Enhanced epithelial gap closure and increased angiogenesis in wounds of diabetic mice treated with adult murine bone marrow stromal progenitor cells

Wound Repair and Regeneration

Volumn 15, Issue 3, 2007, Pages 350-359

  Javazon, Elisabeth H ^a   Keswani, Sundeep G ^a,b   Badillo, Andrea T ^a   Crombleholme, Timothy M ^b   Zoltick, Philip W ^a   Radu, Antoneta P ^a   Kozin, Elliot D ^a   Beggs, Kirstin ^a   Malik, Asim A ^a   Flake, Alan W ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FICOLL; GREEN FLUORESCENT PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL ISOLATION; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; EPITHELIZATION; GRANULATION TISSUE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; STEM CELL; VASCULARIZATION; WOUND; WOUND CLOSURE; WOUND HEALING IMPAIRMENT;

ANALYSIS OF VARIANCE; ANIMALS; CELL DIFFERENTIATION; DIABETES MELLITUS; FLOW CYTOMETRY; IMMUNOENZYME TECHNIQUES; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEOVASCULARIZATION, PHYSIOLOGIC; WOUND HEALING; WOUNDS AND INJURIES;

EID: 34249277465     PISSN: 10671927     EISSN: 1524475X     Source Type: Journal    
DOI: 10.1111/j.1524-475X.2007.00237.x     Document Type: Article

References (40)

