ROLE OF microRNA IN SKIN DEVELOPMENT AND WOUND HEALING_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

SONGZhifang ¹ ,  LIUDewu ²

1. Department of Cardiovascular Medicine, Nanchang Jiangxi, 330006, P. R. China;
2. Department of Burns Center, the First Affiliated Hospital of Nanchang University, Nanchang Jiangxi, 330006, P. R. China;

Corresponding author：

LIUDewu, Email: dewuliu@126.com

Keywords：

microiRNA; Skin development; Skin regeneration; Wound healing

DOI：

10.7507/1002-1892.20140200

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the role of microRNA (miRNA) in skin development and wound healing. Methods The recent literature about miRNA in skin development and wound healing was reviewed and analyzed. Results miRNA extensively involved in the development of the skin,including epidermal cell proliferation,differentiation,aging and hair follicle development;miR-203 known as the "skin-specific miRNA" can directly inhibit the expression of p63 and promote the differentiation of the epidermis.Meanwhile,miRNA also involved in various stages of skin regeneration and wound healing.Abnormal expression of miRNA is closely related with abnormal wound healing. Conclusion miRNA play an important role in maintaining normal skin physiology and skin regeneration.To explore their roles in the healing of skin wounds and their regulatory mechanism can provide a new target for the treatment,which has a potential value and broad prospects.

Citation： SONGZhifang, LIUDewu. ROLE OF microRNA IN SKIN DEVELOPMENT AND WOUND HEALING. Chinese Journal of Reparative and Reconstructive Surgery, 2014, 28(7): 913-918. doi: 10.7507/1002-1892.20140200 Copy

