63
Views
42
CrossRef citations to date
0
Altmetric
Article

Loss of Epithelial Hypoxia-Inducible Factor Prolyl Hydroxylase 2 Accelerates Skin Wound Healing in Mice

, , , , , , , , , , , & show all
Pages 3426-3438 | Received 17 May 2013, Accepted 17 Jun 2013, Published online: 20 Mar 2023

REFERENCES

  • Shaw TJ, Martin P. 2009. Wound repair at a glance. J. Cell Sci. 122:3209–3213.
  • Lowell CA, Mayadas TN. 2012. Overview: studying integrins in vivo. Methods Mol. Biol. 757:369–397.
  • Gailit J, Welch MP, Clark RA. 1994. TGF-beta 1 stimulates expression of keratinocyte integrins during re-epithelialization of cutaneous wounds. J. Invest. Dermatol. 103:221–227.
  • Reynolds LE, Conti FJ, Lucas M, Grose R, Robinson S, Stone M, Saunders G, Dickson C, Hynes RO, Lacy-Hulbert A, Hodivala-Dilke K. 2005. Accelerated re-epithelialization in beta3-integrin-deficient-mice is associated with enhanced TGF-beta1 signaling. Nat. Med. 11:167–174.
  • Grose R, Hutter C, Bloch W, Thorey I, Watt FM, Fassler R, Brakebusch C, Werner S. 2002. A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129:2303–2315.
  • Larjava H, Salo T, Haapasalmi K, Kramer RH, Heino J. 1993. Expression of integrins and basement membrane components by wound keratinocytes. J. Clin. Invest. 92:1425–1435.
  • Zambruno G, Marchisio PC, Marconi A, Vaschieri C, Melchiori A, Giannetti A, De Luca M. 1995. Transforming growth factor-beta 1 modulates beta 1 and beta 5 integrin receptors and induces the de novo expression of the alpha v beta 6 heterodimer in normal human keratinocytes: implications for wound healing. J. Cell Biol. 129:853–865.
  • Shattil SJ. 1995. Function and regulation of the beta 3 integrins in hemostasis and vascular biology. Thromb. Haemost. 74:149–155.
  • Hynes RO. 2009. The extracellular matrix: not just pretty fibrils. Science 326:1216–1219.
  • Moustakas A, Heldin CH. 2009. The regulation of TGFbeta signal transduction. Development 136:3699–3714.
  • Werner S, Grose R. 2003. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83:835–870.
  • Amendt C, Mann A, Schirmacher P, Blessing M. 2002. Resistance of keratinocytes to TGFbeta-mediated growth restriction and apoptosis induction accelerates re-epithelialization in skin wounds. J. Cell Sci. 115:2189–2198.
  • Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE, Anzano M, Greenwell-Wild T, Wahl SM, Deng C, Roberts AB. 1999. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1:260–266.
  • Lokmic Z, Musyoka J, Hewitson TD, Darby IA. 2012. Hypoxia and hypoxia signaling in tissue repair and fibrosis. Int. Rev. Cell Mol. Biol. 296:139–185.
  • Bedogni B, Welford SM, Cassarino DS, Nickoloff BJ, Giaccia AJ, Powell MB. 2005. The hypoxic microenvironment of the skin contributes to Akt-mediated melanocyte transformation. Cancer Cell 8:443–454.
  • Varghese MC, Balin AK, Carter DM, Caldwell D. 1986. Local environment of chronic wounds under synthetic dressings. Arch. Dermatol. 122:52–57.
  • Ninikoski J, Heughan C, Hunt TK. 1972. Oxygen tensions in human wounds. J. Surg. Res. 12:77–82.
  • Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, Bauer C, Gassmann M, Candinas D. 2001. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J. 15:2445–2453.
  • Rankin EB, Biju MP, Liu Q, Unger TL, Rha J, Johnson RS, Simon MC, Keith B, Haase VH. 2007. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J. Clin. Invest. 117:1068–1077.
