RESEARCH PROGRESS ON ROLE OF microRNA IN HEALING OF DIABETIC WOUND_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

SUNShuyao ,  WANGChun ,  RANXingwu

Department of Endocrinology and Metabolism, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

WANGChun, Email: snoopywc@163.com; RANXingwu, Email: ranxingwu@163.com

Keywords：

microRNA; Diabetes; Wound healing; Inflammatory reaction; Angiogenesis

DOI：

10.7507/1002-1892.20140308

Video：

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Objective To review the regulatory effect of microRNA (miRNA) in wound heal ing, which abnormal expression associates with diabetes. Methods The literature on miRNA associating with wound heal ing was reviewed and summarized. Results miRNA plays a key role in wound heal ing, including regulating inflammation, angiogenesis, granulation tissue formation, and re-epithel ization. Conclusion Abnormal expression of miRNA may be related to delayed healing of the diabetic wound, but further research is needed to confirm it.

Citation： SUNShuyao, WANGChun, RANXingwu. RESEARCH PROGRESS ON ROLE OF microRNA IN HEALING OF DIABETIC WOUND. Chinese Journal of Reparative and Reconstructive Surgery, 2014, 28(11): 1431-1434. doi: 10.7507/1002-1892.20140308 Copy

1.	Shilo S, Roy S, Khanna S, et al. MicroRNA in cutaneous wound healing: a new paradigm. DNA Cell Biol, 2007, 26(4):227-237.
2.	Bartel DP. MicroRNAs:genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2):281-297.
3.	Cheng AM, Byrom MW, Shelton J, et al. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res, 2005, 33(4):1290-1297.
4.	Chen CZ, Li L, Lodish HF, et al. MicroRNAs modulate hematopoietic lineage differentiation. Science, 2004, 303(5654):83-86.
5.	Garzon R, Fabbri M, Cimmino A, et al. MicroRNA expression and function in cancer. Trends Mol Med, 2006, 12(12):580-587.
6.	Pauley KM, Chan EK. MicroRNAs and their emerging roles in immunology. Ann N Y Acad Sci, 2008, 1143:226-239.
7.	Banerjee J, Sen CK. MicroRNAs in skin and wound healing. Methods Mol Biol, 2013, 936:343-356.
8.	Bostjancic E, Glavac D. Importance of microRNAs in skin morphogenesis and diseases. Acta Dermatovenerol Alp Panonica Adriat, 2008, 17(3):95-102.
9.	Wetzler C, Kämpfer H, Stallmeyer B, et al. 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 Dermatol, 2000, 115(2):245-253.
10.	Stanczyk J, Pedriol i DM, Brentano F, et al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum, 2008, 58(4):1001-1009.
11.	Tang Y, Luo X, Cui H, et al. MicroRNA-146A contributes to abnormal activation of the type Ⅰ interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum, 2009, 60(4):1065-1075.
12.	Yamasaki K, Nakasa T, Miyaki S, et al. Expression of microRNA-146a in osteoarthritis cartilage. Arthritis Rheum, 2009, 60(4):1035-1041.
13.	Hurst DR, Edmonds MD, Scott GK, et al. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res, 2009, 69(4):1279-1283.
14.	Taganov KD, Boldin MP, Chang KJ, et al. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signal ing proteins of innate immune responses. Proc Natl Acad Sci U S A, 2006, 103(33):12481-12486.
15.	Bhaumik D, Scott GK, Schokrpur S, et al. Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene, 2008, 27(42):5643-5647.
16.	Xu J, Wu W, Zhang L, et al. The role of microRNA-146a in the pathogenesis of the diabetic wound-healing impairment:correction with mesenchymal stem cell treatment. Diabetes, 2012, 61(11):2906-2912.
17.	Nahid MA, Satoh M, Chan EK. Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signal ing. J Immunol, 2011, 186(3):1723-1734.
18.	熊玮, 董少红, 袁建辉, 等. MiRNA-146a通过NF-κB依赖的途径促进血管平滑肌细胞增殖.南方医科大学学报, 2012, 32(2):270-273.
19.	McCoy CE, Sheedy FJ, Qualls JE, et al. IL-10 inhibits miR-155 induction by toll-l ike receptors. J Biol Chem, 2010, 285(27):20492-20498.
20.	Kishore R, Verma SK, Mackie AR, et al. Bone marrow progenitor cell therapy-mediated paracrine regulation of cardiac miRNA-155 modulates fibrotic response in diabetic hearts. PLoS One, 2013, 8(4):e60161.
21.	Villeneuve LM, Kato M, Reddy MA, et al. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes, 2010, 59(11):2904-2915.