1.	Botchkareva NV.MicroRNA/mRNA regulatory networks in the control of skin development and regeneration.Cell Cycle,2012,11(3):468-474.
2.	Yi R,Fuchs E.MicroRNA-mediated control in the skin.Cell Death Differ,2010,17(2):229-235.
3.	Bostjancic E,Glavac D.Importance of microRNAs in skin morphogenesis and diseases.Acta Dermatovenerol Alp Panonica Adriat,2008,17(3):95-102.
4.	Xu L,Yang BF,Ai J.MicroRNA transport:a new way in cell communication.J Cell Physiol,2013,228(8):1713-1719.
5.	Vera J,Lai X,Schmitz U,et al.MicroRNA-regulated networks:the perfect storm for classical molecular biology,the ideal scenario for systems biology.Adv Exp Med Biol,2013,774:55-76.
6.	Finnegan EF,Pasquinelli AE.MicroRNA biogenesis:regulating the regulators.Crit Rev Biochem Mol Biol,2013,48(1):51-68.
7.	Fabian MR,Sonenberg N.The mechanics of miRNA-mediated gene silencing:a look under the hood of miRISC.Nat Struct Mol Biol,2012,19(6):586-593.
8.	Ul Hussain M.Micro-RNAs (miRNAs):genomic organisation,biogenesis and mode of action.Cell Tissue Res,2012,349(2):405-413.
9.	Friedman RC,Farh KK,Burge CB,et al.Most mammalian mRNAs are conserved targets of microRNAs.Genome Res,2009,19(1):92-105.
10.	Reczko M,Maragkakis M,Alexiou P,et al.Functional microRNA targets in protein coding sequences.Bioinformatics,2012,28(6):771-776.
11.	Zhang R,Wang D,Xia Z,et al.The role of microRNAs in adipocyte differentiation.Front Med,2013,7(2):223-230.
12.	Bernstein E,Kim SY,Carmell MA,et al.Dicer is essential for mouse development.Nat Genet,2003,35(3):215-217.
13.	Wang Y,Medvid R,Melton C,et al.DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal.Nat Genet,2007,39(3):380-385.
14.	Yi R,Pasolli HA,Landthaler M,et al.DGCR8-dependent microRNA biogenesis is essential for skin development.Proc Natl Acad Sci U S A,2009,106(2):498-502.
15.	Andl T,Murchison EP,Liu F,et al.The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles.Curr Biol,2006,16(10):1041-1049.
16.	Ning MS,Andl T.Control by a hair's breadth:the role of microRNAs in the skin.Cell Mol Life Sci,2013,70(7):1149-1169.
17.	Sonkoly E,Wei T,Janson PC,et al.MicroRNAs:novel regulators involved in the pathogenesis of psoriasis? PLoS One,2007,2(7):e610.
18.	Yi R,Poy MN,Stoffel M,et al.A skin microRNA promotes differentiation by repressing ‘stemness’.Nature,2008,452(7184):225-229.
19.	Wienholds E,Kloosterman WP,Miska E,et al.MicroRNA expression in zebrafish embryonic development.Science,2005,309(5732):310-311.
20.	Wei T,Orfanidis K,Xu N,et al.The expression of microRNA-203 during human skin morphogenesis.Exp Dermatol,2010,19(9):854-856.
21.	McKenna DJ,McDade SS,Patel D,et al.MicroRNA 203 expression in keratinocytes is dependent on regulation of p53 levels by E6.J Virol,2010,84(20):10644-10652.
22.	Sonkoly E,Wei T,Pavez Loriè E,et al.Protein kinase C-dependent upregulation of miR-203 induces the differentiation of human keratinocytes.J Invest Dermatol,2010,130(1):124-134.
23.	Lena AM,Shalom-Feuerstein R,Rivetti Di Val Cervo P,et al.miR-203 represses ‘stemness’ by repressing DeltaNp63.Cell Death Differ,2008,15(7):1187-1195.
24.	Suzuki D,Senoo M.Increased p63 phosphorylation marks early transition of epidermal stem cells to progenitors.J Invest Dermatol,2012,132(10):2461-2464.
25.	Jackson SJ,Zhang Z,Feng D,et al.Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation.Development,2013,140(9):1882-1891.
