Transplanted bone marrow-derived circulating PDGFRα+ cells restore type VII collagen in recessive dystrophic epidermolysis bullosa mouse skin graft

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1996-2003

  Iinuma, Shin ^a,b   Aikawa, Eriko ^a   Tamai, Katsuto ^a   Fujita, Ryo ^a   Kikuchi, Yasushi ^a   Chino, Takenao ^a   Kikuta, Junichi ^a   McGrath, John A ^c   Uitto, Jouni ^d   Ishii, Masaru ^a   Iizuka, Hajime ^b   Kaneda, Yasufumi ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; COLLAGEN TYPE 7; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STROMAL CELL DERIVED FACTOR 1ALPHA; CXCR4 PROTEIN, MOUSE; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENGRAFTMENT; EPIDERMOLYSIS BULLOSA DYSTROPHICA; FEMALE; KERATINOCYTE; MALE; MESENCHYME CELL; MIGRATION INHIBITION; MOUSE; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; RECESSIVE DYSTROPHIC EPIDERMOLYSIS BULLOSA; SIGNAL TRANSDUCTION; SKIN GRAFT; WILD TYPE; ANIMAL; C57BL MOUSE; CELL SEPARATION; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; KNOCKOUT MOUSE; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SKIN TRANSPLANTATION;

ANIMALS; BONE MARROW TRANSPLANTATION; CELL SEPARATION; CHEMOKINE CXCL12; COLLAGEN TYPE VII; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPIDERMOLYSIS BULLOSA DYSTROPHICA; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; SKIN TRANSPLANTATION;

EID: 84922496708     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400914     Document Type: Article

References (44)

