Comparative genomic, microRNA, and tissue analyses reveal subtle differences between non-diabetic and diabetic foot skin

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Ramirez, Horacio A ^a   Liang, Liang ^a   Pastar, Irena ^a   Rosa, Ashley M ^a   Stojadinovic, Olivera ^a   Zwick, Thomas G ^b   Kirsner, Robert S ^a,b   Maione, Anna G ^c,d   Garlick, Jonathan A ^c,d   Tomic Canic, Marjana ^a  

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

^b UNIVERSITY OF MIAMI HOSPITAL   (United States)

^c TUFTS UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; KI 67 ANTIGEN; MICRORNA; MICRORNA 29C 3P; MICRORNA 31 3P; MICRORNA 31 5P; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD VESSEL; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETIC FOOT; DISEASE PREDISPOSITION; DOWN REGULATION; EPIDERMIS; FEMALE; FOOT SURGERY; GENE; GENE EXPRESSION PROFILING; GENOMICS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LGR5 GENE; LYMPHOCYTE; MALE; OR2A4 GENE; SKIN BIOPSY; SKIN FIBROBLAST; UPREGULATION; WOUND HEALING IMPAIRMENT; DERMIS; FIBROBLAST; FOOT ULCER; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY;

DERMIS; DIABETIC FOOT; EPIDERMIS; FIBROBLASTS; FOOT ULCER; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; MICRORNAS; TRANSCRIPTION, GENETIC;

EID: 84943279695     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137133     Document Type: Article

References (55)

