Prevention of skin flap necrosis by estradiol involves reperfusion of a protected vascular network

Circulation Research

Volumn 104, Issue 2, 2009, Pages 245-254

  Toutain, Céline E ^a,b   Brouchet, Laurent ^a   Raymond Letron, Isabelle ^d   Vicendo, Patricia ^e   Bergès, Hortense ^a,b   Favre, Julie ^b   Fouque, Marie José ^a,b   Krust, Andrée ^f   Schmitt, Anne Marie ^g   Chambon, Pierre ^f   Gourdy, Pierre ^a,b   Arnal, Jean François ^a,b,c   Lenfant, Françoise ^a,b,h  

^a INSERM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c TOULOUSE UNIVERSITY HOSPITAL   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e Université Paul Sabatier   (France)

^f INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^g Centre d'Immunologie Pierre Fabre   (France)

^h CHU RANGUEIL   (France)

Author keywords

Estradiol; Ischemia; Skin flap model

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FIBROBLAST GROWTH FACTOR 2; PROTEIN BCL 2; TAMOXIFEN; VASCULOTROPIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEEDING; BONE MARROW; CONTROLLED STUDY; DRUG EFFECT; EX VIVO STUDY; EXPERIMENTAL MODEL; EXPLANT; FEMALE; GRAFT NECROSIS; GRAFT SURVIVAL; ISCHEMIA; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION; SKIN DEFECT; SKIN FLAP; SKIN SURGERY; ANIMAL; BLOOD FLOW; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL SURVIVAL; DISEASE MODEL; DOSE RESPONSE; DRUG IMPLANT; GENETICS; HAIRLESS MOUSE; METABOLISM; MOUSE MUTANT; NECROSIS; NUDE MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PLASTIC SURGERY; SKIN; TIME; VASCULARIZATION;

ANIMALS; BONE MARROW TRANSPLANTATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG IMPLANTS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; ISCHEMIA; MICE; MICE, HAIRLESS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; NECROSIS; OVARIECTOMY; REGIONAL BLOOD FLOW; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SKIN; SURGICAL FLAPS; TAMOXIFEN; TIME FACTORS;

EID: 59849111506     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.182410     Document Type: Article

References (45)

