Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation

Stem Cells

Volumn 31, Issue 10, 2013, Pages 2231-2241

  Horton, Jason A ^a   Hudak, Kathryn E ^a   Chung, Eun Joo ^a   White, Ayla O ^a   Scroggins, Bradley T ^a   Burkeen, Jeffrey F ^a   Citrin, Deborah E ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Chronic inflammation; Dermal fibrosis; Ionizing radiation; Mesenchymal stem cell

Indexed keywords

CD163 ANTIGEN; COLLAGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR RECEPTOR 2;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CHRONIC INFLAMMATION; COCULTURE; CYTOKINE RELEASE; GENE EXPRESSION PROFILING; IMMUNOASSAY; IN VITRO STUDY; IONIZING RADIATION; MACROPHAGE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; RADIATION EXPOSURE; RADIATION INDUCED SKIN FIBROSIS; SKIN FIBROSIS;

CHRONIC INFLAMMATION; DERMAL FIBROSIS; IONIZING RADIATION; MESENCHYMAL STEM CELL;

ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; GENE EXPRESSION; INFLAMMATION MEDIATORS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; RADIATION INJURIES, EXPERIMENTAL; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; SKIN; SKIN DISEASES;

EID: 84887897144     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1483     Document Type: Article

References (52)

1. Zhao W, Robbins ME Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: Therapeutic implications. Curr Med Chem 2009;16:130-143.
2. Sivan V, Vozenin-Brotons MC, Tricaud Y et al. Altered proliferation and differentiation of human epidermis in cases of skin fibrosis after radiotherapy. Int J Radiat Oncol Biol Phys 2002;53:385-393.
3. Gallet P, Phulpin B, Merlin JL et al. Long-term alterations of cyto-kines and growth factors expression in irradiated tissues and relation with histological severity scoring. PLoS One 2011;6:e29399.
4. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 2006;8:315-317.
5. Abumaree M, Al Jumah M, Pace RA et al. Immunosuppressive properties of mesenchymal stem cells. Stem Cell Rev 2012;8:375-392.
6. Koppula PR, Chelluri LK, Polisetti N et al. Histocompatibility testing of cultivated human bone marrow stromal cells - A promising step towards pre-clinical screening for allogeneic stem cell therapy. Cell Immunol 2009;259:61-65.
7. Sioud M. New insights into mesenchymal stromal cell-mediated t-cell suppression through galectins. Scand J Immunol 2011;73:79-84.
8. Nemeth K, Leelahavanichkul A, Yuen PS et al. Bone marrow stromal cells attenuate sepsis via prostaglandin e(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15:42-49.
9. Kuzmina LA, Petinati NA, Parovichnikova EN et al. Multipotent mes-enchymal stromal cells for the prophylaxis of acute graft-versus-host disease-a phase ii study. Stem Cells Int 2012;2012:968213.
10. Kaplan JM, Youd ME, Lodie TA Immunomodulatory activity of mes-enchymal stem cells. Curr Stem Cell Res Therapy 2011;6:297-316.
11. Wang J, Liao L, Tan J. Mesenchymal-stem-cell-based experimental and clinical trials: Current status and open questions. Expert Opin Biol Ther 2011;11:893-909.
12. Horton JA, Chung EJ, Hudak KE et al. Inhibition of radiation-induced skin fibrosis with imatinib. Int J Radiat Biol 2013;89:162-170.
13. Stone HB. Leg contracture in mice: An assay of normal tissue response. Int J Radiat Oncol Biol Phys 1984;10:1053-1061.
14. Randall K, Coggle JE Expression of transforming growth factor-beta 1 in mouse skin during the acute phase of radiation damage. Int J Radiat Biol 1995;68:301-309.
15. Sudo K, Kanno M, Miharada K et al. Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 2007;25:1610-1617.
16. Philippidis P, Mason JC, Evans BJ et al. Hemoglobin scavenger receptor cd163 mediates interleukin-10 release and heme oxygenase-1 synthesis: Antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ Res 2004;94:119-126.
17. Murray PJ, Wynn TA Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011;11:723-737.
18. Ricardo SD, van Goor H, Eddy AA Macrophage diversity in renal injury and repair. J Clin Invest 2008;118:3522-3530.
19. Lareu RR, Zeugolis DI, Abu-Rub M et al. Essential modification of the sircol collagen assay for the accurate quantification of collagen content in complex protein solutions. Acta Biomater 2010;6:3146-3151.
20. Zhang X, Goncalves R, Mosser DM The isolation and characterization of murine macrophages. Curr Protoc Immunol 2008;Chapter 14:Unit 14 1.
21. Zhang QZ, Su WR, Shi SH et al. Human gingiva-derived mesenchy-mal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 2010;28:1856-1868.
22. Flanders KC. Smad3 as a mediator of the fibrotic response. Int J Exp Pathol 2004;85:47-64.
23. Anscher MS. Targeting the tgf-beta1 pathway to prevent normal tissue injury after cancer therapy. Oncologist 2010;15:350-359.