22.	Til i E, Michaille JJ, Cimino A, et al. Modulation of miR-155 and miR-125b levels following l i popolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol, 2007, 179(8):5082-5089.
23.	Yang WJ, Yang DD, Na S, et al. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem, 2005, 280(10):9330-9335.
24.	Wang S, Aurora AB, Johnson BA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell, 2008, 15(2):261-271.
25.	Zampetaki A, Kiechl S, Drozdov I, et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res, 2012, 107(6):810-817.
26.	Fasanaro P, D'Alessandra Y, Di Stefano V, et al. MicroRNA-210 modulates endothel ial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem, 2008, 283(23):15878-15883.
27.	Giannakakis A, Sandaltzopoulos R, Greshock J, et al. miR-210 l inks hypoxia with cell cycle regulation and is deleted in human epithel ial ovarian cancer. Cancer Biol Ther, 2008, 7(2):255-264.
28.	Camps C, Buffa FM, Colella S, et al. hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res, 2008, 14(5):1340-1348.
29.	Huang X, Ding L, Bennewith KL, et al. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell, 2009, 35(6):856-867.
30.	Biswas S, Roy S, Banerjee J, et al. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc Natl Acad Sci U S A, 2010, 107(15): 6976-6981.
31.	Long J, Wang Y, Wang W, et al. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem, 2010, 285(30):23457-23465.
32.	Roy S, Sen CK. miRNA in wound inflammation and angiogenesis. Microcirculation, 2012, 19(3):224-232.
33.	Wang XH, Qian RZ, Zhang W, et al. MicroRNA-320 expression in myocardial microvascular endothel ial cells and its relationship with insul in-l ike growth factor-1 in type 2 diabetic rats. Clin Exp Pharmacol Physiol, 2009, 36(2):181-188.
34.	Caporali A, Meloni M, Völlenkle C, et al. Deregulation of microRNA-503 contributes to diabetes mell itus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation, 2011, 123(3):282-291.
35.	Matsui J, Wakabayashi T, Asada M, et al. Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J Biol Chem, 2004, 279(18): 18600-18607.
36.	Li Y, Song YH, Li F, et al. MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun, 2009, 381(1):81-83.
37.	Togliatto G, Trombetta A, Dentelli P, et al. MIR221/MIR222-driven post-transcri ptional regulation of P27KIP1 and P57KIP2 is crucial for high-glucose-and AGE-mediated vascular cell damage. Diabetologia, 2011, 54(7):1930-1940.
38.	McArthur K, Feng B, Wu Y, et al. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes, 2011, 60(4):1314-1323.
39.	Gabriely G, Wurdinger T, Kesari S, et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol, 2008, 28(17):5369-5380.
40.	Cottonham CL, Kaneko S, Xu L. miR-21 and miR-31 converge on TIAM1 to regulate migration and invasion of colon carcinom a cells. J Biol Chem, 2010, 285(46):35293-35302.
41.	Madhyastha R, Madhyastha H, Nakajima Y, et al. MicroRNA signature in diabetic wound healing:promotive role of miR-21 in fibroblast migration. Int Wound J, 2012, 9(4):355-361.
42.	Yang X, Wang J, Guo SL, et al. miR-21 promotes keratinocyte migration and re-epithel ial ization during wound heal ing. Int J Biol Sci, 2011, 7(5):685-690.
43.	刘显庆. MicroRNA-21在高糖诱导血管内皮细胞凋亡中的表达及功能.长沙:中南大学, 2010.
44.	Khanna S, Biswas S, Shang Y, et al. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One, 2010, 5(3):e9539.
45.	Sheedy FJ, Palsson-McDermott E, Hennessy EJ, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol, 2010, 11(2):141-147.
46.	Fleenor DL, Shepard AR, Hellberg PE, et al. TGFbeta2-induced changes in human trabecular meshwork:implications for intraocular pressure. Invest Ophthalmol Vis Sci, 2006, 47(1):226-234.
47.	Maurer B, Stanczyk J, Jüngel A, et al. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum, 2010, 62(6): 1733-1743.
48.	van Rooij E, Sutherland LB, Thatcher JE, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A, 2008, 105(35):13027-13032.
49.	He A, Zhu L, Gupta N, et al. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insul in resistance in 3T3-L1 adi pocytes. Mol Endocrinol, 2007, 21(11):2785-2794.

