3,445
Views
31
CrossRef citations to date
0
Altmetric
Reviews

Diabetic ulcer regeneration: stem cells, biomaterials, growth factors

, &
Pages 26-32 | Received 13 Feb 2017, Accepted 06 Mar 2017, Published online: 29 Mar 2017

References

  • Wild S, Roglic G, Green A, et al. Global prevalence of diabetes: estimates for the year 2000 and projection for 2030. Diabetes Care. 2004;27:1047–1053.
  • Whiting DR, Guariguata L, Weil C, et al. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94:311–321.
  • Eldor R, Raz I, Yehuda AB, et al. New and experimental approaches to treatment of diabetic foot ulcers: a comprehensive review of emerging treatment strategies. Diabet Med. 2004;21:1161–1173.
  • Hong JP, Park SW. The combined effect of recombinant human epidermal growth factor and erythropoietin on full-thickness wound healing in diabetic rat model. Int Wound J. 2014;11:373–378.
  • Dinh T, Tecilazich F, Kafanas A, et al. Mechanisms involved in the development and healing of diabetic foot ulceration. Diabetes. 2012;61:2937–2947.
  • Galkowska H, Wojewodzka U, Olszewski WL. Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair Regen. 2006;14:558–565.
  • Eming SA, Koch M, Krieger A, et al. Differential proteomic analysis distinguishes tissue repair biomarker signatures in wound exudates obtained from normal healing and chronic wounds. J Proteome Res. 2010;9:4758–4766.
  • Khanna S, Biswas S, Shang Y, et al. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One. 2015;5:e9539.
  • Hübner G, Brauchle M, Smola H, et al. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine. 1996;8:548–556.
  • Kaiser GC, Polk DB. Tumor necrosis factor alpha regulates proliferation in a mouse intestinal cell line. Gastroenterology. 1997;112:1231–1240.
  • Xu F, Zhang C, Graves DT. Abnormal cell responses and role of TNF-?? in impaired diabetic wound healing. Biomed Res Int. 2013;2013:754802.
  • Steed DL. The role of growth factors in wound healing. Surg Clin North Am. 1997;77:575–586.
  • Desta T, Li J, Chino T, et al. Altered fibroblast proliferation and apoptosis in diabetic gingival wounds. J Dent Res. 2010;89:609–614.
  • Kwon DS, Gao X, Liu YB, et al. Treatment with bone marrow-derived stromal cells accelerates wound healing in diabetic rats. Int Wound J. 2008;5:453–463.
  • Steed DL. Clinical evaluation of recombinant human platelet-derived growth factor for the treatment of lower extremity ulcers. Plast Reconstr Surg. 2006;117:143S–149S. Discussion 150S–151S.
  • Smiell JM, Wieman TJ, Steed DL, et al. Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with nonhealing, lower extremity diabetic ulcers: a combined analysis of four randomized studies. Wound Repair Regen. 1999;7:335–346.
  • Wieman TJ. Clinical efficacy of becaplermin (rhPDGF-BB) gel. Becaplermin Gel Studies Group. Am J Surg. 1998;176:74S–79S.
  • Richard JL, Parer-Richard C, Daures JP, et al. Effect of topical basic fibroblast growth factor on the healing of chronic diabetic neuropathic ulcer of the foot. A pilot, randomized, double-blind, placebo-controlled study. Diabetes Care. 1995;18:64–69.
  • Gough A, Clapperton M, Rolando N, et al. Randomised placebo-controlled trial of granulocyte-colony stimulating factor in diabetic foot infection. Lancet. 1997;350:855–859.
  • de Lalla F, Pellizzer G, Strazzabosco M, et al. Randomized prospective controlled trial of recombinant granulocyte colony-stimulating factor as adjunctive therapy for limb-threatening diabetic foot infection. Antimicrob Agents Chemother. 2001;45:1094–1098.
