Mechanisms of radiation-induced skin injury and implications for future clinical trials

References

• Ahmed EA, Agay D, Schrock G, Drouet M, Meineke V, Scherthan H. 2012. Persistent DNA damage after high-dose in vivo gamma exposure of minipig skin. PLoS ONE 7:e39521.
   PubMed Web of Science ®Google Scholar
• Anscher MS, Marks LB, Shafman TD, Clough R, Huang H, Tisch A, Munley M, Herndon JE, Garst J, Crawford J, Jirtle RL. 2000. Risk of long term complications after TGF-β1-guided very high dose thoracic radiotherapy. International Journal of Radiation Oncology • Biology • Physics 56:988–995.
   Google Scholar
• Archambeau JO, Hauser D, Shymko RM. 1988. Swine basal cell proliferation during a course of daily irradiation five days a week for six weeks. International Journal of Radiation Oncology • Biology • Physics 15:1383–1388.
   Google Scholar
• Archambeau JO, Ines A, Fajardo LF. 1984. Response of swine skin microvasculature to acute single exposure of x-rays: Quantification of endothelial changes. Radiation Research 98:37–51.
   PubMed Web of Science ®Google Scholar
• Avraham T, Yan A, Zampell JC, Daluvoy SV, Haimovitz-Friedman A, Cordeiro AP, Mehrara BJ. 2010. Radiation therapy causes loss of dermal lymphatic vessels and interferes with lymphatic function by TGF-beta1-mediated tissue fibrosis. American Journal of Physiology Cell Physiology 299:C589–605.
   PubMed Web of Science ®Google Scholar
• Barbanova AV. 2002. Acute radiation syndrome with cutaneous syndrome. In: Ricks RC, Berger ME, O’Hara FM, editors. The medical basis for radiation accident preparedness: The clinical care of victims. NY: Parthenon. pp 217–224.
   Google Scholar
• Bastianutto C, Mian A, Symes J, Mocanu J, Alajez N, Sleep G, Shi W, Keating A, Crump M, Gospodarowicz M, Medin J, Minden M, Liu FF. 2007. Local radiotherapy induces homing of hematopoietic stem cells to the irradiated bone marrow. Cancer Research 67:10112–10106.
   Google Scholar
• Brindel I, Legrand M. 2011 Trial of combined Pentoxifylline- tocopherol-clodronate versus placebo in radiation-induced brachial plexopathy (PENTOCLO). [Cited 29 August 2012]. Available from: http://clinicaltrials.gov/ct2/show/NCT01291433.
   Google Scholar
• Brown SL, Kolozsvary A, Jenrow KA, Lapanowski K, Kim JH. 2012. TNF alpha receptor antagonist mitigates radiation induced acute and sub-acute skin injury in mice. Presented at the 58th Annual Meeting of Radiation Research Society, San Juan, Puerto Rico; 30 September to 3 October, 2012.
   Google Scholar
• Burrell K, Hill RP, Zadeh G. 2012. High-resolution in-vivo analysis of normal brain response to cranial irradiation. PLoS ONE 7:e38366.
   PubMed Web of Science ®Google Scholar
• Burroughs L, Mielcarek M, Little MT, Bridger G, Macfarland R, Fricker S, Labrecque J, Sandmaier BM, Storb R. 2005. Durable engraftment of AMD3100-mobilized autologous and allogeneic peripheral-blood mononuclear cells in a canine transplantation model. Blood 106:4002–4008.
   PubMed Web of Science ®Google Scholar
• Campana F, Zervoudis S, Perdereau B, Gez E, Fourquet A, Badiu C, Tsakiris G, Koulaloglou S. 2004. Topical superoxide dismutase reduces post-irradiation breast cancer fibrosis. Journal of Cellular and Molecular Medicine 8:109–116.
   PubMed Web of Science ®Google Scholar
• Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nature Medicine 10:858–864.
   PubMed Web of Science ®Google Scholar
• Chung YL, Wang AJ, Yao LF. 2004. Antitumor histone deacetylase inhibitors suppress cutaneous radiation syndrome: Implications for increasing therapeutic gain in cancer radiotherapy. Molecular Cancer Therapeutics 3:317–325.