1. Shilo S, Roy S, Khanna S, et al. MicroRNA in cutaneous wound healing: a new paradigm. DNA Cell Biol, 2007, 26(4):227-237.
2. Bartel DP. MicroRNAs:genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2):281-297.
3. Cheng AM, Byrom MW, Shelton J, et al. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res, 2005, 33(4):1290-1297.
4. Chen CZ, Li L, Lodish HF, et al. MicroRNAs modulate hematopoietic lineage differentiation. Science, 2004, 303(5654):83-86.
5. Garzon R, Fabbri M, Cimmino A, et al. MicroRNA expression and function in cancer. Trends Mol Med, 2006, 12(12):580-587.
6. Pauley KM, Chan EK. MicroRNAs and their emerging roles in immunology. Ann N Y Acad Sci, 2008, 1143:226-239.
7. Banerjee J, Sen CK. MicroRNAs in skin and wound healing. Methods Mol Biol, 2013, 936:343-356.
8. Bostjancic E, Glavac D. Importance of microRNAs in skin morphogenesis and diseases. Acta Dermatovenerol Alp Panonica Adriat, 2008, 17(3):95-102.
9. Wetzler C, Kämpfer H, Stallmeyer B, et al. 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 Dermatol, 2000, 115(2):245-253.
10. Stanczyk J, Pedriol i DM, Brentano F, et al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum, 2008, 58(4):1001-1009.
11. Tang Y, Luo X, Cui H, et al. MicroRNA-146A contributes to abnormal activation of the type Ⅰ interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum, 2009, 60(4):1065-1075.
12. Yamasaki K, Nakasa T, Miyaki S, et al. Expression of microRNA-146a in osteoarthritis cartilage. Arthritis Rheum, 2009, 60(4):1035-1041.
13. Hurst DR, Edmonds MD, Scott GK, et al. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res, 2009, 69(4):1279-1283.
14. Taganov KD, Boldin MP, Chang KJ, et al. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signal ing proteins of innate immune responses. Proc Natl Acad Sci U S A, 2006, 103(33):12481-12486.
15. Bhaumik D, Scott GK, Schokrpur S, et al. Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene, 2008, 27(42):5643-5647.
16. Xu J, Wu W, Zhang L, et al. The role of microRNA-146a in the pathogenesis of the diabetic wound-healing impairment:correction with mesenchymal stem cell treatment. Diabetes, 2012, 61(11):2906-2912.
17. Nahid MA, Satoh M, Chan EK. Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signal ing. J Immunol, 2011, 186(3):1723-1734.
18. 熊玮, 董少红, 袁建辉, 等. MiRNA-146a通过NF-κB依赖的途径促进血管平滑肌细胞增殖.南方医科大学学报, 2012, 32(2):270-273.
19. McCoy CE, Sheedy FJ, Qualls JE, et al. IL-10 inhibits miR-155 induction by toll-l ike receptors. J Biol Chem, 2010, 285(27):20492-20498.
20. Kishore R, Verma SK, Mackie AR, et al. Bone marrow progenitor cell therapy-mediated paracrine regulation of cardiac miRNA-155 modulates fibrotic response in diabetic hearts. PLoS One, 2013, 8(4):e60161.
21. Villeneuve LM, Kato M, Reddy MA, et al. Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes, 2010, 59(11):2904-2915.
22. Til i E, Michaille JJ, Cimino A, et al. Modulation of miR-155 and miR-125b levels following l i popolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol, 2007, 179(8):5082-5089.
23. Yang WJ, Yang DD, Na S, et al. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem, 2005, 280(10):9330-9335.
24. Wang S, Aurora AB, Johnson BA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell, 2008, 15(2):261-271.
25. Zampetaki A, Kiechl S, Drozdov I, et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res, 2012, 107(6):810-817.
26. Fasanaro P, D'Alessandra Y, Di Stefano V, et al. MicroRNA-210 modulates endothel ial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem, 2008, 283(23):15878-15883.
