Role of wound macrophages in skin flap loss or survival in an experimental diabetes model

British Journal of Surgery

Volumn 97, Issue 9, 2010, Pages 1437-1451

  Schurmann C ^a   Seitz, O ^a,b   Sader, R ^b   Pfeilschifter, J ^b   Goren, I ^a   Frank, S ^a  

^a Pharmazentrum Frankfurt   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; RIBONUCLEASE; RNA;

ANIMAL; ARTICLE; BIOPSY; C57BL MOUSE; DIABETES MELLITUS; FEMALE; GRAFT SURVIVAL; IMMUNOLOGICAL PROCEDURES; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PLASTIC SURGERY; POLYMERASE CHAIN REACTION;

ANIMALS; BIOPSY; CHEMOKINES; DIABETES MELLITUS; FEMALE; GRAFT SURVIVAL; IMMUNOLOGIC TESTS; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; RIBONUCLEASES; RNA; SURGICAL FLAPS;

EID: 77956414150     PISSN: 00071323     EISSN: 13652168     Source Type: Journal    
DOI: 10.1002/bjs.7123     Document Type: Article

References (50)

1. Martin P. Wound healing - aiming for perfect skin regeneration. Science 1997; 276: 75-81.
2. Singer AJ, Clark RAF. Cutaneous wound healing. N Engl J Med 1999; 341: 738-746.
3. Eming SA, Krieg T, Davidson JM. Inflammation in wound repair: molecular and cellular mechanisms. J Invest Dermatol 2007; 127: 514-525.
4. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003; 83: 835-870.
5. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3: 23-35.
6. Rosner K, Ross C, Karlsmark T, Petersen AA, Gottrup F, Vejlsgaard GL. Immunohistochemical characterization of the cutaneous cellular infiltrate in different areas of chronic leg ulcers. APMIS 1995; 103: 293-299.
7. Loots MA, Lamme EN, Zeegelaar J, Mekkes JR, Bos JD, Middelkoop E. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J Invest Dermatol 1998; 111: 850-857.
8. Wetzler C, Kämpfer H, Stallmeyer B, Pfeilschifter J, Frank S. 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. J Invest Dermatol2000; 115: 245-253.
9. Goren I, Kämpfer H, Podda M, Pfeilschifter J, Frank S. Leptin and wound inflammation in diabetic ob/ob mice: differential regulation of neutrophil and macrophage influx and a potential role for the scab as a sink for inflammatory cells and mediators. Diabetes 2003; 52: 2821-2832.
10. Goren I, Müller E, Schiefelbein D, Christen U, Pfeilschifter J, Mühl H. Systemic anti-TNFa treatment restores diabetes-impaired skin repair in ob/ob mice by inactivation of macrophages. J Invest Dermatol 2007; 127: 2259-2267.
11. Goren I, Müller E, Pfeilschifter J, Frank S. Severely impaired insulin signaling in chronic wounds of diabetic ob/ob mice: a potential role of tumor necrosis factor-alpha. Am J Pathol 2006; 168: 765-777.
12. Schürmann C, Seitz O, Klein C, Sader R, Pfeilschifter J, Mühl H et al. Tight spatial and temporal control in dynamic basal to distal migration of epithelial inflammatory responses and infiltration of cytoprotective macrophages determine healing skin flap transplants in mice. Ann Surg 2009; 249: 519-534.
13. Daniel RK, Kerrigan CL. Principles and physiology of skin flap surgery. In: Plastic Surgery, McCarthy JG (ed.). Saunders: Philadelphia, 1990; 275-328.
14. Grabb WC. Techniques in plastic surgery. In Plastic Surgery, Grabb WC, Smith JW (eds). Little, Brown: Boston, 1986; 3-74.
15. Nakatsuka T, Harii K, Asato H, Takushima A, Ebihara S, Kimata Y et al. Analytic review of 2372 free flap transfers for head and neck reconstruction following cancer resection. J Reconstr Microsurg 2003; 19: 363-368.
16. Wei FC, Demirkan F, Chen HC, Chuang DC, Chen SH, Lin CH et al. The outcome of failed free flaps in head and neck and extremity reconstruction: what is next in the reconstructive ladder? Plast Reconstr Surg 2001; 108: 1154-1160.
17. Shah JP, Haribhakti V, Loree TR, Sutaria P. Complications of the pectoralis major myocutaneous flap in head and neck reconstruction. Am J Surg 1990; 160: 352-355.
18. Myers MB, Cherry G. Causes of necrosis in pedicle flaps. Plast Reconstr Surg 1968; 42: 43-50.
19. Kerrigan CL. Skin flap failure: pathophysiology. Plast Reconstr Surg 1983; 72: 766-777.
20. Scalise A, Tucci MG, Lucarini G, Giantomassi F, Orlando F, Pierangeli M et al. Local rh-VEGF administration enhances skin flap survival more than other types of rh-VEGF administration: a clinical, morphological and immunohistochemica study. Exp Dermatol 2004; 13: 682-690.
