Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)
- Authors:
- Yinhua Zheng
- Zhenlan Li
- Min Yin
- Xu Gong
-
Affiliations: Department of Hand and Foot Surgery, The First Hospital of Jilin University, Changchun, Jilin 130021, P.R. China, Department of Rehabilitation Medicine, The First Hospital of Jilin University, Changchun, Jilin 130021, P.R. China, Department of Nephrology, China‑Japan Union Hospital of Jilin University, Changchun, Jilin 130033, P.R. China - Published online on: January 26, 2021 https://doi.org/10.3892/mmr.2021.11874
- Article Number: 235
-
Copyright: © Zheng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
 |
|
Taylor GI, Corlett RJ, Dhar SC and Ashton MW: The anatomical (angiosome) and clinical territories of cutaneous perforating arteries: Development of the concept and designing safe flaps. Plast Reconstr Surg. 127:1447–1459. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Saint-Cyr M, Wong C, Schaverien M, Mojallal A and Rohrich RJ: The perforasome theory: Vascular anatomy and clinical implications. Plast Reconstr Surg. 124:1529–1544. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Callegari PR, Taylor GI, Caddy CM and Minabe T: An anatomic review of the delay phenomenon: I. Experimental studies. Plast Reconstr Surg. 89:397–407; discussion 417-398. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Sanati-Mehrizy P, Massenburg BB, Rozehnal JM, Ingargiola MJ, Hernandez Rosa J and Taub PJ: Risk factors leading to free flap failure: Analysis from the national surgical quality improvement program database. J Craniofac Surg. 27:1956–1964. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Bekara F, Herlin C, Mojallal A, Sinna R, Ayestaray B, Letois F, Chavoin JP, Garrido I, Grolleau JL and Chaput B: A systematic review and meta-analysis of perforator-pedicled propeller flaps in lower extremity defects: Identification of risk factors for complications. Plast Reconstr Surg. 137:314–331. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Wong AK, Joanna Nguyen T, Peric M, Shahabi A, Vidar EN, Hwang BH, Niknam Leilabadi S, Chan LS and Urata MM: Analysis of risk factors associated with microvascular free flap failure using a multi-institutional database. Microsurgery. 35:6–12. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
de Blacam C, Colakoglu S, Ogunleye AA, Nguyen JT, Ibrahim AM, Lin SJ, Kim PS and Lee BT: Risk factors associated with complications in lower-extremity reconstruction with the distally based sural flap: A systematic review and pooled analysis. J Plast Reconstr Aesthet Surg. 67:607–616. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Las DE, de Jong T, Zuidam JM, Verweij NM, Hovius SE and Mureau MA: Identification of independent risk factors for flap failure: A retrospective analysis of 1530 free flaps for breast, head and neck and extremity reconstruction. J Plast Reconstr Aesthet Surg. 69:894–906. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li B, Chang SM, Du SC, Zhuang L and Hu SJ: Distally based sural adipofascial turnover flap for coverage of complicated wound in the foot and ankle region. Ann Plast Surg. 84:580–587. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Lee ZH, Abdou SA, Ramly EP, Daar DA, Stranix JT, Anzai L, Saadeh PB, Levine JP and Thanik VD: Larger free flap size is associated with increased complications in lower extremity trauma reconstruction. Microsurgery. 40:473–478. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Stranix JT, Lee ZH, Anzai L, Jacoby A, Avraham T, Saadeh PB, Levine JP and Thanik VD: Optimizing venous outflow in reconstruction of Gustilo IIIB lower extremity traumas with soft tissue free flap coverage: Are two veins better than one? Microsurgery. 38:745–751. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Gupta A, Lakhiani C, Lim BH, Aho JM, Goodwin A, Tregaskiss A, Lee M, Scheker L and Saint-Cyr M: Free tissue transfer to the traumatized upper extremity: Risk factors for postoperative complications in 282 cases. J Plast Reconstr Aesthet Surg. 68:1184–1190. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Reece EM, Bonelli MA, Livingston T, Mulligan PS, Rockwood J, Wilson JR, Zoldos J and Champagne L: Factors in free fasciocutaneous flap complications: A logistic regression analysis. Plast Reconstr Surg. 136:54e–58e. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Innocenti M, Menichini G, Baldrighi C, Delcroix L, Vignini L and Tos P: Are there risk factors for complications of perforator-based propeller flaps for lower-extremity reconstruction? Clin Orthop Relat Res. 472:2276–2286. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Dolan RT, Butler JS, Murphy SM and Cronin KJ: Health-related quality of life, surgical and aesthetic outcomes following microvascular free flap reconstructions: An 8-year institutional review. Ann R Coll Surg Engl. 94:43–51. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ellabban MA, Fattah IOA, Kader GA, Eldeen OS, Mehana AE, Khodeer DM, Hosny H, Elbasiouny MS and Masadeh S: The effects of sildenafil and/or nitroglycerin on random-pattern skin flaps after nicotine application in rats. Sci Rep. 10:32122020. View Article : Google Scholar : PubMed/NCBI | |
|
Lee W, Oh W, Oh SM and Yang EJ: Comparative effectiveness of different interventions of perivascular hyaluronidase. Plast Reconstr Surg. 145:957–964. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Giatsidis G, Cheng L, Haddad A, Ji K, Succar J, Lancerotto L, Lujan-Hernandez J, Fiorina P, Matsumine H and Orgill DP: Noninvasive induction of angiogenesis in tissues by external suction: Sequential optimization for use in reconstructive surgery. Angiogenesis. 21:61–78. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Giatsidis G, Cheng L, Facchin F, Haddad A, Lujan-Hernandez J, Lancerotto L, Nabzdyk CG, Matsumine H and Orgill DP: Moderate-intensity intermittent external volume expansion optimizes the soft-tissue response in a murine model. Plast Reconstr Surg. 139:882–890. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Doğan F and Özyazgan İ: Flap preconditioning by electrical stimulation as an alternative to surgical delay: Experimental study. Ann Plast Surg. 75:560–564. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Menevşe GT, TeomanTellioglu A, Altuntas N, Cömert A and Tekdemir I: Polidocanol injection for chemical delay and its effect on the survival of rat dorsal skin flaps. J Plast Reconstr Aesthet Surg. 67:851–856. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Tobalem M, Wettstein R, Pittet-Cuénod B, Vigato E, Machens HG, Lohmeyer JA, Rezaeian F and Harder Y: Local shockwave-induced capillary recruitment improves survival of musculocutaneous flaps. J Surg Res. 184:1196–1204. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kubulus D, Amon M, Roesken F, Rücker M, Bauer I and Menger MD: Experimental cooling-induced preconditioning attenuates skin flap failure. Br J Surg. 92:1432–1438. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Morris SF and Taylor GI: The time sequence of the delay phenomenon: When is a surgical delay effective? An experimental study. Plast Reconstr Surg. 95:526–533. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Akimoto M, Takeda A, Matsushita O, Inoue J, Sakamoto K, Hattori M, Kounoike N and Uchinuma E: Effects of CB-VEGF-A injection in rat flap models for improved survival. Plast Reconstr Surg. 131:717–725. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Lindquist S and Craig EA: The heat-shock proteins. Annu Rev Genet. 22:631–677. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Miller DJ and Fort PE: Heat shock proteins regulatory role in neurodevelopment. Front Neurosci. 12:8212018. View Article : Google Scholar : PubMed/NCBI | |
|
Lin D, Wu H, Zhou Z, Tao Z, Jia T and Gao W: Ginkgolide B improves multiterritory perforator flap survival by inhibiting endoplasmic reticulum stress and oxidative stress. J Invest Surg. 1–7. Dec 23–2019.(Epub ahead of print). View Article : Google Scholar | |
|
Kumar D, Jena GR, Ram M, Lingaraju MC, Singh V, Prasad R, Kumawat S, Kant V, Gupta P, Tandan SK and Kumar D: Hemin attenuated oxidative stress and inflammation to improve wound healing in diabetic rats. Naunyn Schmiedebergs Arch Pharmacol. 392:1435–1445. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Kankam HKN, Mehta S and Jain A: Thermal preconditioning for surgery: A systematic review. J Plast Reconstr Aesthet Surg. 73:1645–1664. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Park C, Lee H, Noh JS, Jin CY, Kim GY, Hyun JW, Leem SH and Choi YH: Hemistepsin A protects human keratinocytes against hydrogen peroxide-induced oxidative stress through activation of the Nrf2/HO-1 signaling pathway. Arch Biochem Biophys. 691:1085122020. View Article : Google Scholar : PubMed/NCBI | |