26.	Chikh A,Matin RN,Senatore V,et al.iASPP/p63 autoregulatory feedback loop is required for the homeostasis of stratified epithelia.EMBO J,2011,30(20):4261-4273.
27.	Antonini D,Russo MT,De Rosa L,et al.Transcriptional repression of miR-34 family contributes to p63-mediated cell cycle progression in epidermal cells.J Invest Dermatol,2010,130(5):1249-1257.
28.	Su X,Chakravarti D,Cho MS,et al.TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs.Nature,2010,467(7318):986-990.
29.	Zhang L,Stokes N,Polak L,et al.Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment.Cell Stem Cell,2011,8(3):294-308.
30.	Giglio S,Cirombella R,Amodeo R,et al.MicroRNA miR-24 promotes cell proliferation by targeting the CDKs inhibitors p27Kip1 and p16INK4a.J Cell Physiol,2013,228(10):2015-2023.
31.	Wang X,Tredget EE,Wu Y.Dynamic signals for hair follicle development and regeneration.Stem Cells Dev,2012,21(1):7-18.
32.	Mardaryev AN,Ahmed MI,Vlahov NV,et al.Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle.FASEB J,2010,24(10):3869-3881.
33.	Peng H,Kaplan N,Hamanaka RB,et al.microRNA-31/factor-inhibiting hypoxia-inducible factor 1 nexus regulates keratinocyte differentiation.Proc Natl Sci U S A,2012,109(35):14030-14034.
34.	Shin KH,Pucar A,Kim RH,et al.Identification of senescence-inducing microRNAs in normal human keratinocytes.Int J Oncol,2011,39(5):1205-1211.
35.	Lena AM,Mancini M,Rivetti di Val Cervo P,et al.MicroRNA-191 triggers keratinocytes senescence by SATB1 and CDK6 downregulation.Biochem Biophys Res Commun,2012,423(3):509-514.
36.	Lee YS,Wysocki A,Warburton D,et al.Wound healing in development.Birth Defects Res C Embryo Today,2012,96(3):213-222.
37.	Roy S,Sen CK.miRNA in wound inflammation and angiogenesis.Microcirculation,2012,19(3):224-232.
38.	Schulte LN,Westermann AJ,Vogel J.Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing.Nucleic Acids Res,2013,41(1):542-553.
39.	Olivieri F,Spazzafumo L,Santini G,et al.Age-related differences in the expression of circulating microRNAs:miR-21 as a new circulating marker of inflammating.Mech Ageing Dev,2012,133(11-12):675-685.
40.	Tili E,Michaille JJ,Cimino A,et al.Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock.J Immunol,2007,179(8):5082-5089.
41.	DiPietro LA.Angiogenesis and scar formation in healing wounds.Curr Opin Rheumatol,2013,25(1):87-91.
42.	Caporali A,Emanueli C.MicroRNA regulation in angiogenesis.Vascul Pharmacol,2011,55(4):79-86.
43.	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.
44.	Fiedler J,Thum T.MicroRNAs looping around angiogenesis.Arterioscler Thromb Vasc Biol,2011,31(11):2367-2368.
45.	Chen JJ,Zhou SH.Mesenchymal stem cells overexpressing MiR-126 enhance ischemic angiogenesis via the AKT/ERK-related pathway.Cardiol J,2011,18(6):675-681.
46.	Chen Y,Gorski DH.Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5.Blood,2008,111(3):1217-1226.
47.	Pulkkinen K,Malm T,Turunen M,et al.Hypoxia induces microRNA miR-210 in vitro and in vivo ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210.FEBS Lett,2008,582(16):2397-2401.
48.	Fasanaro P,D'Alessandra Y,Di Stefano V,et al.MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3.J Biol Chem,2008,283(23):15878-15883.