1. United States Department of Health and Human Services. National Diabetes Fact Sheet. 1997.
2. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005 366 : 1736 43.
3. Bennett SP, Griffiths GD, Schor AM, Leese GP, Schor SL. Growth factors in the treatment of diabetic foot ulcers. Br J Surg 2003 90 : 133 46.
4. Chleboun JO, Martins R, Rao S. Laser Doppler velocimetry and platelet-derived growth factor as prognostic indicators for the healing of ulcers and ischaemic lesions of the lower limb. Cardiovasc Surg 1995 3 : 285 90.
5. Pierce GF, Tarpley JE, Tseng J, Bready J, Chang D, Kenney WC, Rudolph R, Robson MC, Vande Berg J, Reid P. Detection of platelet-derived growth factor (PDGF)-AA in actively healing human wounds treated with recombinant PDGF-BB and absence of PDGF in chronic nonhealing wounds. J Clin Invest 1995 96 : 1336 50.
6. Niezgoda JA, Van Gils CC, Frykberg RG, Hodde JP. Randomized clinical trial comparing OASIS wound matrix to regranex gel for diabetic ulcers. Adv Skin Wound Care 2005 18 : 258 66.
7. Keswani SG, Katz AB, Lim FY, Zoltick P, Radu A, Alaee D, Herlyn M, Crombleholme TM. Adenoviral mediated gene transfer of PDGF-B enhances wound healing in type I and type II diabetic wounds. Wound Repair Regen 2004 12 : 497 504.
8. Lee JA, Conejero JA, Mason JM, Parrett BM, Wear-Maggitti KD, Grant RT, Breitbart AS. Lentiviral transfection with the PDGF-B gene improves diabetic wound healing. Plast Reconstr Surg 2005 116 : 532 8.
9. Liechty KW, Crombleholme TM, Quinn TM, Cass DL, Flake AW, Adzick NS. Elevated platelet-derived growth factor-B in congenital cystic adenomatoid malformations requiring fetal resection. J Pediatr Surg 1999 34 : 805 9 discussion 809-10.
10. Badiavas EV, Abedi M, Butmarc J, Falanga V, Quesenberry P. Participation of bone marrow derived cells in cutaneous wound healing. J Cell Physiol 2003 196 : 245 50.
11. Herzog EL, Chai L, Krause DS. Plasticity of marrow-derived stem cells. Blood 2003 102 : 3483 93.
12. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, Shimada K, Iwasaka T, Imaizumi T. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 2002 360 : 427 35.
13. Badiavas EV, Falanga V. Treatment of chronic wounds with bone marrow-derived cells. Arch Dermatol 2003 139 : 510 6.
14. Stepanovic V, Awad O, Jiao C, Dunnwald M, Schatteman GC. Leprdb diabetic mouse bone marrow cells inhibit skin wound vascularization but promote wound healing. Circ Res 2003 92 : 1247 53.
15. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JF, Gartner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002 106 : 2781 6.
16. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974 17 : 331 40.
17. Kadiyala S, Young RG, Thiede MA, Bruder SP. Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell Transplant 1997 6 : 125 34.
18. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997 276 : 71 4.
19. Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, Yang SE, Yang YS, Im HJ, Kim KN, Jung HL, Sung KW, Koo HH. Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine 2005 31 : 119 26.
20. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004 94 : 678 85.
21. Gregory CA, Ylostalo J, Prockop DJ. Adult bone marrow stem/progenitor cells (MSCs) are preconditioned by microenvironmental "niches" in culture: a two-stage hypothesis for regulation of MSC fate. Sci STKE 2005 2005: pe37.
22. Digirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 1999 107 : 275 81.
23. Javazon EH, Colter DC, Schwarz EJ, Prockop DJ. Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 2001 19 : 219 25.
24. Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthr Rheum 2002 46 : 704 13.
25. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, Dragoo JL, Ashjian P, Thomas B, Chan T, Fraser J, Hedrick MV. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003 174 : 101 9.
26. Gang EJ, Jeong JA, Han S, Yan Q, Jeon CJ, Kim H. In vitro endothelial potential of human UC blood-derived mesenchymal stem cells. Cytotherapy 2006 8 : 215 27.
27. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 2004 22 : 377 84.
28. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 2002 109 : 337 46.
29. Kubis N, Tomita Y, Tran-Dinh A, Planat-Benard V, Andre M, Karaszewski B, Waeckel L, Penicaud L, Silvestre JS, Casteilla L, Seylaz J, Pinard E. Vascular fate of adipose tissue-derived adult stromal cells in the ischemic murine brain: a combined imaging-histological study. Neuroimage 2006.
30. Nagaya N, Fujii T, Iwase T, Ohgushi H, Itoh T, Uematsu M, Yamagushi M, Mori H, Kangawa K, Kitamura S. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 2004 287 : H2670 6.
31. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006 98 : 1076 84.
32. Mandel MA, Mahmoud AA. Impairment of cell-mediated immunity in mutation diabetic mice (db/db). J Immunol 1978 120 : 1375 7.
33. Matarese G, Moschos S, Mantzoros CS. Leptin in immunology. J Immunol 2005 174 : 3137 42.
34. Kievits F, Boerenkamp WJ, Ivanyi P. H-2-dependent binding of xenogeneic beta 2-microglobulin from culture media. J Immunol 1988 140 : 4253 5.
35. MacDermott RP, Bragdon MJ. Fetal calf serum augmentation during cell separation procedures accounts for the majority of human autologous mixed leukocyte reactivity. Behring Inst Mitt 1983 : 122 8.
36. Spees JL, Gregory CA, Singh H, Tucker HA, Peister A, Lynch PJ, Hsu SC, Smith J, Prockop DJ. Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy. Mol Ther 2004 9 : 747 56.
37. Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res 2005 306 : 330 5.
38. Murshed M, Harmey D, Millan JL, McKee MD, Karsenty G. Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev 2005 19 : 1093 104.
39. Fathke C, Wilson L, Hutter J, Kapoor V, Smith A, Hocking A, Isik F. Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem Cells 2004 22 : 812 22.
40. Kasten P, Vogel J, Luginbuhl R, Niemeyer P, Weiss S, Schneider S, Kramer M, Leo A, Richter W. Influence of platelet-rich plasma on osteogenic differentiation of mesenchymal stem cells and ectopic bone formation in calcium phosphate ceramics. Cells Tissues Organs 2006 183 : 68 79.