|
Jackson JW, Rivera-Marquez GM, Beebe K, Tran AD, Trepel JB, Gestwicki JE, Blagg BSJ, Ohkubo S and Neckers LM: Pharmacologic dissection of the overlapping impact of heat shock protein family members on platelet function. J Thromb Haemost. 18:1197–1209. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Matsunobu T, Satoh Y, Ogawa K and Shiotani A: Heme oxygenase-1 expression in the guinea pig cochlea induced by intense noise stimulation. Acta Otolaryngol Suppl. 18–23. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Harder Y, Amon M, Schramm R, Georgi M, Banic A, Erni D and Menger MD: Heat shock preconditioning reduces ischemic tissue necrosis by heat shock protein (HSP)-32-mediated improvement of the microcirculation rather than induction of ischemic tolerance. Ann Surg. 242:869–878; discussion 878-869. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Tian W, Bonkovsky HL, Shibahara S and Cohen DM: Urea and hypertonicity increase expression of heme oxygenase-1 in murine renal medullary cells. Am J Physiol Renal Physiol. 281:F983–F991. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
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. View Article : Google Scholar : PubMed/NCBI | |
|
Chang YC, Lai CC, Lin LF, Ni WF and Tsai CH: The up-regulation of heme oxygenase-1 expression in human gingival fibroblasts stimulated with nicotine. J Periodontal Res. 40:252–257. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Contaldo C, Harder Y, Plock J, Banic A, Jakob SM and Erni D: The influence of local and systemic preconditioning on oxygenation, metabolism and survival in critically ischaemic skin flaps in pigs. J Plast Reconstr Aesthet Surg. 60:1182–1192. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Schürmann C, Seitz O, Klein C, Sader R, Pfeilschifter J, Mühl H, Goren I and Frank S: Tight spatial and temporal control in dynamic basal to distal migration of epithelial inflammatory responses and infiltration of cytoprotective macrophages determine healing skin flap transplants in mice. Ann Surg. 249:519–534. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Chen YH, Lin SJ, Lin MW, Tsai HL, Kuo SS, Chen JW, Charng MJ, Wu TC, Chen LC, Ding YA, et al: Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet. 111:1–8. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Schillinger M, Exner M, Mlekusch W, Ahmadi R, Rumpold H, Mannhalter C, Wagner O and Minar E: Heme oxygenase-1 genotype is a vascular anti-inflammatory factor following balloon angioplasty. J Endovasc Ther. 9:385–394. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Whitington PF, Moscioni AD and Gartner LM: The effect of tin (IV)-protoporphyrin-IX on bilirubin production and excretion in the rat. Pediatr Res. 21:487–491. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Vreman HJ, Ekstrand BC and Stevenson DK: Selection of metalloporphyrin heme oxygenase inhibitors based on potency and photoreactivity. Pediatr Res. 33:195–200. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Elbirt KK and Bonkovsky HL: Heme oxygenase: Recent advances in understanding its regulation and role. Proc Assoc Am Physicians. 111:438–447. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Adach W, Błaszczyk M and Olas B: Carbon monoxide and its donors-chemical and biological properties. Chem Biol Interact. 318:1089732020. View Article : Google Scholar : PubMed/NCBI | |
|
Sorrenti V: Editorial of special issue ‘protective and detrimental role of heme oxygenase-1’. Int J Mol Sci. 20:47442019. View Article : Google Scholar | |
|
Sha JY, Zhou YD, Yang JY, Leng J, Li JH, Hu JN, Liu W, Jiang S, Wang YP, Chen C and Li W: Maltol (3-Hydroxy-2-methyl-4-pyrone) slows d-galactose-induced brain aging process by damping the Nrf2/HO-1-mediated oxidative stress in mice. J Agric Food Chem. 67:10342–10351. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Schallner N, Romão CC, Biermann J, Lagrèze WA, Otterbein LE, Buerkle H, Loop T and Goebel U: Carbon monoxide abrogates ischemic insult to neuronal cells via the soluble guanylate cyclase-cGMP pathway. PLoS One. 8:e606722013. View Article : Google Scholar : PubMed/NCBI | |