   PubMed Web of Science ®Google Scholar
• Colvin GA, Dooner MS, Dooner GJ, Sanchez-Guijo FM, Demers DA, Abedi M, Ramanathan M, Chung S, Pascual S, Quesenberry PJ. 2007. Stem cell continuum: Directed differentiation hotspots. Experimental Hematology 35:96–107.
   Google Scholar
• De Clerq E. 2003. The bicyclam AMD3100 story. Nature Reviews Drug Discovery 2:581–587.
   PubMed Web of Science ®Google Scholar
• Delanian S, Baillet F, Huart J, Lefaix JL, Maulard C, Housset M. 1994. Successful treatment of radiation-induced fibrosis using liposomal Cu/Zn superoxide dismutase: Clinical trial. Radiotherapy & Oncology 32:12–20.
   PubMed Web of Science ®Google Scholar
• Delanian S, Lefaix JL. 2007. Current management for late normal tissue injury: Radiation-induced fibrosis and necrosis. Seminars in Radiation Oncology 17:99–107.
   PubMed Web of Science ®Google Scholar
• Delanian S, Porcher R, Balla-Mekias S, Lefaix JL. 2003. Randomized placebo-controlled trial of combined pentoxifylline and tocopherol for regression of superficial radiation-induced fibrosis. Journal of Clinical Oncology 21:2545–2550.
   PubMed Web of Science ®Google Scholar
• Donahue RE, Jin P, Bonifacino AC, Metzger ME, Ren J, Wang E, Stroncek DF. 2009. Plerixafor (AMD3100) and granulocyte colony-stimulating factor (G-CSF) mobilize different CD34 + cell populations based on global gene and microRNA expression signatures. Blood 114:2530–2541.
   PubMed Web of Science ®Google Scholar
• Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegué E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G. 2008. HIF-1 alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13:206–220.
   PubMed Web of Science ®Google Scholar
• Ehrhart EJ, Segarini P, Tsang ML, Carroll AG, Barcellos-Hoff MH. 1997. Latent transforming growth factor beta1 activation in situ: Quantitative and functional evidence after low-dose gamma-irradiation. FASEB Journal. 11:991–1002.
   PubMed Web of Science ®Google Scholar
• Flanders KC. 2004. Smad3 as a mediator of the fibrotic response. International Journal of Experimental Pathology 85:47–64.
   PubMed Web of Science ®Google Scholar
• Flanders KC, Sullivan CD, Fujii M, Sowers A, Anzano MA, Arabshahi A, Major C, Deng C, Russo A, Mitchell JB, Roberts AB. 2002. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. American Journal of Pathology 160:1057–1068.
   PubMed Web of Science ®Google Scholar
• Flechsig P, Dadrich M, Bickelhaupt S, Jenne J, Hauser K, Timke C, Peschke P, Hahn EW, Gröne HJ, Yingling J, Lahn M, Wirkner U, Huber PE. 2012. LY2109761 attenuates radiation-induced pulmonary murine fibrosis via reversal of TGF-beta and BMP-associated proinflammatory and proangiogenic signals. Clinical Cancer Research 18:3616–3627.
   PubMed Web of Science ®Google Scholar
• François S, Mouiseddine M, Mathieu N, Semont A, Monti P, Dudoignon N, Saché A, Boutarfa A, Thierry D, Gourmelon P, Chapel A. 2007. Human mesenchymal stem cells favour healing of the cutaneous radiation syndrome in a xenogenic transplant model. Annals of Hematology 86:1–8.
   PubMed Web of Science ®Google Scholar
• Fruehauf S, Veldwijk MR, Seeger T, Schubert M, Laufs S, Topaly J, Wuchter P, Dillmann F, Eckstein V, Wenz F, Goldschmidt H, Ho AD, Calandra G. 2009. A combination of granulocyte-colony-stimulating factor (G-CSF) and plerixafor mobilizes more primitive peripheral blood progenitor cells than G-CSF alone: Results of a European phase II study. Chemotherapy 11:992–1001.
   Google Scholar
• Gothard L, Cornes P, Earl J, Hall E, MacLaren J, Mortimer P, Peacock J, Peckitt C, Woods M, Yarnold J. 2004. Double-blind placebo-controlled randomised trial of vitamin E and pentoxifylline in patients with chronic arm lymphoedema and fibrosis after surgery and radiotherapy for breast cancer. Radiotherapy & Oncology 73:133–139.
