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BioMed Research International
Volume 2013 (2013), Article ID 754802, 9 pages
http://dx.doi.org/10.1155/2013/754802
Review Article

Abnormal Cell Responses and Role of TNF- in Impaired Diabetic Wound Healing

1School of Life Science and Biotechnology, Dalian University of Technology, Dalian 116024, China
2Department of Periodontics, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Department of Preventive Dentistry, School and Hospital of Stomatology, Peking University, Beijing 100081, China

Received 25 October 2012; Accepted 17 December 2012

Academic Editor: Jorge Berlanga Acosta

Copyright © 2013 Fanxing Xu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. M. V. Narayan, J. P. Boyle, T. J. Thompson, S. W. Sorensen, and D. F. Williamson, “Lifetime risk for diabetes mellitus in the United States,” The Journal of the American Medical Association, vol. 290, no. 14, pp. 1884–1890, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. American Diabetes Association, “Economic costs of diabetes in the U.S. in 2007,” Diabetes Care, vol. 31, no. 3, pp. 596–615, 2008.
  3. J. M. Reinke and H. Sorg, “Wound repair and regeneration,” European Surgical Research, vol. 49, no. 1, pp. 35–43, 2012. View at Publisher · View at Google Scholar
  4. A. J. Singer and R. A. F. Clark, “Cutaneous wound healing,” The New England Journal of Medicine, vol. 341, no. 10, pp. 738–746, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Valluru, C. A. Staton, M. W. Reed, et al., “Transforming growth factor-β and endoglin signaling orchestrate wound healing,” Frontiers in Physiology, vol. 2, article 89, 2011. View at Publisher · View at Google Scholar
  6. R. Blakytny and E. Jude, “The molecular biology of chronic wounds and delayed healing in diabetes,” Diabetic Medicine, vol. 23, no. 6, pp. 594–608, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Leung, “Diabetic foot ulcers—a comprehensive review,” The Surgeon, vol. 5, no. 4, pp. 219–231, 2007. View at Scopus
  8. R. G. Sibbald and K. Y. Woo, “The biology of chronic foot ulcers in persons with diabetes,” Diabetes/Metabolism Research and Reviews, vol. 24, no. 1, pp. S25–S30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. E. Tellechea A, A. Veves, and E. Carvalho, “Inflammatory and angiogenic abnormalities in diabetic wound healing: role of neuropeptides and therapeutic perspectives,” The Open Circulation and Vascular Journal, vol. 3, pp. 43–55, 2010. View at Publisher · View at Google Scholar
  10. G. C. Gurtner, S. Werner, Y. Barrandon, and M. T. Longaker, “Wound repair and regeneration,” Nature, vol. 453, no. 7193, pp. 314–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Barrientos, O. Stojadinovic, M. S. Golinko, H. Brem, and M. Tomic-Canic, “Growth factors and cytokines in wound healing,” Wound Repair and Regeneration, vol. 16, no. 5, pp. 585–601, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Wen, J. Gu, S. L. Li, M. A. Reddy, R. Natarajan, and J. L. Nadler, “Elevated glucose and diabetes promote interleukin-12 cytokine gene expression in mouse macrophages,” Endocrinology, vol. 147, no. 5, pp. 2518–2525, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Q. Lin, T. Kondo, Y. Ishida, T. Takayasu, and N. Mukaida, “Essential involvement of IL-6 in the skin wound-healing process as evidenced by delayed wound healing in IL-6-deficient mice,” Journal of Leukocyte Biology, vol. 73, no. 6, pp. 713–721, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. D. T. Graves, N. Nooh, T. Gillen et al., “IL-1 plays a critical role in oral, but not dermal, wound healing,” Journal of Immunology, vol. 167, no. 9, pp. 5316–5320, 2001. View at Scopus
  15. T. Nagaoka, Y. Kaburagi, Y. Hamaguchi et al., “Delayed wound healing in the absence of intercellular adhesion molecule-1 or L-selectin expression,” The American Journal of Pathology, vol. 157, no. 1, pp. 237–247, 2000. View at Scopus
  16. T. Yukami, M. Hasegawa, Y. Matsushita et al., “Endothelial selectins regulate skin wound healing in cooperation with L-selectin and ICAM-1,” Journal of Leukocyte Biology, vol. 82, no. 3, pp. 519–531, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Zaja-Milatovic and A. Richmond, “CXC chemokines and their receptors: a case for a significant biological role in cutaneous wound healing,” Histology and Histopathology, vol. 23, no. 11, pp. 1399–1407, 2008. View at Scopus
  18. Y. Ishida, J. L. Gao, and P. M. Murphy, “Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function,” Journal of Immunology, vol. 180, no. 1, pp. 569–579, 2008. View at Scopus