1. Chino, T., K. Tamai, T. Yamazaki, S. Otsuru, Y. Kikuchi, K. Nimura, M. Endo, M. Nagai, J. Uitto, Y Kitajima, and Y Kaneda. 2008. Bone marrow cell transfer into fetal circulation can ameliorate genetic skin diseases by providing fibroblasts to the skin and inducing immune tolerance. Am. J. Pathol 173: 803-814.
2. Wagner, J. E., A. Ishida-Yamamoto, J. A. McGrath, M. Hordinsky, D. R. Keene, D. T. Woodley, M. Chen, M. J. Riddle, M. J. Osbom, T. Lund, et al. 2010. Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N Engl. J. Med. 363: 629-639.
3. Prockop, D. J. 2009. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther. 17: 939-946.
4. Orkin, S. H., and L. I. Zon. 2008. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631-644.
5. Pittenger, M. F., A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig, and D. R. Marshak. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
6. Prockop, D. J. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74.
7. Pereira, R. F., K. W. Halford, M. D. O'Hara, D. B. Leeper, B. P. Sokolov, M. D. Pollard, O. Bagasra, and D. J. Prockop. 1995. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc. Natl. Acad. Sci. USA 92: 4857-4861.
8. Galmiche, M. C, V. E. Koteliansky, J. Brière, P. Hervé, and P. Charbord. 1993. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood 82: 66-76.
9. Tropel, P., N. Platet, J. C. Platel, D. Noël, M. Albrieux, A. L. Benabid, and F. Berger. 2006. Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells 24: 2868-2876.
10. Kang, S. K., L. A. Putnam, J. Ylostalo, I. R. Popescu, J. Dufour, A. Belousov, and B. A. Bunnell. 2004. Neurogenesis of Rhesus adipose stromal cells. J. Cell Sci. 117:4289-4299.
11. Deng, W., Q. Han, L. Liao, C. Li, W. Ge, Z. Zhao, S. You, H. Deng, F. Murad, and R. C. Zhao. 2005. Engrafted bone marrow-derived flk-(l+) mesenchymal stem cells regenerate skin tissue. Tissue Eng. 11: 110-119.
12. Brittan, M., K. M. Braun, L. E. Reynolds, F. J. Conti, A. R. Reynolds, R. Poulsom, M. R. Alison, N. A. Wright, and K. M. Hodivala-Dilke. 2005. Bone marrow cells engraft within the epidermis and proliferate in vivo with no evidence of cell fusion. J. Pathol. 205: 1-13.
13. Fafhke, C, L. Wilson, J. Hutter, V. Kapoor, A. Smith, A. Hocking, and F Isik. 2004. Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem Cells 22: 812-822.
14. Tamai, K., T. Yamazaki, T. Chino, M. Ishii, S. Otsuru, Y Kikuchi, S. Iinuma, K. Saga, K. Nimura, T. Shimbo, et al. 2011. PDGFRαlpha-positive cells in bone marrow are mobilized by high mobility group box 1 (HMGB1) to regenerate injured epifhelia. Proc. Natl. Acad. Sci. USA 108: 6609-6614.
15. Morikawa, S., Y Mabuchi, Y Kubota, Y Nagai, K. Niibe, E. Hiratsu, S. Suzuki, C. Miyauchi-Hara, N. Nagoshi, T. Sunabori, et al. 2009. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206: 2483-2496.
16. Takashima, Y, T. Era, K. Nakao, S. Kondo, M. Kasuga, A. G. Smith, and S. Nishikawa. 2007. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129: 1377-1388.
17. Hocking, A. M., and N. S. Gibran. 2010. Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp. Cell Res. 316: 2213-2219.
18. Wu, Y, R. C. Zhao, and E. E. Tredget. 2010. Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells 28: 905-915.
19. Kuznetsov, S. A., M. H. Mankani, S. Gronfhos, K. Satomura, P. Bianco, and P. G. Robey. 2001. Circulating skeletal stem cells. J. Cell Biol. 153: 1133-1140.
20. Kuznetsov, S. A., M. H. Mankani, A. I. Leet, N. Ziran, S. Gronfhos, and P. G. Robey. 2007. Circulating connective tissue precursors: extreme rarity in humans and chondrogenic potential in guinea pigs. Stem Cells 25: 1830-1839.
21. Granero-Moltó, F., J. A. Weis, M. I. Miga, B. Landis, T. J. Myers, L. O'Rear, L. Longobardi, E. D. Jansen, D. P. Mortlock, and A. Spagnoli. 2009. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 27: 1887-1898.
22. Otsuru, S., K. Tamai, T. Yamazaki, H. Yoshikawa, and Y Kaneda. 2008. Circulating bone marrow-derived osteoblast progenitor cells are recruited to the bone-forming site by the CXCR4/stromal cell-derived factor-1 pathway. Stem Cells 26: 223-234.
23. Ceradini, D. J., A. R. Kulkarni, M. J. Callaghan, O. M. Tepper, N. Bastidas, M. E. Kleinman, J. M. Capla, R. D. Galiano, J. P. Levine, and G. C. Gurtner. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10: 858-864.