   PubMed Web of Science ®Google Scholar
• Heissig B, Rafii S, Akiyama H, Ohki Y, Sato Y, Rafael T, Zhu Z, Hicklin DJ, Okumura K, Ogawa H, Werb Z, Hattori K. 2005. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. The Journal of Experimental Medicine 202:739–750.
   PubMed Web of Science ®Google Scholar
• Hill RP, Rodemann HP, Hendry JH. 2001. Normal tissue radiobiology: from the laboratory to the clinic. International Journal of Radiation Oncology • Biology • Physics 49:353–365.
   PubMed Web of Science ®Google Scholar
• Hopewell JW. 1990. The skin: Its structure and response to ionizing radiation. International Journal of Radiation Biology 57:751–773.
   PubMed Web of Science ®Google Scholar
• Jaal J, Richter C, Dörr W. 2010. Effect of recombinant human keratinocyte growth factor (rHuKGF, Palifermin) on inflammatory and immune changes in mouse tongue during fractionated irradiation. International Journal of Radiation Biology 86:860–866.
   PubMed Web of Science ®Google Scholar
• Janko M, Ontiveros F, Fitzgerald TJ, Deng A, DeCicco M, Rock KL. 2012. IL-1 generated subsequent to radiation-induced tissue injury contributes to the pathogenesis of radiodermatitis. Radiation Research 178:166–172.
   PubMed Web of Science ®Google Scholar
• Kim JH, Kolozsvary A, Jenrow KA, Brown SL. 2012. Plerixafor, a CXCR4 antagonist, mitigates skin radiation-induced injury in mice. Radiation Research 178:202–206.
   PubMed Web of Science ®Google Scholar
• Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. 2010. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. Journal of Clinical Investigation 120:694–705.
   PubMed Web of Science ®Google Scholar
• Kohl RR, Kolozsvary A, Brown SL, Zhu G, Kim JH. 2007. Differential radiation effect in tumor and normal tissue after treatment with ramipril, an angiotensin-converting enzyme inhibitor. Radiation Research 168:440–445.
   PubMed Web of Science ®Google Scholar
• Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, Duda DG. 2010. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Research 70:5679–5685.
   PubMed Web of Science ®Google Scholar
• Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K. 2008. Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. Haematologica 93:1457–1465.
   PubMed Web of Science ®Google Scholar
• Lataillade JJ, Doucet C, Bey E, Carsin H, Huet C, Clairand I, Bottollier-Depios JF, Chapel A, Ernou I, Gourven M, Boutin L, Hayden A, Carcamo C, Buglove E, Joussemet M, de Ravel T, Gourmelon P. 2007. New approach to radiation burn treatment by dosemitry-guided surgery combined with autologous mesenchymal stem cell therapy. Regenerative Medicine 2:785–794.
   PubMed Web of Science ®Google Scholar
• Lee JW, Tutela JP, Zoumalan RA, Thanik VD, Nguyen PD, Varjabedian L, Warren SM, Saadeh PB. 2010a. Inhibition of Smad3 expression in radiation-induced fibrosis using a novel method for topical transcutaneous gene therapy. Archives of Otolaryngology – Head & Neck Surgery 136:714–719.
   PubMedGoogle Scholar
• Lee JW, Zoumalan RA, Valenzuela CD, Nguyen PD, Tutela JP, Roman BR, Warren SM, Saadeh PB. 2010b. Regulators and mediators of radiation-induced fibrosis: Gene expression profiles and a rationale for Smad3 inhibition. Otolaryngology – Head and Neck Surgery 143:525–530.
   Google Scholar
• Lefaix JL, Delanian S, Vozenin MC, Leplat JJ, Tricaud Y, Martin M. 1999. Striking regression of subcutaneous fibrosis induced by high doses of gamma rays using a combination of pentoxifylline and alpha- tocopherol: An experimental study. International Journal of Radiation Oncology • Biology • Physics 43:839–847.
   PubMed Web of Science ®Google Scholar
• Liang L, Hu D, Liu W, Williams JP, Okunieff P, Ding I. 2003. Celecoxib reduces skin damage after radiation: Selective reduction of chemokine and receptor mRNA expression in irradiated skin but not in irradiated mammary tumor. American Journal of Clinical Oncology 26:S114–121.