1. Fujihara Y, Koyama H, Nishiyama N, Eguchi T, Takato T. Gene transfer of bFGF to recipient bed improves survival of ischemic skin flap. Br J Plast Surg. 2005;58:511-517.
2. Zacchigna S, Papa G, Antonini A, Novati F, Moimas S, Carrer A, Arsic N, Zentilin L, Visintini V, Pascone M, Giacca M. Improved survival of ischemic cutaneous and musculocutaneous flaps after vascular endothe-lial growth factor gene transfer using adeno-associated virus vectors. Am J Pathol. 2005;167:981-991.
3. Liu PY, Liu K, Wang XT, Badiavas E, Rieger-Christ KM, Tang JB, Summerhayes IC. Efficacy of combination gene therapy with multiple growth factor cDNAs to enhance skin flap survival in a rat model. DNA Cell Biol. 2005;24:751-757.
4. Epstein SE, Kornowski R, Fuchs S, Dvorak HF. Angiogenesis therapy: amidst the hype, the neglected potential for serious side effects. Circulation. 2001;104:115-119.
5. Hurn PD, Brass LM. Estrogen and stroke: a balanced analysis. Stroke. 2003;34:338-341.
6. Murphy SJ, McCullough LD, Smith JM. Stroke in the female: role of biological sex and estrogen. ILAR J. 2004;45:147-159.
7. Kyriakides ZS, Kremastinos DT, Karayannakos P. Estrogen stimulates angiogenesis in normoperfused skeletal muscle in rabbits. Circulation. 2001;103:e107-e108.
8. Losordo DW, Isner JM. Estrogen and angiogenesis: a review. Arterioscler Thromb Vasc Biol. 2001;21:6-12.
9. Alvarez RJ, Gips SJ, Moldovan N, Wilhide CC, Milliken EE, Hoang AT, Hruban RH, Silverman HS, Dang CV, Goldschmidt-Clermont PJ. 17beta-estradiol inhibits apoptosis of endothelial cells. Biochem Biophys Res Commun. 1997;237:372-381.
10. Ashcroft GS, Greenwell-Wild T, Horan MA, Wahl SM, Ferguson MW. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol. 1999; 155:1137-1146.
11. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MW. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med. 1997; 3:1209-1215.
12. Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, Burow M, Horan MA, Wahl SM, Nakayama T. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest. 2003;111:1309-1318.
13. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000;127:4277-4291.
14. Mallat Z, Gojova A, Marchiol-Fournigault C, Esposito B, Kamate C, Merval R, Fradelizi D, Tedgui A. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ Res. 2001;89:930-934.
15. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864.
16. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786.
17. Gelis C, Girard S, Mavon A, Delverdier M, Paillous N, Vicendo P. Assessment of the skin photoprotective capacities of an organo-mineral broad-spectrum sunblock on two ex vivo skin models. Photodermatol Photoimmunol Photomed. 2003;19:242-253.
18. Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA, Stenn KS, Paus R. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol. 2001;117:3-15.
19. Crowe MJ, Doetschman T, Greenhalgh DG. Delayed wound healing in immunodeficient TGF-beta 1 knockout mice. J Invest Dermatol. 2000; 115:3-11.
20. Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986;320:134-139.
21. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A. 1996;93:5925-5930.
22. Carpenter KD, Korach KS. Potential biological functions emerging from the different estrogen receptors. Ann N Y Acad Sci. 2006;1092:361-373.
23. Won CK, Kim MO, Koh PO. Estrogen modulates Bcl-2 family proteins in ischemic brain injury. J Vet Med Sci. 2006;68:277-280.
24. Simpkins JW, Wen Y, Perez E, Yang S, Wang X. Role of nonfeminizing estrogens in brain protection from cerebral ischemia: an animal model of Alzheimer's disease neuropathology. Ann N Y Acad Sci. 2005;1052: 233-242.
25. Kim JK, Pedram A, Razandi M, Levin ER. Estrogen prevents cardiomyo-cyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J Biol Chem. 2006;281: 6760-6767.
26. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR. 17-beta-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Cardiol. 2006;40: 205-212.
27. Kanda N, Watanabe S. 17beta-estradiol inhibits oxidative stress-induced apoptosis in keratinocytes by promoting Bcl-2 expression. J Invest Dermatol. 2003;121:1500-1509.
28. Uzuka M, Nakajima K, Ohta S, Mori Y. Induction of hyaluronic acid synthetase by estrogen in the mouse skin. Biochim Biophys Acta. 1981; 673:387-393.
29. Gendimenico GJ, Mack VJ, Siock PA, Mezick JA. Topical estrogens: their effects on connective tissue synthesis in hairless mouse skin. Arch Dermatol Res. 2002;294:231-236.
30. Tammi R, Pasonen-Seppanen S, Kolehmainen E, Tammi M. Hyaluronan synthase induction and hyaluronan accumulation in mouse epidermis following skin injury. J Invest Dermatol. 2005;124:898-905.
31. Chen WY, Abatangelo G. Functions of hyaluronan in wound repair. Wound Repair Regen. 1999;7:79-89.
32. Shi J, Zhang YQ, Simpkins JW. Effects of 17beta-estradiol on glucose transporter 1 expression and endothelial cell survival following focal ischemia in the rats. Exp Brain Res. 1997;117:200-206.
33. Spyridopoulos I, Sullivan AB, Kearney M, Isner JM, Losordo DW. Estrogen-receptor-mediated inhibition of human endothelial cell apopto-sis. Estradiol as a survival factor. Circulation. 1997;95:1505-1514.
34. Bake S, Sohrabji F. 17beta-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology. 2004;145:5471-5475.
35. Hyder SM, Stancel GM, Chiappetta C, Murthy L, Boettger-Tong HL, Makela S. Uterine expression of vascular endothelial growth factor is increased by estradiol and tamoxifen. Cancer Res. 1996;56:3954-3960. (Pubitemid 26284744)
36. Garmy-Susini B, Delmas E, Gourdy P, Zhou M, Bossard C, Bugler B, Bayard F, Krust A, Prats AC, Doetschman T, Prats H, Arnal JF. Role of fibroblast growth factor-2 isoforms in the effect of estradiol on endothelial cell migration and proliferation. Circ Res. 2004;94:1301-1309.
37. van Weel V, Toes RE, Seghers L, Deckers MM, de Vries MR, Eilers PH, Sipkens J, Schepers A, Eefting D, van Hinsbergh VW, van Bockel JH, Quax PH. Natural killer cells and CD4+ T-cells modulate collateral artery development. Arterioscler Thromb Vasc Biol. 2007;27:2310-2318.
38. Iwakura A, Luedemann C, Shastry S, Hanley A, Kearney M, Aikawa R, Isner JM, Asahara T, Losordo DW. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation. 2003;108:3115-3121.
39. Tepper OM, Capla JM, Galiano RD, Ceradini DJ, Callaghan MJ, Kleinman ME, Gurtner GC. Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood. 2005;105:1068-1077.
40. Aicher A, Zeiher AM, Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension. 2005;45:321-325.
41. Shang Y, Brown M. Molecular determinants for the tissue specificity of SERMs. Science. 2002;295:2465-2468.
42. Hardman MJ, Emmerson E, Campbell L, Ashcroft GS. Selective estrogen receptor modulators accelerate cutaneous wound healing in ovariec-tomized female mice. Endocrinology. 2008;149:551-557.
43. Tsang SY, Yao X, Chan HY, Chan FL, Leung CS, Yung LM, Au CL, Chen ZY, Laher I, Huang Y. Tamoxifen and estrogen attenuate enhanced vascular reactivity induced by estrogen deficiency in rat carotid arteries. Biochem Pharmacol. 2007;73:1330-1339.
44. Savolainen-Peltonen H, Luoto NM, Kangas L, Hayry P. Selective estrogen receptor modulators prevent neointima formation after vascular injury. Mol Cell Endocrinol. 2004;227:9-20.
45. Reimer KA, Lowe JE, Rasmussen MM, Jennings RB. The wavefront phenomenon of ischemic cell death. 1. Myocardial infarct size vs duration of coronary occlusion in dogs. Circulation. 1977;56:786-794.