49.	Langenkamp E,Zwiers PJ,Moorlag HE,et al.Vascular endothelial growth factor receptor 2 inhibition in-vivo affects tumor vasculature in a tumor type-dependent way and downregulates vascular endothelial growth factor receptor 2 protein without a prominent role for miR-296.Anticancer Drugs,2012,23(2):161-172.
50.	Chen LT,Xu SD,Xu H,et al.MicroRNA-378 is associated with non-small cell lung cancer brain metastasis by promoting cell migration,invasion and tumor angiogenesis.Med Oncol,2012,29(3):1673-1680.
51.	Ando H,Okamoto A,Yokota M,et al.Development of a miR-92a delivery system for anti-angiogenesis-based cancer therapy.J Gene Med,2013,15(1):20-27.
52.	Ohyagi-Hara C,Sawada K,Kamiura S,et al.miR-92a inhibits peritoneal dissemination of ovarian cancer cells by inhibiting integrin α5 expression.Am J Pathol,2013,182(5):1876-1889.
53.	Doebele C,Bonauer A,Fischer A,et al.Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells.Blood,2010,115(23):4944-4950.
54.	Roy S,Sen CK.miRNA in wound inflammation and angiogenesis.Microcirculation,2012,19(3):224-232.
55.	Wang XH,Qian RZ,Zhang W,et al.MicroRNA-320 expression in myocardial microvascular endothelial cellsand its relationship with insulin-like growth factor-1 in type 2 diabetic rats.Clin Exp Pharmacol Physiol,2009,36(2):181-188.
56.	Patella F,Rainaldi G.MicroRNAs mediate metabolic stresses and angiogenesis.Cell Mol Life Sci,2012,69(7):1049-1065.
57.	Shibata S,Tada Y,Asano Y,et al.Adiponectin regulates cutaneous wound healing by promoting keratinocyte proliferation and migration via the ERK signaling pathway.J Immunol,2012,189(6):3231-3241.
58.	Yu J,Peng H,Ruan Q,et al.MicroRNA-205 promotes keratinocyte migration via the lipid phosphatase SHIP2.FASEB J,2010,24(10):3950-3959.
59.	Yu J,Ryan DG,Getsios S,et al.MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia.Proc Natl Acad Sci U S A,2008,105(49):19300-19305.
60.	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.
61.	Fasanaro P,Greco S,Lorenzi M,et al.An integrated approach for experimental target identification of hypoxia-induced miR-210.J Biol Chem,2009,284(50):35134-35143.
62.	Yang X,Wang J,Guo SL,et al.miR-21 promotes keratinocyte migration and re-epithelialization during wound healing.Int J Biol Sci,2011,7(5):685-690.
63.	Larson BJ,Longaker MT,Lorenz HP.Scarless fetal wound healing:a basic science review.Plast Reconstr Surg,2010,126(4):1172-1180.
64.	Leung A,Crombleholme TM,Keswani SG.Fetal wound healing:implications for minimal scar formation.Curr Opin Pediatr,2012,24(3):371-378.
65.	Cheng J,Yu H,Deng S,et al.MicroRNA profiling in mid- and late-gestational fetal skin:implication for scarless wound healing.Tohoku J Exp Med,2010,221(3):203-209.
66.	Li Z,Hassan MQ,Jafferji M,et al.Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation.J Biol Chem,2009,284(23):15676-15684.
67.	Kato M,Zhang J,Wang M,et al.MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors.Proc Natl Acad Sci U S A,2007,104(9):3432-3437.
68.	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.
69.	Kashiyama K,Mitsutake N,Matsuse M,et al.miR-196a downregulation increases the expression of type I and Ⅲ collagens in keloid fibroblasts.J Invest Dermatol,2012,132(6):1597-1604.
70.	Bertero T,Gastaldi C,Bourget-Ponzio I,et al.miR-483-3p controls proliferation in wounded epithelial cells.FASEB J,2011,25(9):3092-3105.