|
Ndisang JF, Wu L, Zhao W and Wang R: Induction of heme oxygenase-1 and stimulation of cGMP production by hemin in aortic tissues from hypertensive rats. Blood. 101:3893–3900. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Motterlini R and Otterbein LE: The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 9:728–743. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton JW and Vercellotti GM: Ferritin: A cytoprotective antioxidant strategem of endothelium. J Biol Chem. 267:18148–18153. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Vinchi F, De Franceschi L, Ghigo A, Townes T, Cimino J, Silengo L, Hirsch E, Altruda F and Tolosano E: Hemopexin therapy improves cardiovascular function by preventing heme-induced endothelial toxicity in mouse models of hemolytic diseases. Circulation. 127:1317–1329. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Fang R and Aust AE: Induction of ferritin synthesis in human lung epithelial cells treated with crocidolite asbestos. Arch Biochem Biophys. 340:369–375. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, Chora A, Rodrigues CD, Gregoire IP, Cunha-Rodrigues M, et al: Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med. 13:703–710. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Freitas A, Alves-Filho JC, Secco DD, Neto AF, Ferreira SH, Barja-Fidalgo C and Cunha FQ: Heme oxygenase/carbon monoxide-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol. 149:345–354. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Cepinskas G, Katada K, Bihari A and Potter RF: Carbon monoxide liberated from carbon monoxide-releasing molecule CORM-2 attenuates inflammation in the liver of septic mice. Am J Physiol Gastrointest Liver Physiol. 294:G184–G191. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Mizuguchi S, Stephen J, Bihari R, Markovic N, Suehiro S, Capretta A, Potter RF and Cepinskas G: CORM-3-derived CO modulates polymorphonuclear leukocyte migration across the vascular endothelium by reducing levels of cell surface-bound elastase. Am J Physiol Heart Circ Physiol. 297:H920–H929. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Tsoyi K, Lee TY, Lee YS, Kim HJ, Seo HG, Lee JH and Chang KC: Heme-oxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high-mobility group box 1 release in vitro and improve survival of mice in LPS- and cecal ligation and puncture-induced sepsis model in vivo. Mol Pharmacol. 76:173–182. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Lancel S, Hassoun SM, Favory R, Decoster B, Motterlini R and Neviere R: Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J Pharmacol Exp Ther. 329:641–648. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Chung SW, Liu X, Macias AA, Baron RM and Perrella MA: Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest. 118:239–247. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Desmard M, Davidge KS, Bouvet O, Morin D, Roux D, Foresti R, Ricard JD, Denamur E, Poole RK, Montravers P, et al: A carbon monoxide-releasing molecule (CORM-3) exerts bactericidal activity against pseudomonas aeruginosa and improves survival in an animal model of bacteraemia. FASEB J. 23:1023–1031. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, Loop T, Otterbein SL, Otterbein LE and Choi AM: Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem. 278:36993–36998. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA and Choi AM: Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 6:422–428. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Chen B, Guo L, Fan C, Bolisetty S, Joseph R, Wright MM, Agarwal A and George JF: Carbon monoxide rescues heme oxygenase-1-deficient mice from arterial thrombosis in allogeneic aortic transplantation. Am J Pathol. 175:422–429. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
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.PubMed/NCBI | |
|