  19. C. C. Yates, D. Whaley, P. Kulasekeran et al., “Delayed and deficient dermal maturation in mice lacking the CXCR3 ELR-negative CXC chemokine receptor,” The American Journal of Pathology, vol. 171, no. 2, pp. 484–495, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. R. E. Newman, D. Yoo, M. A. LeRoux, and A. Danilkovitch-Miagkova, “Treatment of inflammatory diseases with mesenchymal stem cells,” Inflammation and Allergy—Drug Targets, vol. 8, no. 2, pp. 110–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. E. N. Arwert, E. Hoste, and F. M. Watt, “Epithelial stem cells, wound healing and cancer,” Nature Reviews Cancer, vol. 12, no. 3, pp. 170–180, 2012. View at Publisher · View at Google Scholar
  22. P. J. Critser and M. C. Yoder, “Endothelial colony-forming cell role in neoangiogenesis and tissue repair,” Current Opinion in Organ Transplantation, vol. 15, no. 1, pp. 68–72, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. O. Ochoa, F. M. Torres, and P. K. Shireman, “Chemokines and diabetic wound healing,” Vascular, vol. 15, no. 6, pp. 350–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Chatzigeorgiou, V. Harokopos, C. Mylona-Karagianni, E. Tsouvalas, V. Aidinis, and E. Kamper, “The pattern of inflammatory/anti-inflammatory cytokines and chemokines in type 1 diabetic patients over time,” Annals of Medicine, vol. 42, no. 6, pp. 426–438, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Khanna, S. Biswas, Y. Shang et al., “Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice,” PLoS ONE, vol. 5, no. 3, Article ID e9539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. B. C. Nwomeh, D. R. Yager, and I. K. Cohen, “Physiology of the chronic wound,” Clinics in Plastic Surgery, vol. 25, no. 3, pp. 341–356, 1998. View at Scopus
  27. C. Wetzler, H. Kampfer, B. Stallmeyer, J. Pfeilschifter, and S. Frank, “Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse: prolonged persistence of neutrophils and macrophages during the late phase of repair,” Journal of Investigative Dermatology, vol. 115, no. 2, pp. 245–253, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Lucas, A. Waisman, R. Ranjan et al., “Differential roles of macrophages in diverse phases of skin repair,” Journal of Immunology, vol. 184, no. 7, pp. 3964–3977, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Maruyama, J. Asai, M. Ii, T. Thorne, D. W. Losordo, and P. A. D'Amore, “Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing,” The American Journal of Pathology, vol. 170, no. 4, pp. 1178–1191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. F. O. Martinez, A. Sica, A. Mantovani, and M. Locati, “Macrophage activation and polarization,” Frontiers in Bioscience, vol. 13, no. 2, pp. 453–461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Benoit, B. Desnues, and J. L. Mege, “Macrophage polarization in bacterial infections,” Journal of Immunology, vol. 181, no. 6, pp. 3733–3739, 2008. View at Scopus
  32. X. Zhang and D. M. Mosser, “Macrophage activation by endogenous danger signals,” Journal of Pathology, vol. 214, no. 2, pp. 161–178, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Grinberg, G. Hasko, D. Wu, and S. J. Leibovich, “Suppression of PLCβ2 by endotoxin plays a role in the adenosine A 2A receptor-mediated switch of macrophages from an inflammatory to an angiogenic phenotype,” The American Journal of Pathology, vol. 175, no. 6, pp. 2439–2453, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. I. Odegaard and A. Chawla, “Mechanisms of macrophage activation in obesity-induced insulin resistance,” Nature Clinical Practice Endocrinology and Metabolism, vol. 4, no. 11, pp. 619–626, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J. E. Kanter, F. Kramer, S. Barnhart, et al., “Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 12, pp. E715–E724, 2012. View at Publisher · View at Google Scholar
  36. J. M. Daley, S. K. Brancato, A. A. Thomay, J. S. Reichner, and J. E. Albina, “The phenotype of murine wound macrophages,” Journal of Leukocyte Biology, vol. 87, no. 1, pp. 59–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. B. M. Delavary, W. M. van der Veer, M. van Egmond, F. B. Niessen, and R. H. J. Beelen, “Macrophages in skin injury and repair,” Immunobiology, vol. 216, no. 7, pp. 753–762, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. J. L. Mège, V. Mehraj, and C. Capo, “Macrophage polarization and bacterial infections,” Current Opinion in Infectious Diseases, vol. 24, no. 3, pp. 230–234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. T. J. Koh and L. A. DiPietro, “Inflammation and wound healing: the role of the macrophage,” Expert Reviews in Molecular Medicine, vol. 13, article e23, 2011. View at Publisher · View at Google Scholar
