Integrative analysis of miRNA and mRNA paired expression profiling of primary fibroblast derived from diabetic foot ulcers reveals multiple impaired cellular functions

Wound Repair and Regeneration

Volumn 24, Issue 6, 2016, Pages 943-953

  Liang, Liang ^a   Stone, Rivka C ^a   Stojadinovic, Olivera ^a,b   Ramirez, Horacio ^a,c   Pastar, Irena ^a   Maione, Anna G ^c,d   Smith, Avi ^a   Yanez, Vanessa ^a   Veves, Aristides ^e   Kirsner, Robert S ^a,b   Garlick, Jonathan A ^c,d   Tomic Canic, Marjana ^a,b,c  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI HEALTH SYSTEM   (United States)

^c TUFTS UNIVERSITY   (United States)

^d TUFTS UNIVERSITY SCHOOL OF DENTAL MEDICINE   (United States)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 145 5P; MICRORNA 21 5P; MICRORNA 34A 5P; UNCLASSIFIED DRUG;

ARTICLE; CELL AGING; CELL ASSAY; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL MOTION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC FOOT; FIBROBLAST; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC REGULATION; GENOME ANALYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; ULCER HEALING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROARRAY ANALYSIS; PATHOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WOUND HEALING;

BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLULAR SENESCENCE; DIABETIC FOOT; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; MICRORNAS; RNA, MESSENGER; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 84990220376     PISSN: 10671927     EISSN: 1524475X     Source Type: Journal    
DOI: 10.1111/wrr.12470     Document Type: Article

References (50)

1. Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet 2005; 366: 1719–24.
2. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest 2007; 117: 1219–22.
3. Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet 2003; 361: 1545–51.
4. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005; 366: 1736–43.
5. Brem H, Golinko MS, Stojadinovic O, Kodra A, Diegelmann RF, Vukelic S, et al. Primary cultured fibroblasts derived from patients with chronic wounds: a methodology to produce human cell lines and test putative growth factor therapy such as GMCSF. J Transl Med 2008; 6: 75.
6. Maione AG, Brudno Y, Stojadinovic O, Park LK, Smith A, Tellechea A, et al. Three-dimensional human tissue models that incorporate diabetic foot ulcer-derived fibroblasts mimic in vivo features of chronic wounds. Tissue Eng Part C Methods 2015; 21: 499–508.
7. Park LK, Maione AG, Smith A, Gerami-Naini B, Iyer LK, Mooney DJ, et al. Genome-wide DNA methylation analysis identifies a metabolic memory profile in patient-derived diabetic foot ulcer fibroblasts. Epigenetics 2014; 9: 1339–49.
8. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350–5.
9. Gras C, Ratuszny D, Hadamitzky C, Zhang H, Blasczyk R, Figueiredo C. miR-145 contributes to hypertrophic scarring of the skin by inducing myofibroblast activity. Mol Med 2015; 21: 296–304.
10. Huang RY, Li L, Wang MJ, Chen XM, Huang QC, Lu CJ. An exploration of the role of microRNAs in psoriasis: a systematic review of the literature. Medicine 2015; 94: e2030.
11. Pastar I, Khan AA, Stojadinovic O, Lebrun EA, Medina MC, Brem H, et al. Induction of specific microRNAs inhibits cutaneous wound healing. J Biol Chem 2012; 287: 29324–35.
12. Deppe J, Steinritz D, Santovito D, Egea V, Schmidt A, Weber C, et al. Upregulation of miR-203 and miR-210 affect growth and differentiation of keratinocytes after exposure to sulfur mustard in normoxia and hypoxia. Toxicol Lett 2016; 244: 81–7.
13. Ramirez HA, Liang L, Pastar I, Rosa AM, Stojadinovic O, Zwick TG, et al. Comparative genomic, microRNA, and tissue analyses reveal subtle differences between non-diabetic and diabetic foot skin. PLoS One 2015; 10: e0137133.
14. Vukelic S, Stojadinovic O, Pastar I, Vouthounis C, Krzyzanowska A, Das S, et al. Farnesyl pyrophosphate inhibits epithelialization and wound healing through the glucocorticoid receptor. J Biol Chem 2010; 285: 1980–8.
15. Hu SJ, Ren G, Liu JL, Zhao ZA, Yu YS, Su RW, et al. MicroRNA expression and regulation in mouse uterus during embryo implantation. J Biol Chem 2008; 283: 23473–84.
16. Junker A, Krumbholz M, Eisele S, Mohan H, Augstein F, Bittner R, et al. MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 2009;132 (Pt 12): 3342–52.
17. Polytarchou C, Iliopoulos D, Hatziapostolou M, Kottakis F, Maroulakou I, Struhl K, et al. Akt2 regulates all Akt isoforms and promotes resistance to hypoxia through induction of miR-21 upon oxygen deprivation. Cancer Res 2011; 71: 4720–31.
18. Shi B, Sepp-Lorenzino L, Prisco M, Linsley P, deAngelis T, Baserga R. Micro RNA 145 targets the insulin receptor substrate-1 and inhibits the growth of colon cancer cells. J Biol Chem 2007; 282: 32582–90.
19. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008; 456: 980–4.
20. Liu R, Liao J, Yang M, Sheng J, Yang H, Wang Y, et al. The cluster of miR-143 and miR-145 affects the risk for esophageal squamous cell carcinoma through co-regulating fascin homolog 1. PLoS One 2012; 7: e33987.
21. Kent OA, McCall MN, Cornish TC, Halushka MK. Lessons from miR-143/145: the importance of cell-type localization of miRNAs. Nucleic Acids Res 2014; 42: 7528–38.
22. Debacq-Chainiaux F, Pascal T, Boilan E, Bastin C, Bauwens E, Toussaint O. Screening of senescence-associated genes with specific DNA array reveals the role of IGFBP-3 in premature senescence of human diploid fibroblasts. Free Radic Biol Med 2008; 44: 1817–32.
23. Cecilia-Matilla A, Lazaro-Martinez JL, Aragon-Sanchez J, Garcia-Morales E, Garcia-Alvarez Y, Beneit-Montesinos JV. Histopathologic characteristics of bone infection complicating foot ulcers in diabetic patients. J Am Podiatr Med Assoc 2013; 103: 24–31.
24. Zhu H, Li Y, Qu S, Luo H, Zhou Y, Wang Y, et al. MicroRNA expression abnormalities in limited cutaneous scleroderma and diffuse cutaneous scleroderma. J Clin Immunol 2012; 32: 514–22.
25. Dellago H, Preschitz-Kammerhofer B, Terlecki-Zaniewicz L, Schreiner C, Fortschegger K, Chang MW, et al. High levels of oncomiR-21 contribute to the senescence-induced growth arrest in normal human cells and its knock-down increases the replicative lifespan. Aging Cell 2013; 12: 446–58.
26. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, et al. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 2001; 107: 789–800.
