Interleukin-22 Promotes Wound Repair in Diabetes by Improving Keratinocyte Pro-Healing Functions

Journal of Investigative Dermatology

Volumn 135, Issue 11, 2015, Pages 2862-2870

  Avitabile, Simona ^a   Odorisio, Teresa ^a   Madonna, Stefania ^a   Eyerich, Stefanie ^b   Guerra, Liliana ^a   Eyerich, Kilian ^b   Zambruno, Giovanna ^a   Cavani, Andrea ^a   Cianfarani, Francesca ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 1; INTERLEUKIN 22; INVOLUCRIN; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 1; SODIUM CHLORIDE; STAT3 PROTEIN; VASCULOTROPIN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC PATIENT; ENZYME PHOSPHORYLATION; EPITHELIZATION; GRANULATION TISSUE; HISTOLOGY; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SIGNALING; KERATINOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE REPAIR; VASCULARIZATION; WOUND CLOSURE; WOUND CONTRACTION; WOUND HEALING; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; NEEDLE BIOPSY; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN ULCER; TOPICAL DRUG ADMINISTRATION; WESTERN BLOTTING;

ADMINISTRATION, TOPICAL; ANIMALS; BIOPSY, NEEDLE; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; INTERLEUKINS; KERATINOCYTES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; SKIN ULCER; STAT3 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 84947022276     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2015.278     Document Type: Article

References (44)