   PubMed Web of Science ®Google Scholar
• Liu W, Ding I, Chen K, Olschowka J, Xu J, Hu D, Morrow GR, Okunieff P. 2006. Interleukin 1beta (IL1β) signaling is a critical component of radiation-induced skin fibrosis. Radiation Research 165:181–191.
   PubMed Web of Science ®Google Scholar
• Lo YY, Wong JM, Cruz TF. 1996. Reactive oxygen species mediate cytokine activation of c-Jun NH2-terminal kinases. The Journal of Biological Chemistry 271:15703–15707.
   PubMed Web of Science ®Google Scholar
• Lombaert IM, Wierenga PK, Kok T, Kampinga HH, deHaan G, Coppes RP. 2006. Mobilization of bone marrow stem cells by granulocyte colony-stimulating factor (G-CSF) ameliorates radiation-induced damage to salivary glands. Clinical Cancer Research 12:1804–1812.
   PubMed Web of Science ®Google Scholar
• Mantovani A. 2006. Macrophage diversity and polarization in vivo veritas. Blood 108:408–409.
   Web of Science ®Google Scholar
• Martin M, Lefaix J, Delanian S. 2000. TGF-β1 and radiation fibrosis: A master switch and a specific therapeutic target?International Journal of Radiation Oncology • Biology • Physics 47:277–290.
   PubMed Web of Science ®Google Scholar
• Müller K, Meineke V. 2007. Radiation-induced alterations in cytokine production by skin cells. Experimental Hematology 35:96–104.
   PubMed Web of Science ®Google Scholar
• Nawroth I, Alsner J, Behlke MA, Besenbacher F, Overgaard J, Howard KA, Kjems J. 2010. Intraperitoneal administration of chitosan/DsiRNA nanoparticles targeting TNF-α prevents radiation-induced fibrosis. Radiotherapy & Oncology 97:143–148.
   PubMed Web of Science ®Google Scholar
• Ning S, Budas GR, Churchill EN, Chen CH, Knox SJ, Mochly-Rosen D. 2012. Mitigation of radiation-induced dermatitis by activation of aldehyde dehydrogenase 2 using topical adla-1 in mice. Radiation Research 178:69–74.
   PubMed Web of Science ®Google Scholar
• Okunieff P, Augustine E, Hicks JE, Cornelison TL, Altemus RM, Naydich BG, Ding I, Huser AK, Abraham EH, Smith JJ, Coleman N. 2004. Pentoxifylline in the treatment of radiation-induecd fibrosis. Journal of Clinical Oncology 22:2207–2213.
   PubMed Web of Science ®Google Scholar
• Patan S. 2004. Vasculogenesis and angiogenesis. Cancer Treatment and Research 117:3–32.
   PubMedGoogle Scholar
• Peled A, Kollet O, Ponomaryov T, Petit I, Franitza S, Grabovsky V, Slav MM, Nagler A, Lider O, Alon R, Zipori D, Lapidot T. 2000. The chemokine SDF-1 activates the integrins LFA-1, VLA-4 and VLA-5 on immature CD34(+) cells: Role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 95:3289–3296.
   PubMed Web of Science ®Google Scholar
• Penn MS. 2009. Importance of the SDF-1:CXCR4 axis in myocardial repair. Circulation Research 104:1133–1135.
   PubMed Web of Science ®Google Scholar
• Rabbani ZN, Anscher MS, Folz RJ, Archer E, Huang H, Chen L, Golson ML, Samulski TS, Dewhirst MW, Vujaskovic Z. 2005. Overexpression of extracellular superoxide dismutase reduces acute radiation induced lung toxicity. BMC Cancer 5:59.
   PubMed Web of Science ®Google Scholar
• Randall K, Coggle JE. 1995. Expression of transforming growth factor-beta 1 in mouse skin during the acute phase of radiation damage. International Journal of Radiation Biology 68:301–309.
   PubMed Web of Science ®Google Scholar
• Riccobono D, Agay D, Scherthan H, Forcheron F, Vivier M, Ballester B, Meineke V, Drouet M. 2012. Application of adipocyte-derived stem cells in treatment of cutaneous radiation syndrome. Health Physics 103:120–126.