  • Wiesener MS, Jurgensen JS, Rosenberger C, Scholze CK, Horstrup JH, Warnecke C, Mandriota S, Bechmann I, Frei UA, Pugh CW, Ratcliffe PJ, Bachmann S, Maxwell PH, Eckardt KU. 2003. Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 17:271–273.
  • Rezvani HR, Ali N, Nissen LJ, Harfouche G, de Verneuil H, Taieb A, Mazurier F. 2011. HIF-1alpha in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non-cancer disorders. J. Invest. Dermatol. 131:1793–1805.
  • Kaelin WGJr, Ratcliffe PJ. 2008. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30:393–402.
  • Maxwell PH, Ratcliffe PJ. 2002. Oxygen sensors and angiogenesis. Semin. Cell Dev. Biol. 13:29–37.
  • Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. 2006. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 26:8336–8346.
  • Botusan IR, Sunkari VG, Savu O, Catrina AI, Grunler J, Lindberg S, Pereira T, Yla-Herttuala S, Poellinger L, Brismar K, Catrina SB. 2008. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc. Natl. Acad. Sci. U. S. A. 105:19426–19431.
  • Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS. 2000. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60:4010–4015.
  • Franke K, Kalucka J, Mamlouk S, Singh RP, Muschter A, Weidemann A, Iyengar V, Jahn S, Wieczorek K, Geiger K, Muders M, Sykes AM, Poitz DM, Ripich T, Otto T, Bergmann S, Breier G, Baretton G, Fong GH, Greaves DR, Bornstein S, Chavakis T, Fandrey J, Gassmann M, Wielockx B. 2013. HIF-1alpha is a protective factor in conditional PHD2-deficient mice suffering from severe HIF-2alpha-induced excessive erythropoiesis. Blood 121:1436–1445.
  • Hattori N, Mochizuki S, Kishi K, Nakajima T, Takaishi H, D'Armiento J, Okada Y. 2009. MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am. J. Pathol. 175:533–546.
  • Hafner M, Wenk J, Nenci A, Pasparakis M, Scharffetter-Kochanek K, Smyth N, Peters T, Kess D, Holtkotter O, Shephard P, Kudlow JE, Smola H, Haase I, Schippers A, Krieg T, Muller W. 2004. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 38:176–181.
  • Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265–277.
  • Licht AH, Raab S, Hofmann U, Breier G. 2004. Endothelium-specific Cre recombinase activity in flk-1-Cre transgenic mice. Dev. Dyn. 229:312–318.
  • Singh RP, Franke K, Kalucka J, Mamlouk S, Muschter A, Gembarska A, Grinenko T, Willam C, Naumann R, Anastassiadis K, Stewart AF, Bornstein S, Chavakis T, Breier G, Waskow C, Wielockx B. 10 May 2013. HIF-prolyl hydroxylase 2 (PHD2) is a critical regulator of hematopoietic stem cell maintenance during steady-state and stress. Blood [Epub ahead of print.] doi:10.1182/blood-2012-12-471185.
  • Boutin AT, Weidemann A, Fu Z, Mesropian L, Gradin K, Jamora C, Wiesener M, Eckardt KU, Koch CJ, Ellies LG, Haddad G, Haase VH, Simon MC, Poellinger L, Powell FL, Johnson RS. 2008. Epidermal sensing of oxygen is essential for systemic hypoxic response. Cell 133:223–234.
  • Rezvani HR, Ali N, Serrano-Sanchez M, Dubus P, Varon C, Ged C, Pain C, Cario-Andre M, Seneschal J, Taieb A, de Verneuil H, Mazurier F. 2011. Loss of epidermal hypoxia-inducible factor-1alpha accelerates epidermal aging and affects re-epithelialization in human and mouse. J. Cell Sci. 124:4172–4183.
  • Keely S, Glover LE, MacManus CF, Campbell EL, Scully MM, Furuta GT, Colgan SP. 2009. Selective induction of integrin beta1 by hypoxia-inducible factor: implications for wound healing. FASEB J. 23:1338–1346.
  • Cowden Dahl KD, Robertson SE, Weaver VM, Simon MC. 2005. Hypoxia-inducible factor regulates alphavbeta3 integrin cell surface expression. Mol. Biol. Cell 16:1901–1912.
  • Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, Klier G, Cheresh DA. 1994. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79:1157–1164.
  • Amendt C, Schirmacher P, Weber H, Blessing M. 1998. Expression of a dominant negative type II TGF-beta receptor in mouse skin results in an increase in carcinoma incidence and an acceleration of carcinoma development. Oncogene 17:25–34.
  • Frank S, Madlener M, Werner S. 1996. Transforming growth factors beta1, beta2, and beta3 and their receptors are differentially regulated during normal and impaired wound healing. J. Biol. Chem. 271:10188–10193.
  • Faler BJ, Macsata RA, Plummer D, Mishra L, Sidawy AN. 2006. Transforming growth factor-beta and wound healing. Perspect. Vasc. Surg. Endovasc. Ther. 18:55–62.
  • Rahimi RA, Leof EB. 2007. TGF-beta signaling: a tale of two responses. J. Cell. Biochem. 102:593–608.
  • Tatti O, Vehvilainen P, Lehti K, Keski-Oja J. 2008. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp. Cell Res. 314:2501–2514.
  • Wang M, Zhao D, Spinetti G, Zhang J, Jiang LQ, Pintus G, Monticone R, Lakatta EG. 2006. Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler. Thromb. Vasc. Biol. 26:1503–1509.
  • Singer AJ, Clark RA. 1999. Cutaneous wound healing. N. Engl. J. Med. 341:738–746.
  • Biswas S, Roy S, Banerjee J, Hussain SR, Khanna S, Meenakshisundaram G, Kuppusamy P, Friedman A, Sen CK. 2010. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc. Natl. Acad. Sci. U. S. A. 107:6976–6981.
  • Elson DA, Ryan HE, Snow JW, Johnson R, Arbeit JM. 2000. Coordinate up-regulation of hypoxia inducible factor (HIF)-1alpha and HIF-1 target genes during multi-stage epidermal carcinogenesis and wound healing. Cancer Res. 60:6189–6195.
  • Elson DA, Thurston G, Huang LE, Ginzinger DG, McDonald DM, Johnson RS, Arbeit JM. 2001. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev. 15:2520–2532.
  • Kong T, Eltzschig HK, Karhausen J, Colgan SP, Shelley CS. 2004. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of beta2 integrin gene expression. Proc. Natl. Acad. Sci. U. S. A. 101:10440–10445.
  • Dvorak HF. 1986. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315:1650–1659.
  • Schäfer M, Werner S. 2008. Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9:628–638.
  • Kremser ME, Przybylo M, Hoja-Lukowicz D, Pochec E, Amoresano A, Carpentieri A, Bubka M, Litynska A. 2008. Characterisation of alpha3beta1 and alpha (v) beta3 integrin N-oligosaccharides in metastatic melanoma WM9 and WM239 cell lines. Biochim. Biophys. Acta 1780:1421–1431.
  • Hudson LG, Gale JM, Padilla RS, Pickett G, Alexander BE, Wang J, Kusewitt DF. 2010. Microarray analysis of cutaneous squamous cell carcinomas reveals enhanced expression of epidermal differentiation complex genes. Mol. Carcinog. 49:619–629.
  • Jeanes AI, Wang P, Moreno-Layseca P, Paul N, Cheung J, Tsang R, Akhtar N, Foster FF, Brennan K, Streuli CH. 2012. Specific beta-containing integrins exert differential control on proliferation and 2D collective cell migration in mammary epithelial cells. J. Biol. Chem. 287:24103–24112.
  • Arwert EN, Hoste E, Watt FM. 2012. Epithelial stem cells, wound healing and cancer. Nat. Rev. Cancer 12:170–180.
  • Diaz-Gonzalez F, Forsyth J, Steiner B, Ginsberg MH. 1996. Trans-dominant inhibition of integrin function. Mol. Biol. Cell 7:1939–1951.
  • Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, Huang X, Sheppard D, Hynes RO, Hodivala-Dilke KM. 2002. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 8:27–34.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.