24. Askari, A. T., S. Unzek, Z. B. Popovic, C. K. Goldman, F. Forudi, M. Kiedrowski, A. Rovner, S. G. Ellis, J. D. Thomas, P. E. DiCorleto, et al. 2003. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362: 697-703.
25. Ma, Q., D. Jones, and T. A. Springer. 1999. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10: 463-471.
26. Nagasawa, T., S. Hirota, K Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, and T. Kishimoto. 1996. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382: 635-638.
27. Heinonen, S., M. Männikkö, J. F Klement, D. Whitaker-Menezes, G. F Murphy, and J. Uitto. 1999. Targeted inactivation of the type VII collagen gene (Co17al) in mice results in severe blistering phenotype: a model for recessive dystrophic epidermolysis bullosa. J. Cell Sci. 112: 3641-3648.
28. Alexeev, V., J. Uitto, and O. Igoucheva. 2011. Gene expression signatures of mouse bone marrow-derived mesenchymal stem cells in the cutaneous environment and therapeutic implications for blistering skin disorder. Cytotherapy 13: 30-45.
29. Morikawa, S., Y. Mabuchi, K. Niibe, S. Suzuki, N. Nagoshi, T. Sunabori, S. Shimmura, Y. Nagai, T. Nakagawa, H. Okano, and Y Matsuzaki. 2009. Development of mesenchymal stem cells partially originate from the neural crest. Biochem. Biophys. Res. Commun. 379: 1114-1119.
30. Sasaki, M., R. Abe, Y Fujita, S. Ando, D. Inokuma, and H. Shimizu. 2008. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J. Immunol. 180: 2581-2587.
31. Chen, L., E. E. Tredget, P. Y Wu, and Y Wu. 2008. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 3: e1886.
32. Wu, Y, J. Wang, P. G. Scott, and E. E. Tredget. 2007. Bone marrow-derived stem cells in wound healing: a review. Wound Repair Regen. 15(Suppl 1): S18-S26.
33. Kavanagh, H., and B. P. Mahon. 2011. Allogeneic mesenchymal stem cells prevent allergic airway inflammation by inducing murine regulatory T cells. Allergy 66: 523-531.
34. Choi, H., R. H. Lee, N. Bazhanov, J. Y Oh, and D. J. Prockop. 2011. Antiinflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NE-ΚB signaling in resident macrophages. Blood 118: 330-338.
35. Németh, K., A. Leelahavanichkul, P. S. Yuen, B. Mayer, A. Parmelee, K. Doi, P. G Robey, K. Leelahavanichkul, B. H. Koller, J. M. Brown, et al. 2009. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 15: 42-49.
36. English, K., J. M. Ryan, L. Tobin, M. J. Murphy, F. P. Barry, and B. P. Mahon. 2009. Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+ CD25(High) forkhead box P3+ regulatory T cells. Clin. Exp. Immunol. 156: 149-160.
37. Ji, J. F., B. P. He, S. T. Dheen, and S. S. Tay. 2004. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells 22: 415-427.
38. Cheng, Z., L. Ou, X. Zhou, F L.i., X. Jia, Y Zhang, X. Liu, Y L.i., C. A. Ward, L. G Melo, and D. Kong. 2008. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol. Ther. 16: 571-579.
39. Sackstein, R., J. S. Merzaban, D. W. Cain, N. M. Dagia, J. A. Spencer, C. P. Lin, and R. Wohlgemuth. 2008. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat. Med. 14: 181-187.
40. Ip, J. E., Y W.u., J. Huang, L. Zhang, R. E. Pratt, and V. J. Dzau. 2007. Mesenchymal stem cells use integrin betal not CXC chemokine receptor 4 for myocardial migration and engraftment. Mol. Biol. Cell 18: 2873-2882.
41. Ryynänen, J., S. Sollberg, M. G. Parente, L. C. Chung, A. M. Christiano, and J. Uitto. 1992. Type VII collagen gene expression by cultured human cells and in fetal skin. Abundant mRNA and protein levels in epidermal keratinocytes. J. Clin. Invest. 89: 163-168.
42. Woodley, D. T., R. A. Briggaman, W. R. Gammon, and E. J. O'Keefe. 1985. Epidermolysis bullosa acquisita antigen is synthesized by human keratinocytes cultured in serum-free medium. Biochem. Biophys. Res. Commun. 130: 1267-1272.
43. Stanley, J. R., N. Rubinstein, and V. Klaus-Kovtun. 1985. Epidermolysis bullosa acquisita antigen is synthesized by both human keratinocytes and human dermal fibroblasts. J. Invest. Dermatol. 85: 542-545.
44. Conget, P., F Rodriguez, S. Kramer, C. Allers, V. Simon, F Palisson, S. Gonzalez, and M. J. Yubero. 2010. Replenishment of type VII collagen and re-epithelialization of chronically ulcerated skin after intradermal administration of allogeneic mesenchymal stromal cells in two patients with recessive dystrophic epidermolysis bullosa. Cytotherapy 12: 429-431.