   PubMed Web of Science ®Google Scholar
• Rhee SG, Chae HZ, Kim K. 2005. Peroxiredoxins; a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radical Biology and Medicine 38:1543–1552.
   PubMed Web of Science ®Google Scholar
• Robbins ME, Zhao W. 2004. Chronic oxidative stress and radiation-induced late normal tissue injury: A review. International Journal of Radiation Biology 80:251–259.
   PubMed Web of Science ®Google Scholar
• Rosenthal RA, Fish B, Hill RP, Huffman KD, Lazarova Z, Mahmood J, Medhora M, Molthen R, Moulder JE, Sonis ST, Tofilon PJ, Doctrow SR. 2011. Salen Mn complexes mitigate radiation injury in normal tissues. Anti-Cancer Agents in Medicinal Chemistry 11:359–372.
   PubMed Web of Science ®Google Scholar
• Schnackenberg CG. 2002. Oxygen radicals in cardiovascular-renal disease. Current Opinion in Pharmacology 2:121–125.
   PubMed Web of Science ®Google Scholar
• Sharma M, Afrin F, Satija N, Tripathi RP, Gangenahalli GU. 2011. Stromal-derived factor-1/CXCR4 signaling: Indispensable role in homing and engraftment of hematopoietic stem cells in bone marrow. Stem Cells and Development 20:933–946.
   PubMedGoogle Scholar
• Steinberg M, Silva M. 2010. Plerixafor: A chemokine receptor-4 antagonist for mobilization of hematopoetic stem cells for transplantation after high-dose chemotherapy for non-Hodgkin's lymphoma or multiple myeloma. Clinical Therapeutics 32:821–843.
   PubMed Web of Science ®Google Scholar
• Uchida D, Onoue T, Kuribayashi N, Tomizuka Y, Tamatani T, Nagai H, Miyamoto Y. 2011. Blockade of CXCR4 in oral squamous cell carcinoma inhibits lymph node metastases. European Journal of Cancer 47:452–459.
   Google Scholar
• Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology 39:44–84.
   PubMed Web of Science ®Google Scholar
• van Horssen R, Ten Hagen TL, Eggermont AM. 2006. TNF-alpha in cancer treatment: Molecular insights, antitumor effects, and clinical utility. Oncologist 11:397–408.
   PubMed Web of Science ®Google Scholar
• Varmavuo V, Mantymaa P, Silvennoinen R, Nousiainen T, Kuittinen T, Jantunen E. 2012. CD34 + cell subclasses and lymphocyte subsets in blood grafts collected after various mobilization methods in myeloma patients. Transfusion (In press). doi: 10.1111/j.1537-2995.2012.03848.x.
   Google Scholar
• Wright N, Hidalgo A, Rodríguez-Frade JM, Soriano SF, Mellado M, Parmo-Cabañas M, Briskin MJ, Teixidó J. 2002. The chemokine stromal cell-derived factor-1 alpha modulates alpha 4 beta 7 integrin-mediated lymphocyte adhesion to mucosal addressin cell adhesion molecule-1 and fibronectin. Journal of Immunology 168: 5268–5277.
   Google Scholar
• Wong D, Korz W. 2008. Translating an antagonist of chemokine receptor CXCR4: From bench to bedside. Clinical Cancer Research 14:7975–7980.
   PubMed Web of Science ®Google Scholar
• Xavier S, Piek E, Fujii M, Javelaud D, Mauviel A, Flanders KC, Samuni AM, Felici A, Reiss M, Yarkoni S, Sowers A, Mitchell JB, Roberts AB, Russo A. 2004. Amelioration of radiation-induced fibrosis: Inhibition of transforming growth factor-beta signaling by halofuginone. The Journal of Biological Chemistry 279: 15167–15176.
   PubMed Web of Science ®Google Scholar
• Yan S, Brown SL, Kolozsvary A, Freytag SO, Lu M, Kim JH. 2008. Mitigation of radiation-induced skin injury by AAV2-medicated MnSOD gene therapy. The Journal of Gene Medicine 10:1012–1018.
   PubMed Web of Science ®Google Scholar
• Yarnold J, Brotons MC. 2010. Pathogenic mechanisms in radiation fibrosis. Radiotherapy & Oncology 97:149–161.
   PubMed Web of Science ®Google Scholar