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

International Journal of Radiation Biology

Volumn 89, Issue 5, 2013, Pages 311-318

  Kim, Jae Ho ^a   Kolozsvary, Andrew J J ^a   Jenrow, Kenneth A ^a   Brown, Stephen L ^a  

^a HENRY FORD HOSPITAL   (United States)

Author keywords

Cutaneous; Injury; Mechanism; Radiation

Indexed keywords

ALPHA TOCOPHEROL; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; BUTYRIC ACID; CELECOXIB; CHEMOKINE; CLODRONIC ACID; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ETANERCEPT; FREE RADICAL; HALOFUGINONE; HISTONE DEACETYLASE INHIBITOR; LY 2109761; PENTOXIFYLLINE; PLERIXAFOR; PROTEIN KINASE INHIBITOR; RAMIPRIL; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VALPROIC ACID;

ARTICLE; BONE MARROW CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER TISSUE; CELL DEATH; DISEASE SEVERITY; EPITHELIUM; HUMAN; INTENSITY MODULATED RADIATION THERAPY; MACROPHAGE; MICROVASCULATURE; MOLECULAR MECHANICS; MORBIDITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIATION INJURY; RADIATION SKIN INJURY; RISK ASSESSMENT; SKIN FIBROSIS; SKIN INJURY; STEM CELL; STROMA CELL; TISSUE INJURY; TISSUE REPAIR; TREATMENT OUTCOME;

ANIMALS; BONE MARROW CELLS; CHEMOKINES; CLINICAL TRIALS AS TOPIC; HUMANS; RADIATION INJURIES; REACTIVE OXYGEN SPECIES; SKIN;

EID: 84877309085     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553002.2013.765055     Document Type: Article

References (73)