  • Steed DL, Goslen JB, Holloway GA, et al. Randomized prospective double-blind trial in healing chronic diabetic foot ulcers. CT-102 activated platelet supernatant, topical versus placebo. Diabetes Care. 1992;15:1598–1604.
  • Ren G, Chen X, Dong F, et al. Concise review: mesenchymal stem cells and translational medicine: emerging issues. Stem Cells Transl Med. 2012;1:51–58.
  • Sasaki M, Abe R, Fujita Y, et al. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J Immunol. 2008;180:2581–2587.
  • Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815–1822.
  • Nakamura Y, Ishikawa H, Kawai K, et al. Enhanced wound healing by topical administration of mesenchymal stem cells transfected with stromal cell-derived factor-1. Biomaterials. 2013;34:9393–9400.
  • Tark K-C, Hong J-W, Kim Y-S, et al. Effects of human cord blood mesenchymal stem cells on cutaneous wound healing in leprdb mice. Ann Plast Surg. 2010;65:565–572.
  • Wu Y, Zhao RCH, Tredget EE. Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells. 2010;28:905–915.
  • Yoshikawa T, Mitsuno H, Nonaka I, et al. Wound therapy by marrow mesenchymal cell transplantation. Plast Reconstr Surg. 2008;121:860–877.
  • Zou J-P, Huang S, Peng Y, et al. Mesenchymal stem cells/multipotent mesenchymal stromal cells (MSCs): potential role in healing cutaneous chronic wounds. Int J Low Extreme Wounds. 2012;11:244–253.
  • Dash NR, Dash SN, Routray P, et al. Targeting nonhealing ulcers of lower extremity in human through autologous bone marrow-derived mesenchymal stem cells. Rejuvenation Res. 2009;12:359–366.
  • Lu D, Chen B, Liang Z, et al. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: a double-blind, randomized, controlled trial. Diabetes Res Clin Pract. 2011;92:26–36.
  • Hocking AM, Gibran NS. Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp Cell Res. 2010;316:2213–2219.
  • Lee SH, Jin SY, Song JS, et al. Paracrine effects of adipose-derived stem cells on keratinocytes and dermal fibroblasts. Ann Dermatol. 2012;24:136–143.
  • Mizuno H, Tobita M, Uysal AC. Concise review: adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells. 2012;30:804–810.
  • Kim EK, Li G, Lee TJ, et al. The effect of human adipose-derived stem cells on healing of ischemic wounds in a diabetic nude mouse model. Plast Reconstr Surg. 2011;128:387–394.
  • Yang M, Sheng L, Li H, et al. Improvement of the skin flap survival with the bone marrow-derived mononuclear cells transplantation in a rat model. Microsurgery. 2010;30:275–281.
  • Sivan-Loukianova E, Awad OA, Stepanovic V, et al. CD34+ blood cells accelerate vascularization and healing of diabetic mouse skin wounds. J Vasc Res. 2003;40:368–377.
  • Ruiz-Salmeron R, de la Cuesta-Diaz a, Constantino-Bermejo M, et al. Angiographic demonstration of neoangiogenesis after intra-arterial infusion of autologous bone marrow mononuclear cells in diabetic patients with critical limb ischemia. Cell Transplant. 2011;20:1629–1639.
  • Wu Y, Chen L, Scott PG, et al. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 2007;25:2648–2659.
  • Pedroso DCS, Tellechea A, Moura L, et al. Improved survival, vascular differentiation and wound healing potential of stem cells co-cultured with endothelial cells. PLoS One. 2011;6:e16114.
  • Kirana S, Stratmann B, Prante C, et al. Autologous stem cell therapy in the treatment of limb ischaemia induced chronic tissue ulcers of diabetic foot patients. Int J Clin Pract. 2012;66:384–393.
  • Ravari H, Hamidi-Almadari D, Salimifar M, et al. Treatment of non-healing wounds with autologous bone marrow cells, platelets, fibrin glue and collagen matrix. Cytotherapy. 2011;13:705–711.