27. Omura A, Matsuzaki T, Mio K, Ogura T, Yamamoto M, Fujita A, et al. RECK forms cowbell-shaped dimers and inhibits matrix metalloproteinase-catalyzed cleavage of fibronectin. J Biol Chem 2009; 284: 3461–9.
28. Kimura T, Okada A, Yatabe T, Okubo M, Toyama Y, Noda M, et al. RECK is up-regulated and involved in chondrocyte cloning in human osteoarthritic cartilage. Am J Pathol 2010; 176: 2858–67.
29. Adam O, Lohfelm B, Thum T, Gupta SK, Puhl SL, Schafers HJ, et al. Role of miR-21 in the pathogenesis of atrial fibrosis. Basic Res Cardiol 2012; 107: 278.
30. Zanotti S, Gibertini S, Curcio M, Savadori P, Pasanisi B, Morandi L, et al. Opposing roles of miR-21 and miR-29 in the progression of fibrosis in Duchenne muscular dystrophy. Biochim Biophys Acta 2015; 1852: 1451–64.
31. Wang YS, Li SH, Guo J, Mihic A, Wu J, Sun L, et al. Role of miR-145 in cardiac myofibroblast differentiation. J Mol Cell Cardiol 2014; 66: 94–105.
32. Yang S, Cui H, Xie N, Icyuz M, Banerjee S, Antony VB, et al. miR-145 regulates myofibroblast differentiation and lung fibrosis. FASEB J 2013; 27: 2382–91.
33. Davis-Dusenbery BN, Chan MC, Reno KE, Weisman AS, Layne MD, Lagna G, et al. Down-regulation of Kruppel-like factor-4 (KLF4) by microRNA-143/145 is critical for modulation of vascular smooth muscle cell phenotype by transforming growth factor-beta and bone morphogenetic protein 4. J Biol Chem 2011; 286: 28097–110.
34. Yang X, Popescu NC, Zimonjic DB. DLC1 interaction with S100A10 mediates inhibition of in vitro cell invasion and tumorigenicity of lung cancer cells through a RhoGAP-independent mechanism. Cancer Res 2011; 71: 2916–25.
35. Ng DC, Lin BH, Lim CP, Huang G, Zhang T, Poli V, et al. Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. J Cell Biol 2006; 172: 245–57.
36. Pang M, Ma L, Liu N, Ponnusamy M, Zhao TC, Yan H, et al. Histone deacetylase 1/2 mediates proliferation of renal interstitial fibroblasts and expression of cell cycle proteins. J Cell Biochem 2011; 112: 2138–48.
37. Zhang Y, Sime W, Juhas M, Sjolander A. Crosstalk between colon cancer cells and macrophages via inflammatory mediators and CD47 promotes tumour cell migration. Eur J Cancer 2013; 49: 3320–34.
38. Zheng M, Sun X, Li Y, Zuo W. MicroRNA-145 inhibits growth and migration of breast cancer cells through targeting oncoprotein ROCK1. Tumour Biol 2016; 37: 8189–96.
39. Cho WC, Chow AS, Au JS. Restoration of tumour suppressor hsa-miR-145 inhibits cancer cell growth in lung adenocarcinoma patients with epidermal growth factor receptor mutation. Eur J Cancer 2009; 45: 2197–206.
40. Wang Z, Zhang X, Yang Z, Du H, Wu Z, Gong J, et al. MiR-145 regulates PAK4 via the MAPK pathway and exhibits an antitumor effect in human colon cells. Biochem Biophys Res Commun 2012; 427: 444–9.
41. Wang Y, Hu C, Cheng J, Chen B, Ke Q, Lv Z, et al. MicroRNA-145 suppresses hepatocellular carcinoma by targeting IRS1 and its downstream Akt signaling. Biochem Biophys Res Commun 2014; 446: 1255–60.
42. Kumar A, Hou X, Lee C, Li Y, Maminishkis A, Tang Z, et al. Platelet-derived growth factor-DD targeting arrests pathological angiogenesis by modulating glycogen synthase kinase-3beta phosphorylation. J Biol Chem 2010; 285: 15500–10.
43. Kong L, Zhu J, Han W, Jiang X, Xu M, Zhao Y, et al. Significance of serum microRNAs in pre-diabetes and newly diagnosed type 2 diabetes: a clinical study. Acta Diabetol 2011; 48: 61–9.
44. Maes OC, Sarojini H, Wang E. Stepwise up-regulation of microRNA expression levels from replicating to reversible and irreversible growth arrest states in WI-38 human fibroblasts. J Cell Physiol 2009; 221: 109–19.
45. Khee SG, Yusof YA, Makpol S. Expression of senescence-associated microRNAs and target genes in cellular aging and modulation by tocotrienol-rich fraction. Oxid Med Cell Longev 2014; 2014: 725929.
46. Liu FJ, Wen T, Liu L. MicroRNAs as a novel cellular senescence regulator. Ageing Res Rev 2012; 11: 41–50.
47. Mendez MV, Stanley A, Park HY, Shon K, Phillips T, Menzoian JO. Fibroblasts cultured from venous ulcers display cellular characteristics of senescence. J Vasc Surg 1998; 28: 876–83.
48. Sorrell JM, Baber MA, Caplan AI. Construction of a bilayered dermal equivalent containing human papillary and reticular dermal fibroblasts: use of fluorescent vital dyes. Tissue Eng 1996; 2: 39–49.
49. Sorrell JM, Baber MA, Caplan AI. Site-matched papillary and reticular human dermal fibroblasts differ in their release of specific growth factors/cytokines and in their interaction with keratinocytes. J Cell Physiol 2004; 200: 134–45.
50. Harper RA, Grove G. Human skin fibroblasts derived from papillary and reticular dermis: differences in growth potential in vitro. Science 1979; 204: 526–7.