27. Giannakakis A, Sandaltzopoulos R, Greshock J, et al. miR-210 l inks hypoxia with cell cycle regulation and is deleted in human epithel ial ovarian cancer. Cancer Biol Ther, 2008, 7(2):255-264.
28. Camps C, Buffa FM, Colella S, et al. hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res, 2008, 14(5):1340-1348.
29. Huang X, Ding L, Bennewith KL, et al. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell, 2009, 35(6):856-867.
30. Biswas S, Roy S, Banerjee J, et al. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc Natl Acad Sci U S A, 2010, 107(15): 6976-6981.
31. Long J, Wang Y, Wang W, et al. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem, 2010, 285(30):23457-23465.
32. Roy S, Sen CK. miRNA in wound inflammation and angiogenesis. Microcirculation, 2012, 19(3):224-232.
33. Wang XH, Qian RZ, Zhang W, et al. MicroRNA-320 expression in myocardial microvascular endothel ial cells and its relationship with insul in-l ike growth factor-1 in type 2 diabetic rats. Clin Exp Pharmacol Physiol, 2009, 36(2):181-188.
34. Caporali A, Meloni M, Völlenkle C, et al. Deregulation of microRNA-503 contributes to diabetes mell itus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation, 2011, 123(3):282-291.
35. Matsui J, Wakabayashi T, Asada M, et al. Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J Biol Chem, 2004, 279(18): 18600-18607.
36. Li Y, Song YH, Li F, et al. MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun, 2009, 381(1):81-83.
37. Togliatto G, Trombetta A, Dentelli P, et al. MIR221/MIR222-driven post-transcri ptional regulation of P27KIP1 and P57KIP2 is crucial for high-glucose-and AGE-mediated vascular cell damage. Diabetologia, 2011, 54(7):1930-1940.
38. McArthur K, Feng B, Wu Y, et al. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes, 2011, 60(4):1314-1323.
39. Gabriely G, Wurdinger T, Kesari S, et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol, 2008, 28(17):5369-5380.
40. Cottonham CL, Kaneko S, Xu L. miR-21 and miR-31 converge on TIAM1 to regulate migration and invasion of colon carcinom a cells. J Biol Chem, 2010, 285(46):35293-35302.
41. Madhyastha R, Madhyastha H, Nakajima Y, et al. MicroRNA signature in diabetic wound healing:promotive role of miR-21 in fibroblast migration. Int Wound J, 2012, 9(4):355-361.
42. Yang X, Wang J, Guo SL, et al. miR-21 promotes keratinocyte migration and re-epithel ial ization during wound heal ing. Int J Biol Sci, 2011, 7(5):685-690.
43. 刘显庆. MicroRNA-21在高糖诱导血管内皮细胞凋亡中的表达及功能.长沙:中南大学, 2010.
44. Khanna S, Biswas S, Shang Y, et al. Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One, 2010, 5(3):e9539.
45. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol, 2010, 11(2):141-147.
46. Fleenor DL, Shepard AR, Hellberg PE, et al. TGFbeta2-induced changes in human trabecular meshwork:implications for intraocular pressure. Invest Ophthalmol Vis Sci, 2006, 47(1):226-234.
47. Maurer B, Stanczyk J, Jüngel A, et al. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum, 2010, 62(6): 1733-1743.
48. van Rooij E, Sutherland LB, Thatcher JE, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A, 2008, 105(35):13027-13032.
49. He A, Zhu L, Gupta N, et al. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insul in resistance in 3T3-L1 adi pocytes. Mol Endocrinol, 2007, 21(11):2785-2794.

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RESEARCH PROGRESS ON ROLE OF microRNA IN HEALING OF DIABETIC WOUND

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