Wang R: Resurgence of carbon monoxide: An endogenous gaseous vasorelaxing factor. Can J Physiol Pharmacol. 76:1–15. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Varadi J, Lekli I, Juhasz B, Bacskay I, Szabo G, Gesztelyi R, Szendrei L, Varga E, Bak I, Foresti R, et al: Beneficial effects of carbon monoxide-releasing molecules on post-ischemic myocardial recovery. Life Sci. 80:1619–1626. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Guo Y, Stein AB, Wu WJ, Tan W, Zhu X, Li QH, Dawn B, Motterlini R and Bolli R: Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am J Physiol Heart Circ Physiol. 286:H1649–H1653. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Józkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R and Dulak J: Heme oxygenase and angiogenic activity of endothelial cells: Stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal. 5:155–162. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Soares MP, Usheva A, Brouard S, Berberat PO, Gunther L, Tobiasch E and Bach FH: Modulation of endothelial cell apoptosis by heme oxygenase-1-derived carbon monoxide. Antioxid Redox Signal. 4:321–329. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Clark JE, Naughton P, Shurey S, Green CJ, Johnson TR, Mann BE, Foresti R and Motterlini R: Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res. 93:e2–e8. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Sato K, Balla J, Otterbein L, Smith RN, Brouard S, Lin Y, Csizmadia E, Sevigny J, Robson SC, Vercellotti G, et al: Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J Immunol. 166:4185–4194. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Sandouka A, Fuller BJ, Mann BE, Green CJ, Foresti R and Motterlini R: Treatment with CO-RMs during cold storage improves renal function at reperfusion. Kidney Int. 69:239–247. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Jansen T and Daiber A: Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase? Front Pharmacol. 3:302012. | |
|
Maines MD, Miralem T, Lerner-Marmarosh N, Shen J and Gibbs PE: Human biliverdin reductase, a previously unknown activator of protein kinase C betaII. J Biol Chem. 282:8110–8122. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Gibbs PE, Tudor C and Maines MD: Biliverdin reductase: More than a namesake-the reductase, its peptide fragments, and biliverdin regulate activity of the three classes of protein kinase C. Front Pharmacol. 3:312012. View Article : Google Scholar : PubMed/NCBI | |
|
Lerner-Marmarosh N, Shen J, Torno MD, Kravets A, Hu Z and Maines MD: Human biliverdin reductase: A member of the insulin receptor substrate family with serine/threonine/tyrosine kinase activity. Proc Natl Acad Sci USA. 102:7109–7114. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Jansen T, Hortmann M, Oelze M, Opitz B, Steven S, Schell R, Knorr M, Karbach S, Schuhmacher S, Wenzel P, et al: Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1-evidence for direct and indirect antioxidant actions of bilirubin. J Mol Cell Cardiol. 49:186–195. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Pae HO, Son Y, Kim NH, Jeong HJ, Chang KC and Chung HT: Role of heme oxygenase in preserving vascular bioactive NO. Nitric Oxide. 23:251–257. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Eppihimer MJ and Granger DN: Ischemia/reperfusion-induced leukocyte-endothelial interactions in postcapillary venules. Shock. 8:16–25. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Kunkel EJ, Jung U, Bullard DC, Norman KE, Wolitzky BA, Vestweber D, Beaudet AL and Ley K: Absence of trauma-induced leukocyte rolling in mice deficient in both P-selectin and intercellular adhesion molecule 1. J Exp Med. 183:57–65. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Menger MD and Vollmar B: Adhesion molecules as determinants of disease: From molecular biology to surgical research. Br J Surg. 83:588–601. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Menger MD, Pelikan S, Steiner D and Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: Significance of ‘reflow paradox’. Am J Physiol. 263:H1901–H1906. 1992.PubMed/NCBI | |
|