  • Jain P, Perakath B, Jesudason MR, et al. The effect of autologous bone marrow-derived cells on healing chronic lower extremity wounds: results of a randomized controlled study. Ostomy Wound Manage. 2011;57:38–44.
  • Falanga V, Iwamoto S, Chartier M, et al. Autologous bone marrow–derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 2007;13:1299–1312.
  • Kirana S, Stratmann B, Lammers D, et al. Wound therapy with autologous bone marrow stem cells in diabetic patients with ischaemia-induced tissue ulcers affecting the lower limbs. Int J Clin Pract. 2007;61:690–692.
  • Badiavas EV, Ford D, Liu P, et al. Long-term bone marrow culture and its clinical potential in chronic wound healing. Wound Repair Regen. 2007;15:856–865.
  • Asai J, Takenaka H, Ichihashi K, et al. Successful treatment of diabetic gangrene with topical application of a mixture of peripheral blood mononuclear cells and basic fibroblast growth factor. J Dermatol. 2006;33:349–352.
  • Humpert PM, Bärtsch U, Konrade I, et al. Locally applied mononuclear bone marrow cells restore angiogenesis and promote wound healing in a type 2 diabetic patient. Exp Clin Endocrinol Diabetes. 2005;113:538–540.
  • Vojtassák J, Danisovic L, Kubes M, et al. Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot. Neuro Endocrinol Lett. 2006;27(Suppl 2):134–137.
  • Badiavas EV, Falanga V. Treatment of chronic wounds with bone marrow-derived cells. Arch Dermatol. 2003;139:510–516.
  • Galiano RD, Tepper OM, Pelo CR, et al. Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol. 2004;164:1935–1947.
  • Li H, Fu X, Zhang L, et al. Research of PDGF-BB gel on the wound healing of diabetic rats and its pharmacodynamics. J Surg Res. 2008;145:41–48.
  • Uchi H, Igarashi A, Urabe K, et al. Clinical efficacy of basic fibroblast growth factor (bFGF) for diabetic ulcer. Eur J Dermatol. 2009;19:461–468.
  • Gallagher KA, Liu ZJ, Xiao M, et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha J Clin Invest. 2007;117:1249–1259.
  • Barcelos LS, Duplaa C, Kr??nkel N, et al. Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ Res. 2009;104:1095–1102.
  • Amos PJ, Kapur SK, Stapor PC, et al. Human adipose-derived stromal cells accelerate diabetic wound healing: impact of cell formulation and delivery. Tissue Eng Part A. 2010;16:1–12.
  • Lee K-B, Choi J, Cho S-B, et al. Topical embryonic stem cells enhance wound healing in diabetic rats. J Orthop Res. 2011;29:1554–1562.
  • Asai J, Takenaka H, Ii M, et al. Topical application of ex vivo expanded endothelial progenitor cells promotes vascularisation and wound healing in diabetic mice. Int Wound J. 2013;10:527–533.
  • Sionkowska A. Current research on the blends of natural and synthetic polymers as new biomaterials: review. Prog Polym Sci. 2011;36:1254–1276.
  • Seetharaman S, Natesan S, Stowers RS, et al. A PEGylated fibrin-based wound dressing with antimicrobial and angiogenic activity. Acta Biomater. 2011;7:2787–2796.
  • Wang W, Lin S, Xiao Y, et al. Acceleration of diabetic wound healing with chitosan-crosslinked collagen sponge containing recombinant human acidic fibroblast growth factor in healing-impaired STZ diabetic rats. Life Sci. 2008;82:190–204.
  • Ben-Shalom N, Nevo Z, Patchornik A, et al. Novel injectable chitosan mixtures forming hydrogels. Pat Coop Treaty Appl. 2008;5.