1. Boniface K, Bernard FX, Garcia M et al. (2005) IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol 174:3695-702
2. Brown LF, Yeo KT, Berse B et al. (1992) Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J Exp Med 176:1375-9
3. Cianfarani F, Zambruno G, Brogelli L et al. (2006) Placenta growth factor in diabetic wound healing. Am J Pathol 169:1167-82
4. Dudakov JA, Hanash AM, Jenq RR et al. (2012) Interleukin-22 drives endogenous thymic regeneration in mice. Science 336:91-5
5. Eyerich S, Eyerich K, Pennino D et al. (2009) Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 119:3573-85
6. Fadini GP, Albiero M, Menegazzo L et al. (2010) The redox enzyme p66Shc contributes to diabetes and ischemia-induced delay in cutaneous wound healing. Diabetes 59:2306-14
7. Failla CM, Odorisio T, Cianfarani F et al. (2000) Placenta growth factor is induced in human keratinocytes during wound healing. J Invest Dermatol 115:388-95
8. Frank S, Hubner G, Breier G et al. (1995) Regulation of vascular endothelial growth factor expression in cultured keratinocytes: implications for normal and impaired wound healing. J Biol Chem 270:12607-13
9. Galiano RD, Tepper OM, Pelo CR et al. (2004) Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 164:1935-47
10. Guo H, Xu BC, Yang XG et al. (2014) A high frequency of peripheral blood IL-22+ CD4+ T cCells in patients with new onset type 2 diabetes mellitus. J Clin Lab Anal; doi:10.1002/jcla.21821
11. Graiani G, Emanueli C, Desortes E et al. (2004) Nerve growth factor promotes reparative angiogenesis and inhibits endothelial apoptosis in cutaneous wounds of type 1 diabetic mice. Diabetologia 47:1047-54
12. Ikeuchi H, Kuroiwa T, Hiramatsu N et al. (2005) Expression of interleukin-22 in rheumatoid arthritis: potential role as a proinflammatory cytokine. Arthritis Rheum 52:103
13. Kira M, Sano S, Takagi S et al. (2002) STAT3 deficiency in keratinocytes leads to compromised cell migration through hyperphosphorylation of p130(cas). J Biol Chem 277:12931-6
14. Koster MI, Roop D. (2007) Mechanisms regulating epithelial stratification. Annu Rev Cell Dev Biol 23:93-113
15. Lejeune D, Dumoutier L, Constantinescu et al. (2002) Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10. J Biol Chem 277:33676-82
16. Lim YC, Bhatt MP, Kwon MH et al. (2015) Proinsulin C-peptide prevents impaired wound healing by activating angiogenesis in diabetes. J Invest Dermatol 135:269-78
17. Loots MA, Lamme EN, Zeegelaar J et al. (1998) Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J Invest Dermatol 111:850-7
18. Madonna S, Scarponi C, De Pità O et al. (2008) Suppressor of cytokine signaling 1 inhibits IFN-gamma inflammatory signaling in human keratinocytes by sustaining ERK1/2 activation. FASEB J 22:3287-97
19. McGee HM, Schmidt B, Booth CJ et al. (2013) Interleukin-22 promotes fibroblast-mediated wound repair in the skin. J Invest Derm 133:1321-9
20. Odorisio T, Schietroma C, Zaccaria ML et al. (2002) Mice overexpressing placenta growth factor exhibit increased vascularization and vessel permeability. J Cell Sci 115:2559-67
21. Pastore S, Mascia F, Mariotti F et al. (2005) ERK1/2 regulates epidermal chemokine expression and skin inflammation. J Immunol 174:5047-56
22. Pfaffl M (2001) A new mathematical model for relative quantification in real time RT-PCR. Nucleic Acids Res 29:2002-7
23. Pickert G, Neufert C, Leppkes M et al. (2009) STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 206: 1465-72
24. Pociask DA, Scheller EV, Mandalapu S et al. (2013) IL-22 is essential for lung epithelial repair following influenza infection. Am J Pathol 182:1286-96
25. Pukstad B, Ryan L, Flo T et al. (2010) Non-healing is associated with persistent stimulation of the innate immune response in chronic venous leg ulcers. J Dermatol Sci 59:115-22
26. Ren X, Hu B, Colletti IM (2010) IL-22 is involved in liver regeneration after hepatectomy. Am J Physiol Gastrointest Liver Physiol 298:G74-80
27. Romano Di Peppe S, Mangoni A, Zambruno G et al. (2002) Adenovirusmediated VEGF165 gene transfer enhances wound healing by promoting angiogenesis in CD1 diabetic mice. Gene Ther 9:271-7
28. Sano S, Itami S, Takeda K et al. (1999) Keratinocyte specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 18:4657-68
29. Schaffer M, Barbul A (1998) Lymphocyte function in wound healing and following injury. Br J Surg 85:444-60
30. Semenova E, Koegel H, Hasse S et al. (2008) Overexpression of mIGF-1 in keratinocytes improves wound healing and accelerates hair follicle formation and cycling in mice. Am J Pathol 173:1295-310
31. Sestito R, Madonna S, Scarponi C et al. (2011) STAT3-dependent effects of IL-22 in human keratinocytes are counterregulated by sirtuin 1 through a direct inhibition of STAT3 acetylation. FASEB J 25:916-27
32. Sprachikov N, Sizyakov G, Gartsbein M et al. (2001) Glucose effects on skin keratinocytes: implications for diabetes skin complications. Diabetes 50: 1627-35
33. Taylor KR, Mills RE, Costanzo AE et al. (2010) γδ T cells are reduced and rendered unresponsive by hyperglycaemia and chronic TNFα in mouse models of obesity and metabolic disease. PLoS ONE 5:e11422
34. Toulon A, Breton L, Taylor KR et al. (2009) A role for human skin-resident T cells in wound healing. J Exp Med 206:743-50
35. Trifari S, Kaplan CD, Tran EH et al. (2009) Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17,T(H)1 and T(H)2 cells. Nat Immunol 10:864-71
36. Wang X, Ota N, Manzanillo P et al. (2014) Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature 514:237-41
37. Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835-70
38. Witte E, Witte K, Warszawska K et al. (2010) Interleukin-22: a cytokine produced by T, NK and NKT cell subsets, with importance in the innate immune defense and tissue protection. Cytokine Growth Factor Rev 21: 365-79
39. Wolk K, Haugen HS, XuWet al. (2009) IL-22 and IL-20 are key mediators of the epidermal alterations in psoriasis while IL-17 and IFN-gamma are not. J Mol Med 87:523-36
40. Wolk K, Kunz S, Witte E et al. (2004) IL-22 increases the innate immunity of tissues. Immunity 21:241-54
41. Xu Q, Briggs J, Park S et al. (2005) Targeting Stat3 blocks both HIF-1 and VEGF expression induced by multiple oncogenic growth signaling pathways. Oncogene 24:5552-60
42. Zhang W, Dang E, Shi X et al. (2012) The pro-inflammatory cytokine IL-22 up-regulates keratin 17 expression in keratinocytes via STAT3 and ERK1/2. PLoS ONE 7:e4079
43. Zhao R, Tang D, Yi S et al. (2014) Elevated peripheral frequencies of Th22 cells: a novel potent participant in obesity and type 2 diabetes. PLoS ONE 9: e85770
44. Zheng Y (2007) Interleukin-22, a T(H)17 cytokine, mediates IL-23 induced dermal inflammation and achantosis. Nature 445:648-51