  40. X. Fu and H. Li, “Mesenchymal stem cells and skin wound repair and regeneration: possibilities and questions,” Cell and Tissue Research, vol. 335, no. 2, pp. 317–321, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Liu, Q. Yu, J. Lin, et al., “Hypoxia-inducible factor-1α is essential for hypoxia-induced mesenchymal stem cell mobilization into the peripheral blood,” Stem Cells and Development, vol. 20, no. 11, pp. 1961–1971, 2011. View at Publisher · View at Google Scholar
  42. M. Sasaki, R. Abe, Y. Fujita, S. Ando, D. Inokuma, and H. Shimizu, “Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type,” Journal of Immunology, vol. 180, no. 4, pp. 2581–2587, 2008. View at Scopus
  43. Y. Wu, L. Chen, P. G. Scott, and E. E. Tredget, “Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis,” Stem Cells, vol. 25, no. 10, pp. 2648–2659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Chen, E. E. Tredget, P. Y. G. Wu, Y. Wu, and Y. Wu, “Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing,” PLoS ONE, vol. 3, no. 4, Article ID e1886, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. N. G. Singer and A. I. Caplan, “Mesenchymal stem cells: mechanisms of inflammation,” Annual Review of Pathology, vol. 6, pp. 457–478, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Jin, X. Zhang, Y. Wu et al., “Streptozotocin-induced diabetic rat-derived bone marrow mesenchymal stem cells have impaired abilities in proliferation, paracrine, antiapoptosis, and myogenic differentiation,” Transplantation Proceedings, vol. 42, no. 7, pp. 2745–2752, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Vojtassak, L. Danisovic, M. Kubes, et al., “Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot,” Neuro Endocrinology Letters, vol. 27, supplement 2, pp. 134–137, 2006.
  48. Y. R. Kuo, C. T. Wang, J. T. Cheng, et al., “Bone marrow-derived mesenchymal stem cells enhanced diabetic wound healing through recruitment of tissue regeneration in a rat model of streptozotocin-induced diabetes,” Plastic and Reconstructive Surgery, vol. 128, no. 4, pp. 872–880, 2011. View at Publisher · View at Google Scholar
  49. C. Roh and S. Lyle, “Cutaneous stem cells and wound healing,” Pediatric Research, vol. 59, no. 4, part 2, pp. 100R–103R, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Lau, R. Paus, S. Tiede, P. Day, and A. Bayat, “Exploring the role of stem cells in cutaneous wound healing,” Experimental Dermatology, vol. 18, no. 11, pp. 921–933, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Werner and R. Grose, “Regulation of wound healing by growth factors and cytokines,” Physiological Reviews, vol. 83, no. 3, pp. 835–870, 2003. View at Scopus
  52. P. Martin, “Wound healing—aiming for perfect skin regeneration,” Science, vol. 276, no. 5309, pp. 75–81, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Galkowska, W. L. Olszewski, U. Wojewodzka, J. Mijal, and E. Filipiuk, “Expression of apoptosis-and cell cycle-related proteins in epidermis of venous leg and diabetic foot ulcers,” Surgery, vol. 134, no. 2, pp. 213–220, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Galkowska, U. Wojewodzka, and W. L. Olszewski, “Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers,” Wound Repair and Regeneration, vol. 14, no. 5, pp. 558–565, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. M. L. Usui, J. N. Mansbridge, W. G. Carter, M. Fujita, and J. E. Olerud, “Keratinocyte migration, proliferation, and differentiation in chronic ulcers from patients with diabetes and normal wounds,” Journal of Histochemistry and Cytochemistry, vol. 56, no. 7, pp. 687–696, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. C. C. E. Lan, I. H. Liu, A. H. Fang, C. H. Wen, and C. S. Wu, “Hyperglycaemic conditions decrease cultured keratinocyte mobility: implications for impaired wound healing in patients with diabetes,” British Journal of Dermatology, vol. 159, no. 5, pp. 1103–1115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Werner, T. Krieg, and H. Smola, “Keratinocyte-fibroblast interactions in wound healing,” Journal of Investigative Dermatology, vol. 127, no. 5, pp. 998–1008, 2007. View at Publisher · View at Google Scholar · View at Scopus