  • Zhang H, Qadeer A, Chen W. In situ gelable interpenetrating double network hydrogel formulated from binary components: Thiolated chitosan and oxidized dextran. Biomacromolecules. 2011;12:1428–1437.
  • Lobmann R, Pittasch D, Mühlen I, et al. Autologous human keratinocytes cultured on membranes composed of benzyl ester of hyaluronic acid for grafting in nonhealing diabetic foot lesions: a pilot study. J Diabetes Complicat. 2003;17:199–204.
  • Choi DS, Kim S, Lim YM, et al. Hydrogel incorporated with chestnut honey accelerates wound healing and promotes early HO-1 protein expression in diabetic (db/db) mice. Tissue Eng Regen Med. 2012;9:36–42.
  • Shaw J, Hughes CM, Lagan KM, et al. The effect of topical phenytoin on healing in diabetic foot ulcers: a randomized controlled trial. Diabet Med. 2011;28:1154–1157.
  • Kawai K, Suzuki S, Tabata Y, et al. Accelerated tissue regeneration through incorporation of basic fibroblast growth factor-impregnated gelatin microspheres into artificial dermis. Biomaterials. 2000;21:489–499.
  • Iorio ML, Goldstein J, Adams M, et al. Functional limb salvage in the diabetic patient: the use of a collagen bilayer matrix and risk factors for amputation. Plast Reconstr Surg. 2011;127:260–267.
  • Sun G, Zhang X, Shen Y-I, et al. Dextran hydrogel scaffolds enhance angiogenic responses and promote complete skin regeneration during burn wound healing. Proc Natl Acad Sci USA. 2011;108:20976–20981.
  • Bohl Masters KS, Leibovich SJ, Belem P, et al. Effects of nitric oxide releasing poly(vinyl alcohol) hydrogel dressings on dermal wound healing in diabetic mice. Wound Repair Regen. 2002;10:286–294.
  • Choi JS, Choi SH, Yoo HS. Coaxial electrospun nanofibers for treatment of diabetic ulcers with binary release of multiple growth factors. J Mater Chem. 2011;21:5258.
  • Chen Z, Lu H. Constructing sacrificial bonds and hidden lengths for ductile graphene/polyurethane elastomers with improved strength and toughness. J Mater Chem. 2012;22:12479.
  • Yang Y, Xia T, Chen F, et al. Electrospun fibers with plasmid bFGF polyplex loadings promote skin wound healing in diabetic rats. Mol Pharm. 2012;9:48–58.
  • Li Y, Lee PI. Controlled nitric oxide delivery platform based on S-nitrosothiol conjugated interpolymer complexes for diabetic wound healing. Mol Pharm. 2010;7:254–266.
  • Dong X, Xu J, Wang W, et al. Repair effect of diabetic ulcers with recombinant human epidermal growth factor loaded by sustained-release microspheres. Sci China Ser C. 2008;51:1039–1044.
  • Merrell JG, McLaughlin SW, Tie L, et al. Curcumin-loaded poly(epsilon-caprolactone) nanofibres: diabetic wound dressing with anti-oxidant and anti-inflammatory properties. Clin Exp Pharmacol Physiol. 2009;36:1149–1156.
  • Yang Y, Xia T, Zhi W, et al. Promotion of skin regeneration in diabetic rats by electrospun core-sheath fibers loaded with basic fibroblast growth factor. Biomaterials. 2011;32:4243–4254.
  • Moura LIF, Dias AMA, Carvalho E, et al. Recent advances on the development of wound dressings for diabetic foot ulcer treatment - A review. Acta Biomater. 2013;9:7093–7114.
  • Bennett SP, Griffiths GD, Schor a M, et al. Growth factors in the treatment of diabetic foot ulcers. Br J Surg. 2003;90:133–146.
  • Yang M, Sheng L, Zhang TR, et al. Stem cell therapy for lower extremity diabetic ulcers: Where do we stand? Biomed Res Int. 2013. doi: 10.1155/2013/462179

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.