24. Masli S, Turpie B. Anti-inflammatory effects of tumour necrosis factor (tnf)-alpha are mediated via tnf-r2 (p75) in tolerogenic transforming growth factor-beta-treated antigen-presenting cells. Immunology 2009; 127:62-72.
25. Xavier S, Piek E, Fujii M et al. Amelioration of radiation-induced fibrosis: Inhibition of transforming growth factor-beta signaling by hal-ofuginone. J Biol Chem 2004;279:15167-15176.
26. Flanders KC, Major CD, Arabshahi A et al. Interference with transforming growth factor-beta/ smad3 signaling results in accelerated healing of wounds in previously irradiated skin. Am J Pathol 2003; 163:2247-2257.
27. Landry Y, Le O, Mace KA et al. Secretion of sdf-1alpha by bone marrow-derived stromal cells enhances skin wound healing of c57bl/6 mice exposed to ionizing radiation. J Cell Mol Med 2010;14:1594-1604.
28. Jackson WM, Nesti LJ, Tuan RS Mesenchymal stem cell therapy for attenuation of scar formation during wound healing. Stem Cell Res Ther 2012;3:20.
29. Heo SC, Jeon ES, Lee IH et al. Tumor necrosis factor-alpha-activated human adipose tissue-derived mesenchymal stem cells accelerate cutaneous wound healing through paracrine mechanisms. J Invest Derma-tol 2011;131:1559-1567.
30. Ding J, Hori K, Zhang R et al. Stromal cell-derived factor 1 (sdf-1) and its receptor cxcr4 in the formation of postburn hypertrophic scar (hts). Wound Repair Regen 2011;19:568-578.
31. Agay D, Scherthan H, Forcheron F et al. Multipotent mesenchymal stem cell grafting to treat cutaneous radiation syndrome: Development of a new minipig model. Exp Hematol 2010;38:945-956.
32. Akita S, Akino K, Hirano A et al. Mesenchymal stem cell therapy for cutaneous radiation syndrome. Health Phys 2010;98:858-862.
33. Lataillade JJ, Doucet C, Bey E et al. New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mes-enchymal stem cell therapy. Regen Med 2007;2:785-794.
34. Ortiz LA, Gambelli F, McBride C et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 2003;100: 8407-8411.
35. Brody AR, Salazar KD, Lankford SM Mesenchymal stem cells modulate lung injury. Proc Am Thorac Soc 2010;7:130-133.
36. Hanson SE, Bentz ML, Hematti P. Mesenchymal stem cell therapy for nonhealing cutaneous wounds. Plast Reconstr Surg 2010;125:510-516.
37. Ryan JM, Barry FP, Murphy JM et al. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond) 2005;2:8.
38. Zonta S, De Martino M, Bedino G et al. Which is the most suitable and effective route of administration for mesenchymal stem cell-based immunomodulation therapy in experimental kidney transplantation: Endovenous or arterial? Transplant Proc 2010;42:1336-1340.
39. Sensebe L, Bourin P, Tarte K. Good manufacturing practices production of mesenchymal stem/stromal cells. Hum Gene Ther 2011;22: 19-26.
40. Romieu-Mourez R., Francois M, Boivin MN et al. Regulation of MHC class ii expression and antigen processing in murine and human mes-enchymal stromal cells by IFN-gamma, TGF-beta, and cell density. J Immunol 2007;179:1549-1558.
41. Chan WK, Lau AS, Li JC et al. Mhc expression kinetics and immuno-genicity of mesenchymal stromal cells after short-term ifn-gamma challenge. Exp Hematol 2008;36:1545-1555.
42. Chan JL, Tang KC, Patel AP et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood 2006;107:4817-4824.
43. Crop MJ, Baan CC, Korevaar SS et al. Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesen-chymal stem cells. Clin Exp Immunol 2010;162:474-486.
44. Lugade AA, Sorensen EW, Gerber SA et al. Radiation-induced ifn-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008;180:3132-3139.
45. Netea MG, Nold-Petry CA, Nold MF et al. Differential requirement for the activation of the inflammasome for processing and release of il-1beta in monocytes and macrophages. Blood 2009;113:2324-2335.
46. Liu G, Ma H, Qiu L et al. Phenotypic and functional switch of macrophages induced by regulatory cd4+cd25+ t cells in mice. Immunol Cell Biol 2011;89:130-142.
47. Gur-Wahnon D., Borovsky Z, Beyth S et al. Contact-dependent induction of regulatory antigen-presenting cells by human mesenchymal stem cells is mediated via stat3 signaling. Exp Hematol 2007;35:426-433.
48. Maggini J, Mirkin G, Bognanni I et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 2010;5:e9252.
49. Zhang H, Han G, Liu H et al. The development of classically and alternatively activated macrophages has different effects on the varied stages of radiation-induced pulmonary injury in mice. J Radiat Res 2011;52:717-726.
50. He Z, Zhang H, Yang C et al. The interaction between different types of activated raw 264.7 cells and macrophage inflammatory protein-1 alpha. Radiat Oncol 2011;6:86.
51. Schaue D, Xie MW, Ratikan JA et al. Regulatory t cells in radiothera-peutic responses. Front Oncol 2012;2:90.
52. Mayer A, Lee S, Jung F et al. Cd14+ cd163+ il-10+ monocytes/mac-rophages: Pro-angiogenic and non pro-inflammatory isolation, enrichment and long-term secretion profile. Clin Hemorheol Microcirc 2010; 46:217-223.