1. 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
2. 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- ® 1-guided very high dose thoracic radiotherapy . International Journal of Radiation Oncology • Biology • Physics 56: 988- 995
3. Archambeau JO, Hauser D, Shymko RM . 1988. Swine basal cell proliferation during a course of daily irradiation fi ve days a week for six weeks . International Journal of Radiation Oncology • Biology • Physics 15: 1383- 1388
4. Archambeau JO, Ines A, Fajardo LF . 1984 . Response of swine skin microvasculature to acute single exposure of x-rays: Quantifi cation of endothelial changes . Radiation Research 98: 37- 51
5. 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 fi brosis . American Journal of Physiology Cell Physiology 299: C589- 605
6. 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
7. 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
8. Brindel I, Legrand M . 2011 Trial of combined Pentoxifyllinetocopherol- clodronate versus placebo in radiation-induced brachial plexopathy (PENTOCLO) . [Cited 29 August 2012]. Available from: Http://clinicaltrials.gov/ct2/show/ NCT01291433
9. 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
10. Burrell K, Hill RP, Zadeh G . 2012 . High-resolution in-vivo analysis of normal brain response to cranial irradiation . PLoS ONE 7 : E38366
11. 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
12. 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 fi brosis . Journal of Cellular and Molecular Medicine 8 : 109 - 116
13. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC . 2004 Progenitor cell traffi cking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 . Nature Medicine 10 : 858 - 864
14. 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
15. 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
16. De Clerq E . 2003 . The bicyclam AMD3100 story . Nature Reviews Drug Discovery 2: 581- 587
17. Delanian S, Baillet F, Huart J, Lefaix JL, Maulard C, Housset M . 1994 . Successful treatment of radiation-induced fi brosis using liposomal Cu/Zn superoxide dismutase: Clinical trial. Radiotherapy & Oncology 32 : 12 - 20
18. Delanian S, Lefaix JL . 2007 . Current management for late normal tissue injury: Radiation-induced fi brosis and necrosis . Seminars in Radiation Oncology 17 : 99 - 107
19. 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 fi brosis . Journal of Clinical Oncology 21 : 2545 - 2550
20. Donahue RE, Jin P, Bonifacino AC, Metzger ME, Ren J, Wang E, Stroncek DF . 2009 . Plerixafor (AMD3100) and granulocyte colonystimulating factor (G-CSF) mobilize different CD34 - cell populations based on global gene and microRNA expression signatures . Blood 114 : 2530 - 2541
21. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegu é 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
22. 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
23. Flanders KC . 2004 . Smad3 as a mediator of the fi brotic response . International Journal of Experimental Pathology 85 : 47 - 64
24. 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
25. Flechsig P, Dadrich M, Bickelhaupt S, Jenne J, Hauser K, Timke C, Peschke P, Hahn EW, Gr öne HJ, Yingling J, Lahn M, Wirkner U, Huber PE . 2012 . LY2109761 attenuates radiation-induced pulmonary murine fi brosis via reversal of TGF-beta and BMP-associated proinfl ammatory and proangiogenic signals . Clinical Cancer Research 18: 3616- 3627
26. Fran ç ois S, Mouiseddine M, Mathieu N, Semont A, Monti P, Dudoignon N, Saché A, Boutarfa A, Th ierry D, Gourmelon P, Chapel A 2007 . Human mesenchymal stem cells favour healing of the cutaneous radiation syndrome in a xenogenic transplaet model . Annals of Hematology 86 : 1 - 8
27. 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
28. 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 fi brosis after surgery and radiotherapy for breast cancer . Radiotherapy & Oncology 73 : 133 - 139
29. Heissig B, Rafi i 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
30. 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
31. Hopewell JW . 1990 . The skin: Its structure and response to ionizing radiation . International Journal of Radiation Biology 57 : 751 - 773
32. Jaal J, Richter C, D ö rr W . 2010 . Effect of recombinant human keratinocyte growth factor (rHuKGF, Palifermin) on infl ammatory and immune changes in mouse tongue during fractionated irradiation . International Journal of Radiation Biology 86 : 860 - 866
33. 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
34. 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
35. Kioi M, Vogel H, Schultz G, Hoff man 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
36. 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
37. 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
38. Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K . 2008. Factors that infl uence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model . Haematologica 93 : 1457 - 1465
39. 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
40. Lee JW, Tutela JP, Zoumalan RA, Th anik VD, Nguyen PD, Varjabedian L, Warren SM, Saadeh PB . 2010a . Inhibition of Smad3 expression in radiation-induced fi brosis using a novel method for topical transcutaneous gene therapy. Archives of Otolaryngology - Head & Neck Surgery 136: 714- 719
41. Lee JW, Zoumalan RA, Valenzuela CD, Nguyen PD, Tutela JP, Roman BR, Warren SM, Saadeh PB . 2010b . Regulators and mediators of radiationinduced fi brosis: Gene expression profi les and a rationale for Smad3 inhibition. Otolaryngology - Head and Neck Surgery 143: 525- 530
42. Lefaix JL, Delanian S, Vozenin MC, Leplat JJ, Tricaud Y, Martin M . 1999. Striking regression of subcutaneous fi brosis induced by high doses of gamma rays using a combination of pentoxifylline and alphatocopherol: An experimental study . International Journal of Radiation Oncology • Biology • Physics 43: 839- 847
43. 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
44. Liu W, Ding I, Chen K, Olschowka J, Xu J, Hu D, Morrow GR, Okunieff P . 2006 . Interleukin 1beta (IL1 ®) signaling is a critical component of radiation-induced skin fi brosis . Radiation Research 165: 181- 191
45. 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
46. Lombaert IM, Wierenga PK, Kok T, Kampinga HH, deHaan G, Coppes RP . 2006 . Mobilization of bone marrow stem cells by granulocyte colonystimulating factor (G-CSF) ameliorates radiation-induced damage to salivary glands . Clinical Cancer Research 12: 1804- 1812
47. Mantovani A . 2006. Macrophage diversity and polarization in vivo veritas . Blood 108 : 408 - 409
48. Martin M, Lefaix J, Delanian S . 2000 . TGF- ® 1 and radiation fi brosis: A master switch and a specifi c therapeutic target? International Journal of Radiation Oncology • Biology • Physics 47: 277- 290
49. M üller K, Meineke V . 2007. Radiation-induced alterations in cytokine production by skin cells . Experimental Hematology 35 : 96 - 104
50. Nawroth I, Alsner J, Behlke MA, Besenbacher F, Overgaard J, Howard KA, Kjems J . 2010 . Intraperitoneal administration of chitosan/DsiRNA nanoparticles targeting TNF- 〈 prevents radiationinduced fi brosis . Radiotherapy & Oncology 97: 143- 148
51. 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
52. 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 fi brosis . Journal of Clinical Oncology 22 : 2207 - 2213
53. Patan S . 2004 . Vasculogenesis and angiogenesis . Cancer Treatment and Research 117: 3- 32
54. 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
55. Penn MS . 2009. Importance of the SDF-1:CXCR4 axis in myocardial repair . Circulation Research 104: 1133- 1135
56. 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
57. Randall K, Coggle JE . 1995 . Expression of transforming growth factorbeta 1 in mouse skin during the acute phase of radiation damage . International Journal of Radiation Biology 68 : 301 - 309
58. 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
59. 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
60. Robbins ME, Zhao W . 2004. Chronic oxidative stress and radiationinduced late normal tissue injury: A review . International Journal of Radiation Biology 80: 251- 259
61. Rosenthal RA, Fish B, Hill RP, Huff man KD, Lazarova Z, Mahmood J, Medhora M, Molthen R, Moulder JE, Sonis ST, Tofi lon PJ, Doctrow SR . 2011 . Salen Mn complexes mitigate radiation injury in normal tissues . Anti-Cancer Agents in Medicinal Chemistry 11 : 359 - 372
62. Schnackenberg CG . 2002. Oxygen radicals in cardiovascular-renal disease . Current Opinion in Pharmacology 2: 121- 125
63. 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
64. 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
65. 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
66. 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
67. 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
68. 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.
69. Wright N, Hidalgo A, Rodr íguez-Frade JM, Soriano SF, Mellado M, Parmo-Cabañ as 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 fi bronectin . Journal of Immunology 168 : 5268 - 5277
70. Wong D, Korz W . 2008. Translating an antagonist of chemokine receptor CXCR4: From bench to bedside . Clinical Cancer Research 14 : 7975 - 7980
71. 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 fi brosis: Inhibition of transforming growth factor-beta signaling by halofuginone . The Journal of Biological Chemistry 279 : 15167 - 15176
72. 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
73. Yarnold J, Brotons MC . 2010 . Pathogenic mechanisms in radiation fi brosis . Radiotherapy & Oncology 97: 149- 161