver. Hepatology 27: 829-838, 1998.
8. Bauer M and Bauer I. Heme oxygenase-1: redoxregulation and role in the hepatic response to oxidative stress. Antiox Redox Signal 4: 749-758, 2002.
9. Black CE, Huang N, Neligan PC, Forrest CR, Lipa JE, and Pang CY. Vasoconstrictor effect and mechanism of action of endothelin-1 in human radial artery and vein: implication of skin flap vasospasm. J Cardiovasc Pharmacol 41: 460-467, 2003.
10. Braverman IM and Sibley J. Ultrastructural and three-dimensional analysis of the contractile cells of the cutaneous microvasculature. J Invest Dermatol 95: 90-96, 1990.
11. Brüne B and Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 32: 497-504, 1987.
12. Cederna PS, Chang P, Pittet-Cuenod BM, Razaboni RM, and Cram AE. The effect of the delay phenomenon on the vascularity of rabbit abdominal cutaneous island flaps. Plast Reconstr Surg 99: 183-193, 1997.
13. Choi AM and Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15: 9-19, 1996.
14. Costa LE, Llesuy S, and Boveris A. Active oxygen species in the liver of rats submitted to chronic hypobaric hypoxia. Am J Physlol Cell Physiol 264: C1395-C1400, 1993.
15. Elbirt KK and Bonkovsky HL. Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 111: 438-447, 1999.
16. Furchgott RF and 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.
17. Gaudio E, Pannarale L, Caggiati A, and Marinozzi G. A three-dimensional study of the morphology and topography of pericytes in the microvascular bed of skeletal muscle. Scanning Microsc 4: 491-499, 1990.
18. Gonzales S, Erario MA, and Tomaro ML. Heme oxygenase-1 induction and dependent increase in ferritin. A protective antioxidant stratagem in hemin-treated rat brain. Dev Neurosci 24: 161-168, 2002.
19. Guba AM Jr. Study of the delay phenomenon in axial pattern flaps in pigs. Plast Reconstr Surg 63: 550-554, 1979.
20. Hampton CR, Shimamoto A, Rothnie CL, Griscavage-Ennis J, Chong A, Dix DJ, Verrier ED, and Pohlman TH. HSP70.1, and -70.3 are required for late-phase protection induced by ischemic preconditioning of mouse hearts. Am J Physiol Heart Circ Physiol 285: H866-H874, 2003.
21. Hirschi KK and D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res 32: 687-698, 1996.
22. Hockel M and Burke JF. Angiotropin treatment prevents flap necrosis and enhances dermal regeneration in rabbits. Arch Surg 124: 693-698, 1989.
23. Kerrigan CL. Skin flap failure: pathophysiology. Plast Reconstr Surg 72: 767-777, 1983.
24. Kerrigan CL. Skin flap perfusion and bFGF. Ann Plast Surg 32: 365-366, 1994.
25. Keyse SM and 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 USA 86: 99-103, 1989.
26. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2: 2557-2568, 1988.
27. McCoubrey WK Jr, Huang TJ, and Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247: 725-732, 1997.
28. Menger MD, Barker JH, and Messmer K. Capillary blood perfusion during postischemic reperfusion in striated muscle. Plast Reconstr Surg 89: 1104-1114, 1992.
29. Morita T, Perrella MA, Lee M, and Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA 92: 1475-1479, 1995.
30. Nover L. Heat Shock Response. Boca Raton, FL: CRC, 1991.
31. Odland RM, Poole DV, Rice RD Jr, and Koobs DH. Use of the tunable dye laser to delay McFarlane skin flaps. Arch Otolaryngol Head Neck Surg 121: 1158-1161, 1995.
32. Pang CY, Forrest CR, Neligan PC, and Lindsay WK. Augmentation of blood flow in delayed random skin flaps in the pig: effect of length of delay period and angiogenesis. Plast Reconstr Surg 78: 68-74, 1986.
33. Ramos KS, Lin H, and McGrath JJ. Modulation of cyclic guanosine monophosphate levels in cultured smooth muscle cells by carbon monoxide and nitric oxide. Biochem Pharmacol 38: 1368-1370, 1989.
34. Reinisch JF. The pathophysiology of skin flaps circulation: the delay phenomenon. Plast Reconstr Surg 54: 585-598, 1974.
35. Rücker M, Schäfer T, Roesken F, Spitzer WJ, Bauer M, and 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.
36. Ryter SW and Choi AM. Heme oxygenase-1: molecular mechanisms of gene expression in oxygen-related stress. Antiox Redox Signal 4: 625-632, 2002.
37. Sato K and Hirano M. Fine three-dimensional structure of pericytes in the vocal fold mucosa. Ann Otol Rhinol Laryngol 106: 490-494, 1997.
38. Shibahara S, Mueller RM, and Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 262: 12889-12892, 1987.
39. Shibahara S, Yoshida T, and Kikuchi G. Induction of heme oxygenase by hemin in cultured pig alveolar macrophages. Arch Biochem Biophys 188: 243-250, 1978.
40. Shimada T, Kitamura H, and Nakamura M. Three-dimensional architecture of pericytes with special reference to their topographical relationship to microvascular beds. Arch Histol Cytol 55, Suppl: 77-85, 1992.
41. Skalli O, Pelte MF, Peclet MC, Gabbiani G, Gugliotta P, Bussolati G, Ravazzola M, and Orci L. Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37: 315-321, 1989.
42. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, and Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1045, 1987.
43. Suematsu M, Goda N, Sano T, Kashiwagi S, Egawa T, Shinoda Y, and Ishimura Y. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J Clin Invest 96: 2431-2437, 1995.
44. Suematsu M, Wakabayashi Y, and Ishimura Y. Gaseous monoxides: a new class of microvascular regulator in the liver. Cardiovasc Res 32: 679-686, 1996.
45. Suzuki S, Isshiki N, Ohtsuka M, and Maeda T. Experimental study on "delay" phenomenon in relation to flap width and ischemia. Br J Plast Surg 41: 389-394, 1988.
46. Taylor GI, Corlett RJ, Caddy CM, and Zelt RG. An anatomic review of the delay phenomenon. II. Clinical applications. Plast Reconstr Surg 89: 408-416, 1992.
47. Tenhunen R, Marver HS, and Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61: 748-755, 1968.