Anti-fibrotic actions of interleukin-10 against hypertrophic scarring by activation of PI3K/AKT and STAT3 signaling pathways in scar-forming fibroblasts

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Shi, Jihong ^a   Li, Jun ^a   Guan, Hao ^a   Cai, Weixia ^a   Bai, Xiaozhi ^a   Fang, Xiaobing ^a   Hu, Xiaolong ^a   Wang, Yaojun ^a   Wang, Hongtao ^a   Zheng, Zhao ^a   Su, Linlin ^a   Hu, Dahai ^a   Zhu, Xiongxiang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CYTOKINE RECEPTOR ANTAGONIST; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 10 RECEPTOR ANTAGONIST; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANTIFIBROTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTROPHIC SCAR; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOLECULAR INTERACTION; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; UPREGULATION; WESTERN BLOTTING; CICATRIX, HYPERTROPHIC; DRUG EFFECTS; FIBROBLAST; FIBROSIS; METABOLISM; PATHOLOGY; SKIN;

CICATRIX, HYPERTROPHIC; ENZYME ACTIVATION; FIBROBLASTS; FIBROSIS; HUMANS; INTERLEUKIN-10; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, INTERLEUKIN-10; SIGNAL TRANSDUCTION; SKIN; STAT3 TRANSCRIPTION FACTOR;

EID: 84902322296     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098228     Document Type: Article

References (43)