Rücker M, Schäfer T, Roesken F, Spitzer WJ, Bauer M and Menger MD: Reduction of inflammatory response in composite flap transfer by local stress conditioning-induced heat-shock protein 32. Surgery. 129:292–301. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Taleb S, Moghaddas P, Rahimi Balaei M, Taleb S, Rahimpour S, Abbasi A, Ejtemaei-Mehr S and Dehpour AR: Metformin improves skin flap survival through nitric oxide system. J Surg Res. 192:686–691. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Han HH, Lim YM, Park SW, Lee SJ, Rhie JW and Lee JH: Improved skin flap survival in venous ischemia-reperfusion injury with the use of adipose-derived stem cells. Microsurgery. 35:645–652. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Forrester SJ, Kikuchi DS, Hernandes MS, Xu Q and Griendling KK: Reactive oxygen species in metabolic and inflammatory signaling. Circ Res. 122:877–902. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Lin CC, Hsiao LD, Cho RL and Yang CM: Carbon monoxide releasing molecule-2-upregulated ROS-dependent heme oxygenase-1 axis suppresses lipopolysaccharide-induced airway inflammation. Int J Mol Sci. 20:31572019. View Article : Google Scholar | |
|
Shi Y, Liang XC, Zhang H, Sun Q, Wu QL and Qu L: Combination of quercetin, cinnamaldehyde and hirudin protects rat dorsal root ganglion neurons against high glucose-induced injury through Nrf-2/HO-1 activation and NF-κB inhibition. Chin J Integr Med. 23:663–671. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM and Soares MP: Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med. 192:1015–1026. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Edmunds MC, Czopek A, Wigmore SJ and Kluth DC: Paradoxical effects of heme arginate on survival of myocutaneous flaps. Am J Physiol Regul Integr Comp Physiol. 306:R10–R22. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Harder Y, Amon M, Schramm R, Rücker M, Scheuer C, Pittet B, Erni D and Menger MD: Ischemia-induced up-regulation of heme oxygenase-1 protects from apoptotic cell death and tissue necrosis. J Surg Res. 150:293–303. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Harder Y, Contaldo C, Klenk J, Banic A, Jakob SM and Erni D: Improved skin flap survival after local heat preconditioning in pigs. J Surg Res. 119:100–105. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Harder Y, Amon M, Georgi M, Scheuer C, Schramm R, Rücker M, Pittet B, Erni D and Menger MD: Aging is associated with an increased susceptibility to ischaemic necrosis due to microvascular perfusion failure but not a reduction in ischaemic tolerance. Clin Sci (Lond). 112:429–440. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kubulus D, Roesken F, Amon M, Rücker M, Bauer M, Bauer I and 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. View Article : Google Scholar : PubMed/NCBI | |
|
Sun Y, Li QF, Zhang Y, Hu R and Jiang H: Isoflurane preconditioning increases survival of rat skin random-pattern flaps by induction of HIF-1α expression. Cell Physiol Biochem. 31:579–591. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Chiang SK, Chen SE and Chang LC: A dual role of heme oxygenase-1 in cancer cells. Int J Mol Sci. 20:392018. View Article : Google Scholar | |
|
Nitti M, Piras S, Brondolo L, Marinari UM, Pronzato MA and Furfaro AL: Heme oxygenase 1 in the nervous system: Does it favor neuronal cell survival or induce neurodegeneration? Int J Mol Sci. 19:22602018. View Article : Google Scholar | |
|
Hopper CP, Meinel L, Steiger C and Otterbein LE: Where is the clinical breakthrough of heme oxygenase-1/carbon monoxide therapeutics? Curr Pharm Des. 24:2264–2282. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Steiger C, Hermann C and Meinel L: Localized delivery of carbon monoxide. Eur J Pharm Biopharm. 118:3–12. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bereczki D Jr, Balla J and Bereczki D: Heme oxygenase-1: Clinical relevance in ischemic stroke. Curr Pharm Des. 24:2229–2235. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Szabo IL, Kenyeres A, Szegedi A and Szollosi AG: Heme oxygenase and the skin in health and disease. Curr Pharm Des. 24:2303–2310. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Haines DD and Tosaki A: Role of heme oxygenases in cardiovascular syndromes and co-morbidities. Curr Pharm Des. 24:2322–2325. 2018. View Article : Google Scholar : PubMed/NCBI |
