Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
April-2021 Volume 23 Issue 4

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
April-2021 Volume 23 Issue 4

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)

  • Authors:
    • Yinhua Zheng
    • Zhenlan Li
    • Min Yin
    • Xu Gong
  • View Affiliations / Copyright

    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
    Copyright: © Zheng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 235
    |
    Published online on: January 26, 2021
       https://doi.org/10.3892/mmr.2021.11874
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Heat shock protein 32 (Hsp32), also known as heme oxygenase‑1 (HO‑1), is an enzyme that exists in microsomes. HO‑1 can be induced by a variety of stimuli, including heavy metals, heat shock, inflammatory stimuli, heme and its derivatives, stress, hypoxia, and biological hormones. HO‑1 is the rate‑limiting enzyme of heme catabolism, which splits heme into biliverdin, carbon monoxide (CO) and iron. The metabolites of HO‑1 have anti‑inflammatory and anti‑oxidant effects, and provide protection to the cardiovascular system and transplanted organs. This review summarizes the biological characteristics of HO‑1 and the functional significance of its products, and specifically elaborates on its protective effect on skin flaps. HO‑1 improves the survival rate of ischemic skin flaps through anti‑inflammatory, anti‑oxidant and vasodilatory effects of enzymatic reaction products. In particular, this review focuses on the role of carbon monoxide (CO), one of the primary metabolites of HO‑1, in flap survival and discusses the feasibility and existing challenges of HO‑1 in flap surgery.
View Figures

Figure 1

View References

1 

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

2 

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

3 

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

4 

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

5 

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

6 

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

7 

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

8 

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

9 

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

10 

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

11 

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

12 

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

13 

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

14 

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

15 

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

16 

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

17 

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

18 

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

19 

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

20 

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

21 

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

22 

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

23 

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

24 

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

25 

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

26 

Lindquist S and Craig EA: The heat-shock proteins. Annu Rev Genet. 22:631–677. 1988. View Article : Google Scholar : PubMed/NCBI

27 

Miller DJ and Fort PE: Heat shock proteins regulatory role in neurodevelopment. Front Neurosci. 12:8212018. View Article : Google Scholar : PubMed/NCBI

28 

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

29 

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

30 

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

31 

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

32 

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

33 

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

34 

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

35 

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

36 

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

37 

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

38 

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

39 

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

40 

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

41 

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

42 

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

43 

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

44 

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

45 

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

46 

Sorrenti V: Editorial of special issue ‘protective and detrimental role of heme oxygenase-1’. Int J Mol Sci. 20:47442019. View Article : Google Scholar

47 

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

48 

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

49 

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

50 

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

51 

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

52 

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

53 

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

54 

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

55 

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

56 

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

57 

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

58 

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

59 

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

60 

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

61 

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

62 

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

63 

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

64 

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

65 

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

66 

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

67 

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

68 

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

69 

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

70 

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

71 

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

72 

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

73 

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

74 

Jansen T and Daiber A: Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase? Front Pharmacol. 3:302012.

75 

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

76 

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

77 

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

78 

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

79 

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

80 

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

81 

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

82 

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

83 

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

84 

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

85 

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

86 

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

87 

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

88 

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

89 

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

90 

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

91 

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

92 

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

93 

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

94 

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

95 

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

96 

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

97 

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

98 

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

99 

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

100 

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

101 

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

102 

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

103 

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

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Zheng Y, Li Z, Yin M and Gong X: Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review). Mol Med Rep 23: 235, 2021.
APA
Zheng, Y., Li, Z., Yin, M., & Gong, X. (2021). Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review). Molecular Medicine Reports, 23, 235. https://doi.org/10.3892/mmr.2021.11874
MLA
Zheng, Y., Li, Z., Yin, M., Gong, X."Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)". Molecular Medicine Reports 23.4 (2021): 235.
Chicago
Zheng, Y., Li, Z., Yin, M., Gong, X."Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)". Molecular Medicine Reports 23, no. 4 (2021): 235. https://doi.org/10.3892/mmr.2021.11874
Copy and paste a formatted citation
x
Spandidos Publications style
Zheng Y, Li Z, Yin M and Gong X: Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review). Mol Med Rep 23: 235, 2021.
APA
Zheng, Y., Li, Z., Yin, M., & Gong, X. (2021). Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review). Molecular Medicine Reports, 23, 235. https://doi.org/10.3892/mmr.2021.11874
MLA
Zheng, Y., Li, Z., Yin, M., Gong, X."Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)". Molecular Medicine Reports 23.4 (2021): 235.
Chicago
Zheng, Y., Li, Z., Yin, M., Gong, X."Heme oxygenase‑1 improves the survival of ischemic skin flaps (Review)". Molecular Medicine Reports 23, no. 4 (2021): 235. https://doi.org/10.3892/mmr.2021.11874
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team