1. van der Veer WM, Bloemen MC, Ulrich MM, Molema G, van Zuijlen PP, et al. (2009) Potential cellular and molecular causes of hypertrophic scar formation. Burns 35: 15-29.
2. Kircik LH (2013) Comparative study of the efficacy and tolerability of a unique topical scar product vs white petrolatum following shave biopsies. J Drugs Dermatol 12: 86-90.
3. Bayat A, McGrouther DA, Ferguson MW (2003) Skin scarring. BMJ 326: 88-92. (Pubitemid 36092292)
4. Brown BC, McKenna SP, Siddhi K, McGrouther DA, Bayat A (2008) The hidden cost of skin scars: quality of life after skin scarring. J Plast Reconst Aesthet Surg 61: 1049-1058.
5. Aarabi S, Longaker MT, Gurtner GC (2007) Hypertrophic Scar Formation Following Burns and Trauma: New Approaches to Treatment. PloS Med 4: e234.
6. Shi JH, Guan H, Shi S, Cai WX, Bai XZ, et al. (2013) Protection against TGF-β1-induced fibrosis effects of IL-10 on dermal fibroblasts and its potential therapeutics for the reduction of skin scarring. Arch Dermatol Res 305: 341-352.
7. Gauglitz GG, Korting HC, Pavicic T, Ruzicka T, Jeschke MG (2011) Hypertrophic scarring and keloids: pathomechanisms and current and emerging treatment strategies. Mol Med 17: 113-125.
8. Saito M, Yamazaki M, Maeda T, Matsumura H, Setoguchi Y, et al. (2012) Pirfenidone suppresses keloid fibroblast-embedded collagen gel contraction. Arch Dermatol Res 304: 217-222.
9. Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170: 2081-2095.
10. Moore KW, O'Garra A, de Waal Malefyt R, Vieira P, Mosmann TR (1993) Interleukin-10. Annu Rev Immunol 11: 165-190. (Pubitemid 23115005)
11. Signer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341: 738-746.
12. Weiss E, Mamelak AJ, La Morgia S, Wang B, Feliciani C, et al. (2004) The role of interleukin 10 in the pathogenesis and potential treatment of skin diseases. J Am Acad Dermatol 50: 657-675.
13. Peranteau WH, Zhang L, Muvarak N, Badillo AT, Radu A, et al. (2008) IL-10 overexpression decrease inflammatoly mediators and promotes regenerative healing in an adult model of scar formation. J Invest Dermatol 128: 1852-1860. (Pubitemid 351847365)
14. Liechty KW, Kim HB, Adzick NS, Crombleholme TM (2000) Fetal wound repair results in scar formation in interleukin-10-deficient mice in a syngeneic murine model of scarless fetal wound repair. J Pediatr Surg 35: 866-872.
15. Nakagome K, Dohi M, Okunishi K, Tanaka R, Miyazaki J, et al. (2006) In vivo IL-10 gene delivery attenuates blemycin induced pulmonary fibrosis by inhibiting the production and activation of TGF-β in the lung. Thorax 61: 886-894. (Pubitemid 44570310)
16. Occleston NL, O'Kane S, Goldspink N, Ferguson MWJ (2008) New therapeutics for the prevention and reduction of scarring. Drug Discovery Today 13: 973-981.
17. Mrowietz U, Seifert O (2009) Keloid scarring: new treatments ahead. Actas Dermosifiliogr 100: 75-83.
18. Seifert O, Mrowietz U (2009) Keloid scarring: bench and bedside. Arch Dermatol Res 301: 259-272.
19. Yamamoto T, Eckes B, Krieg T (2001) Effect of interleukin-10 on the gene expression of type I collagen, fibronectin, and decorin in human skin fibroblasts: differential regulation by transforming growth factor-beta and monocyte chemoattractant protein-1. Biochem Biophys Res Commun 281: 200-205. (Pubitemid 32924419)
20. Reitamo S, Remitz A, Tamai K, Uitto J (1994) Interleukin-10 modulates type I collagen and matrix metalloprotease gene expression in cultured human skin fibroblasts. J Clin Invest 94: 2489-2492. (Pubitemid 24379626)
21. Yuan W, Varga J (2001) Transforming growth factor-beta repression of matrix metalloproteinase-1 in dermal fibroblasts involves Smad3. J Biol Chem 276: 38502-38510.
22. Arai T, Abe K, Matsuoka H, Yoshida M, Mori M, et al. (2000) Introduction of the interleukin-10 gene into mice inhibited bleomycin-induced lung injury in vivo. Am J Physiol Lung Cell Mol Physiol 278: L914-922. (Pubitemid 30351046)
23. Bogdan C, Vodovotz Y, Nathan C (1991) Macrophage deactivation by interleukin 10. J Exp Med 174: 1549-1555.
24. Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, et al. (2010) Biology of interleukin-10. Cytokine & Growth Factor Reviews 21: 331-344.
25. Glocker EO, Kotlarz D, Klein C, Shah N, Grimbacher B (2011) IL-10 and IL-10 receptor defects in humans. Ann N Y Acad Sci 1246: 102-107.
26. Niessen FB, Spauwen PH, Schalkwijk J, Kon M (1999) On the nature of hypertrophic scars and keloids: a review. Plast Reconstr Surg 104: 1435-1458. (Pubitemid 29466295)
27. Sidgwick GP, Bayat A (2012) Extracellular matrix molecules implicated in hypertrophic and keloid scarring. J Eur Acad Dermatol Venereol 26: 141-152.
28. Zhang ZF, Zhang YG, Hu DH, Shi JH, Liu JQ, et al. (2011) Smad interacting protein 1 as a regulator of skin fibrosis in pathological scars. Burns 37: 665-672.
29. Campaner AB, Ferreira LM, Gragnani A, Bruder JM, Cusick JL, et al. (2006) Upregulation of TGF-β1 expression may be necessary but is not sufficient for excessive scarring. J Invest Dermatol 126: 1168-1176.
30. Wolfram D, Tzankov A, Pülzl P, Piza-Katzer H (2009) Hypertrophic scars and keloids-a review of their pathophysiology, risk factors, and therapeutic management. Dermatol Surg 35: 171-181.
31. Ong CT, Khoo YT, Mukhopadhyay A, Do DV, Lim IJ, et al. (2007) mTOR as a potential therapeutic target for treatment of keloids and excessive scars. Exp Dermatol 16: 394-404. (Pubitemid 46585367)
32. Diao JS, Xia WS, Yi CG, Wang YM, Li B, et al. (2011) Trichostatin A inhibits collagen synthesis and induces apoptosis in keloid fibroblasts. Arch Dermatol Res 303: 573-580.
33. Hsu YC, Chen MJ, Yu YM, Ko SY, Chang CC (2010) Suppression of TGF-β1/SMAD pathway and extracellular matrix production in primary keloid fibroblasts by curcuminoids: its potential therapeutic use in the chemoprevention of keloid. Arch Dermatol Res 302: 717-724.
34. Tang B, Zhu B, Liang Y, Bi L, Hu Z, et al. (2011) Asiaticoside suppresses collagen expression and TGF-β/Smad signaling through inducing Smad7 and inhibiting TGF-βRI and TGF-βRII in keloid fibroblasts. Arch Dermatol Res 303: 563-572.
35. Shi JH, Hu DH, Zhang ZF, Bai XZ, Wang HT, et al. (2012) Reduced expression of microtubule-associated protein 1 light chain 3 in hypertrophic scars. Arch Dermatol Res 304: 209-215.
36. Hinz B (2007) Formation and function of the myofibroblast during tissue repair. J Invest Demmatol 127: 526-537.
37. Hinz B (2010) The myofibroblast: paradigm for a mechanically active cell. J Biomech 43: 146-155.
38. Zhang H, Ran X, Hu CL, Qin LP, Lu Y, et al. (2012) Therapeutic effects of liposome-enveloped Ligusticum chuanxiong essential oil on hypertrophic scars in the rabbit ear model. PLoS One 7: e31157.
39. Hu X, Wang H, Liu J, Fang X, Tao K, et al. (2013) The role of ERK and JNK signaling in connective tissue growth factor induced extracellular matrix protein production and scar formation. Arch Dermatol Res 305: 433-445.
40. Franke TF, Kaplan DR, Cantley LC (1997) pI3K: downstream AKTion block apoptosis. Cell 88: 435-437. (Pubitemid 27154408)
41. Franke TF (2008) Intracellular signaling by AKT: bound to be specific. Sci Signal 1: pe29.
42. Park HJ, Lee SJ, Kim SH, Han J, Bae J, et al. (2011) IL-10 inhibits the starvation induced autophagy in macrophages via class I phosphatidylinositol 3-kinase (PI3K) pathway. Mol Immunol 48: 720-727.
43. Donnelly RP, Dickensheets H, Finbloom DS (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 19: 563-573. (Pubitemid 29331308)