21. Michlits W, Mittermayr R, Schäfer R, Redl H, Aharinejad S. Fibrin-embedded administration of VEGF plasmid enhances skin flap survival. Wound Repair Regen 2007; 15: 360-367.
22. Huang N, Khan A, Ashrafpour H, Neligan PC, Forrest CR, Kontos CD et al. Efficacy and mechanism of adenovirus-mediated VEGF-165 gene therapy for augmentation of skin flap viability. Am J Physiol Heart Circ Physiol 2006; 291: H127-H137.
23. Zheng Y, Yi C, Xia W, Ding T, Zhou Z, Han Y et al. Mesenchymal stem cells transduced by vascular endothelial growth factor gene for ischemic random skin flaps. Plast Reconstr Surg 2008; 121: 59-69.
24. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8: 958-969.
25. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009; 27: 451-483.
26. Coleman DL. Obese and diabetes: two mutant genes causing diabetes-obesity syndromes in mice. Diabetologia 1978; 14: 141-148.
27. Van Rooijen N, Bakker J, Sanders A. Transient suppression of macrophage functions by liposome-encapsulated drugs. Trends Bioteclmol 1997; 15: 178-185.
28. Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods 1989; 124: 1-6.
29. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 1994; 372: 425-432.
30. Frank S, Stallmeyer B, Kämpfer H, Kolb N, Pfeilschifter J. Nitric oxide triggers enhanced induction of vascular endothelial growth factor expression in cultured keratinocytes (HaCaT) and during cutaneous wound repair. FASEB J 1999; 13: 2002-2014.
31. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159.
32. Frank S, Stallmeyer B, Kämpfer H, Kolb N, Pfeilschifter J. Leptin enhances wound re-epithelialization and constitutes a direct function of leptin in skin repair. J Clin Invest 2000; 106: 501-509.
33. Viola A, Luster AD. Chemokines and their receptors: drug targets in immunity and inflammation. Annu Rev Pharmacol Toxicol 2008; 48: 171-197.
34. Tepper RI, Coffman RL, Leder P. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 1992; 257: 548-551.
35. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 2008; 83: 64-70.
36. Austyn JM, Gordon S. F4/80, monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 1981;11:805-815.
37. Hübner G, Brauchle M, Smola H, Madlener M, Fässler R, Werner S. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine 1996; 8: 548-556.
38. Claassen I, van Rooijen N, Claassen E. A new method for removal of mononuclear phagocytes from heterogeneous cell populations in vitro, using the liposome-mediated macrophage 'suicide' technique. J Immunol Methods 1990; 134: 153-161.
39. Martin P, Leibovich SL. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 2005; 15: 599-607.
40. McFarlane RM, DeYoung G, Henry RA. The design of a pedicle flap in the rat to study necrosis and its prevention. Plast Reconstr Surg 1965; 35: 177-182.
41. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 2004; 56: 549-580.
42. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Cirulation 2006; 113: 1888-1904.
43. Engelhardt E, Toksoy A, Goebeler M, Debus S, Bröcker EB, Gillitzer R. Chemokines IL-8, GROalpha, MCP-1, IP-10, and MIG are sequentially and differentially expressed during phase-specific infiltration of leukocyte subsets in human wound healing. Am JPathol 1998; 153: 1849-1860.
44. Hayden MS, Ghosh S. Signaling to NF-kappa.B. Genes Dev 2004; 18: 2195-2224.
45. D'Acquisto F, Iuvone T, Rombolà L, Sautebin L, Di Rosa M, Carnuccio R. Involvement of NF-kappaB in the regulation of cycIooxygenase-2 protein expression in LPS-stimulated J774 macrophages. FEBS Lett 1997; 418: 175-178.
46. Xie Q, Nathan C. The high-output nitric oxide pathway: role and regulation. J Leukoc Biol 1994; 56: 576-582.
47. Qian Q, Jutila MA, Van Rooijen N, Cutler JE. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J Immunol 1994; 152: 5000-5008.
48. Wang H, Peters T, Kess D, Sindrilaru A, Oreshkova T, Van Rooijen N et al. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J Clin Invest 2006; 116: 2105-2114.
49. Stratis A, Pasparakis M, Rupee RA, Markur D, Hartmann K, Scharffetter-Kochanek K et al. Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J Clin Invest 2006; 116: 2094-2104.
50. (-/-) mice due to a decrease in TGF-betal and myofibroblast differentiation. EMBO J 2005; 24: 3400-3410.