1. Botchkareva NV.MicroRNA/mRNA regulatory networks in the control of skin development and regeneration.Cell Cycle,2012,11(3):468-474.
2. Yi R,Fuchs E.MicroRNA-mediated control in the skin.Cell Death Differ,2010,17(2):229-235.
3. Bostjancic E,Glavac D.Importance of microRNAs in skin morphogenesis and diseases.Acta Dermatovenerol Alp Panonica Adriat,2008,17(3):95-102.
4. Xu L,Yang BF,Ai J.MicroRNA transport:a new way in cell communication.J Cell Physiol,2013,228(8):1713-1719.
5. Vera J,Lai X,Schmitz U,et al.MicroRNA-regulated networks:the perfect storm for classical molecular biology,the ideal scenario for systems biology.Adv Exp Med Biol,2013,774:55-76.
6. Finnegan EF,Pasquinelli AE.MicroRNA biogenesis:regulating the regulators.Crit Rev Biochem Mol Biol,2013,48(1):51-68.
7. Fabian MR,Sonenberg N.The mechanics of miRNA-mediated gene silencing:a look under the hood of miRISC.Nat Struct Mol Biol,2012,19(6):586-593.
8. Ul Hussain M.Micro-RNAs (miRNAs):genomic organisation,biogenesis and mode of action.Cell Tissue Res,2012,349(2):405-413.
9. Friedman RC,Farh KK,Burge CB,et al.Most mammalian mRNAs are conserved targets of microRNAs.Genome Res,2009,19(1):92-105.
10. Reczko M,Maragkakis M,Alexiou P,et al.Functional microRNA targets in protein coding sequences.Bioinformatics,2012,28(6):771-776.
11. Zhang R,Wang D,Xia Z,et al.The role of microRNAs in adipocyte differentiation.Front Med,2013,7(2):223-230.
12. Bernstein E,Kim SY,Carmell MA,et al.Dicer is essential for mouse development.Nat Genet,2003,35(3):215-217.
13. Wang Y,Medvid R,Melton C,et al.DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal.Nat Genet,2007,39(3):380-385.
14. Yi R,Pasolli HA,Landthaler M,et al.DGCR8-dependent microRNA biogenesis is essential for skin development.Proc Natl Acad Sci U S A,2009,106(2):498-502.
15. Andl T,Murchison EP,Liu F,et al.The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles.Curr Biol,2006,16(10):1041-1049.
16. Ning MS,Andl T.Control by a hair's breadth:the role of microRNAs in the skin.Cell Mol Life Sci,2013,70(7):1149-1169.
17. Sonkoly E,Wei T,Janson PC,et al.MicroRNAs:novel regulators involved in the pathogenesis of psoriasis? PLoS One,2007,2(7):e610.
18. Yi R,Poy MN,Stoffel M,et al.A skin microRNA promotes differentiation by repressing ‘stemness’.Nature,2008,452(7184):225-229.
19. Wienholds E,Kloosterman WP,Miska E,et al.MicroRNA expression in zebrafish embryonic development.Science,2005,309(5732):310-311.
20. Wei T,Orfanidis K,Xu N,et al.The expression of microRNA-203 during human skin morphogenesis.Exp Dermatol,2010,19(9):854-856.
21. McKenna DJ,McDade SS,Patel D,et al.MicroRNA 203 expression in keratinocytes is dependent on regulation of p53 levels by E6.J Virol,2010,84(20):10644-10652.
22. Sonkoly E,Wei T,Pavez Loriè E,et al.Protein kinase C-dependent upregulation of miR-203 induces the differentiation of human keratinocytes.J Invest Dermatol,2010,130(1):124-134.
23. Lena AM,Shalom-Feuerstein R,Rivetti Di Val Cervo P,et al.miR-203 represses ‘stemness’ by repressing DeltaNp63.Cell Death Differ,2008,15(7):1187-1195.
24. Suzuki D,Senoo M.Increased p63 phosphorylation marks early transition of epidermal stem cells to progenitors.J Invest Dermatol,2012,132(10):2461-2464.
25. Jackson SJ,Zhang Z,Feng D,et al.Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation.Development,2013,140(9):1882-1891.
26. Chikh A,Matin RN,Senatore V,et al.iASPP/p63 autoregulatory feedback loop is required for the homeostasis of stratified epithelia.EMBO J,2011,30(20):4261-4273.
27. Antonini D,Russo MT,De Rosa L,et al.Transcriptional repression of miR-34 family contributes to p63-mediated cell cycle progression in epidermal cells.J Invest Dermatol,2010,130(5):1249-1257.
28. Su X,Chakravarti D,Cho MS,et al.TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs.Nature,2010,467(7318):986-990.
29. Zhang L,Stokes N,Polak L,et al.Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment.Cell Stem Cell,2011,8(3):294-308.
30. Giglio S,Cirombella R,Amodeo R,et al.MicroRNA miR-24 promotes cell proliferation by targeting the CDKs inhibitors p27Kip1 and p16INK4a.J Cell Physiol,2013,228(10):2015-2023.
31. Wang X,Tredget EE,Wu Y.Dynamic signals for hair follicle development and regeneration.Stem Cells Dev,2012,21(1):7-18.
32. Mardaryev AN,Ahmed MI,Vlahov NV,et al.Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle.FASEB J,2010,24(10):3869-3881.
33. Peng H,Kaplan N,Hamanaka RB,et al.microRNA-31/factor-inhibiting hypoxia-inducible factor 1 nexus regulates keratinocyte differentiation.Proc Natl Sci U S A,2012,109(35):14030-14034.
34. Shin KH,Pucar A,Kim RH,et al.Identification of senescence-inducing microRNAs in normal human keratinocytes.Int J Oncol,2011,39(5):1205-1211.
35. Lena AM,Mancini M,Rivetti di Val Cervo P,et al.MicroRNA-191 triggers keratinocytes senescence by SATB1 and CDK6 downregulation.Biochem Biophys Res Commun,2012,423(3):509-514.
36. Lee YS,Wysocki A,Warburton D,et al.Wound healing in development.Birth Defects Res C Embryo Today,2012,96(3):213-222.
37. Roy S,Sen CK.miRNA in wound inflammation and angiogenesis.Microcirculation,2012,19(3):224-232.
38. Schulte LN,Westermann AJ,Vogel J.Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing.Nucleic Acids Res,2013,41(1):542-553.
39. Olivieri F,Spazzafumo L,Santini G,et al.Age-related differences in the expression of circulating microRNAs:miR-21 as a new circulating marker of inflammating.Mech Ageing Dev,2012,133(11-12):675-685.
40. Tili E,Michaille JJ,Cimino A,et al.Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock.J Immunol,2007,179(8):5082-5089.
41. DiPietro LA.Angiogenesis and scar formation in healing wounds.Curr Opin Rheumatol,2013,25(1):87-91.
42. Caporali A,Emanueli C.MicroRNA regulation in angiogenesis.Vascul Pharmacol,2011,55(4):79-86.
43. 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.
44. Fiedler J,Thum T.MicroRNAs looping around angiogenesis.Arterioscler Thromb Vasc Biol,2011,31(11):2367-2368.
45. Chen JJ,Zhou SH.Mesenchymal stem cells overexpressing MiR-126 enhance ischemic angiogenesis via the AKT/ERK-related pathway.Cardiol J,2011,18(6):675-681.
46. Chen Y,Gorski DH.Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5.Blood,2008,111(3):1217-1226.
47. Pulkkinen K,Malm T,Turunen M,et al.Hypoxia induces microRNA miR-210 in vitro and in vivo ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210.FEBS Lett,2008,582(16):2397-2401.
48. Fasanaro P,D'Alessandra Y,Di Stefano V,et al.MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3.J Biol Chem,2008,283(23):15878-15883.
49. Langenkamp E,Zwiers PJ,Moorlag HE,et al.Vascular endothelial growth factor receptor 2 inhibition in-vivo affects tumor vasculature in a tumor type-dependent way and downregulates vascular endothelial growth factor receptor 2 protein without a prominent role for miR-296.Anticancer Drugs,2012,23(2):161-172.
50. Chen LT,Xu SD,Xu H,et al.MicroRNA-378 is associated with non-small cell lung cancer brain metastasis by promoting cell migration,invasion and tumor angiogenesis.Med Oncol,2012,29(3):1673-1680.
51. Ando H,Okamoto A,Yokota M,et al.Development of a miR-92a delivery system for anti-angiogenesis-based cancer therapy.J Gene Med,2013,15(1):20-27.
52. Ohyagi-Hara C,Sawada K,Kamiura S,et al.miR-92a inhibits peritoneal dissemination of ovarian cancer cells by inhibiting integrin α5 expression.Am J Pathol,2013,182(5):1876-1889.
53. Doebele C,Bonauer A,Fischer A,et al.Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells.Blood,2010,115(23):4944-4950.
54. Roy S,Sen CK.miRNA in wound inflammation and angiogenesis.Microcirculation,2012,19(3):224-232.
55. Wang XH,Qian RZ,Zhang W,et al.MicroRNA-320 expression in myocardial microvascular endothelial cellsand its relationship with insulin-like growth factor-1 in type 2 diabetic rats.Clin Exp Pharmacol Physiol,2009,36(2):181-188.
56. Patella F,Rainaldi G.MicroRNAs mediate metabolic stresses and angiogenesis.Cell Mol Life Sci,2012,69(7):1049-1065.
57. Shibata S,Tada Y,Asano Y,et al.Adiponectin regulates cutaneous wound healing by promoting keratinocyte proliferation and migration via the ERK signaling pathway.J Immunol,2012,189(6):3231-3241.
58. Yu J,Peng H,Ruan Q,et al.MicroRNA-205 promotes keratinocyte migration via the lipid phosphatase SHIP2.FASEB J,2010,24(10):3950-3959.
59. Yu J,Ryan DG,Getsios S,et al.MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia.Proc Natl Acad Sci U S A,2008,105(49):19300-19305.
60. 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.
61. Fasanaro P,Greco S,Lorenzi M,et al.An integrated approach for experimental target identification of hypoxia-induced miR-210.J Biol Chem,2009,284(50):35134-35143.
62. Yang X,Wang J,Guo SL,et al.miR-21 promotes keratinocyte migration and re-epithelialization during wound healing.Int J Biol Sci,2011,7(5):685-690.
63. Larson BJ,Longaker MT,Lorenz HP.Scarless fetal wound healing:a basic science review.Plast Reconstr Surg,2010,126(4):1172-1180.
64. Leung A,Crombleholme TM,Keswani SG.Fetal wound healing:implications for minimal scar formation.Curr Opin Pediatr,2012,24(3):371-378.
65. Cheng J,Yu H,Deng S,et al.MicroRNA profiling in mid- and late-gestational fetal skin:implication for scarless wound healing.Tohoku J Exp Med,2010,221(3):203-209.
66. Li Z,Hassan MQ,Jafferji M,et al.Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation.J Biol Chem,2009,284(23):15676-15684.
67. Kato M,Zhang J,Wang M,et al.MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors.Proc Natl Acad Sci U S A,2007,104(9):3432-3437.
68. 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.
69. Kashiyama K,Mitsutake N,Matsuse M,et al.miR-196a downregulation increases the expression of type I and Ⅲ collagens in keloid fibroblasts.J Invest Dermatol,2012,132(6):1597-1604.
70. Bertero T,Gastaldi C,Bourget-Ponzio I,et al.miR-483-3p controls proliferation in wounded epithelial cells.FASEB J,2011,25(9):3092-3105.

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ROLE OF microRNA IN SKIN DEVELOPMENT AND WOUND HEALING

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