1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes research and clinical practice. 2010;87(1):4-14. doi: 10.1016/j.diabres.2009.10.007 PMID: 19896746.
2. Perez MI, Kohn SR. Cutaneous manifestations of diabetes mellitus. Journal of the American Academy of Dermatology. 1994;30(4):519-31; quiz 32-4. PMID: 8157778.
3. Van Hattem S, Bootsma AH, Thio HB. Skin manifestations of diabetes. Cleveland Clinic journal of medicine. 2008;75(11):772, 4, 6-7 passim. PMID: 19068958.
4. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. The Journal of clinical investigation. 2007;117(5):1219-22. Epub 2007/05/04. doi: 10.1172/JCI32169 PMID: 17476353; PubMed Central PMCID: PMC1857239.
5. Reiber GE, Boyko E. J., and Smith D. G. Lower extremity foot ulcers and amputations in diabetes. In: Stern MIHaMP, editor. Diabetes in America. Bethesda, Maryland, USA.: U. S. Government Printing Office; 1995. p. 409-28.
6. Gregg EW, Li Y, Wang J, Burrows NR, Ali MK, Rolka D, et al. Changes in diabetes-related complications in the United States, 1990-2010. The New England journal of medicine. 2014;370(16):1514-23. doi: 10.1056/NEJMoa1310799 PMID: 24738668.
7. Eming SA, Martin P, Tomic-Canic M. Wound repair and regeneration: Mechanisms, signaling, and translation. Science translational medicine. 2014;6(265):265sr6. doi: 10.1126/scitranslmed.3009337 PMID: 25473038.
8. Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet. 2003;361(9368):1545-51. doi: 10.1016/S0140-6736 (03) 13169-8 PMID: 12737879.
9. Fowler MJ. Microvascular and macrovascular complications of diabetes. Clin Diabetes. 2008;26:77-82.
10. Xu L, Kanasaki K, Kitada M, Koya D. Diabetic angiopathy and angiogenic defects. Fibrogenesis & tissue repair. 2012;5(1):13. doi: 10.1186/1755-1536-5-13 PMID: 22853690; PubMed Central PMCID: PMC3465576.
11. Geerlings SE, Hoepelman AI. Immune dysfunction in patients with diabetes mellitus (DM). FEMS immunology and medical microbiology. 1999;26(3-4):259-65. PMID: 10575137.
12. Ban CR, Twigg SM. Fibrosis in diabetes complications: pathogenic mechanisms and circulating and urinary markers. Vascular health and risk management. 2008;4(3):575-96. PMID: 18827908; PubMed Central PMCID: PMC2515418.
13. Arya AK, Tripathi R, Kumar S, Tripathi K. Recent advances on the association of apoptosis in chronic non healing diabetic wound. World journal of diabetes. 2014;5(6):756-62. doi: 10.4239/wjd.v5.i6.756 PMID: 25512778; PubMed Central PMCID: PMC4265862.
14. Pastar I, Khan AA, Stojadinovic O, Lebrun EA, Medina MC, Brem H, et al. Induction of Specific Micro-RNAs Inhibits Cutaneous Wound Healing. The Journal of biological chemistry. 2012;287(35):29324-35. Epub 2012/07/10. doi: 10.1074/jbc. M112.382135 PMID: 22773832.
15. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of micro-RNAs. Genome research. 2009;19(1):92-105. Epub 2008/10/29. doi: 10.1101/gr.082701.108 PMID: 18955434; PubMed Central PMCID: PMC2612969.
16. Shukla GC, Singh J, Barik S. MicroRNAs: Processing, Maturation, Target Recognition and Regulatory Functions. Molecular and cellular pharmacology. 2011;3(3):83-92. PMID: 22468167; PubMed Central PMCID: PMC3315687.
17. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-33. Epub 2009/01/27. doi: 10.1016/j.cell.2009.01.002 PMID: 19167326.
18. Pastar I, Ramirez H, Stojadinovic O, Brem H, Kirsner RS, Tomic-Canic M. Micro-RNAs: New Regulators of Wound Healing. Surgical technology international. 2011; XXI: 51-60. Epub 2012/04/17. PMID: 22504970.
19. Zhong X, Coukos G, Zhang L. miRNAs in human cancer. Methods in molecular biology. 2012;822:295-306. doi: 10.1007/978-1-61779-427-8-21 PMID: 22144208; PubMed Central PMCID: PMC4076826.
20. Sonkoly E, Wei T, Janson PC, Saaf A, Lundeberg L, Tengvall-Linder M, et al. MicroRNAs: novel regulators involved in the pathogenesis of psoriasis? PloS one. 2007;2(7):e610. Epub 2007/07/12. doi: 10. 1371/journal.pone.0000610 PMID: 17622355; PubMed Central PMCID: PMC1905940.
21. Funari VA, Winkler M, Brown J, Dimitrijevich SD, Ljubimov AV, Saghizadeh M. Differentially expressed wound healing-related microRNAs in the human diabetic cornea. PloS one. 2013;8(12):e84425. doi: 10.1371/journal.pone.0084425 PMID: 24376808; PubMed Central PMCID: PMC3869828.
22. Stojadinovic O, Landon JN, Gordon KA, Pastar I, Escandon J, Vivas A, et al. Quality assessment of tissue specimens for studies of diabetic foot ulcers. Experimental dermatology. 2013;22(3):216-8. doi: 10.1111/exd.12104 PMID: 23489425.
23. Slusarz A, Pulakat L. The two faces of miR-29. Journal of cardiovascular medicine. 2015. doi: 10.2459/JCM.0000000000000246 PMID: 25689084.
24. Spanheimer RG, Umpierrez GE, Stumpf V. Decreased collagen production in diabetic rats. Diabetes. 1988;37(4):371-6. PMID: 3378683.
25. Riser BL, Denichilo M, Cortes P, Baker C, Grondin JM, Yee J, et al. Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis. Journal of the American Society of Nephrology: JASN. 2000;11(1):25-38. PMID: 10616837.
26. Ye X, Cheng X, Liu L, Zhao D, Dang Y. Blood glucose fluctuation affects skin collagen metabolism in the diabetic mouse by inhibiting the mitogen-activated protein kinase and Smad pathways. Clinical and experimental dermatology. 2013;38(5):530-7. doi: 10.1111/ced.12002 PMID: 23601172.
27. Loots MA, Lamme EN, Zeegelaar J, Mekkes JR, Bos JD, Middelkoop E. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. The Journal of investigative dermatology. 1998;111(5):850-7. doi: 10.1046/j.1523-1747.1998.00381.x PMID: 9804349.
28. Brem H, Tomic-Canic M, Entero H, Hanflik AM, Wang VM, Fallon JT, et al. The synergism of age and db/db genotype impairs wound healing. Experimental gerontology. 2007;42(6):523-31. doi: 10.1016/j. exger.2006.11.018 PMID: 17275236.
29. Otton R, Soriano FG, Verlengia R, Curi R. Diabetes induces apoptosis in lymphocytes. The Journal of endocrinology. 2004;182(1):145-56. PMID: 15225139.
30. Stojadinovic O, Brem H, Vouthounis C, Lee B, Fallon J, Stallcup M, et al. Molecular pathogenesis of chronic wounds: the role of beta-catenin and c-myc in the inhibition of epithelialization and wound healing. The American journal of pathology. 2005;167(1):59-69. Epub 2005/06/24. PMID: 15972952; PubMed Central PMCID: PMC1603435.
31. He A, Zhu L, Gupta N, Chang Y, Fang F. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Molecular endocrinology. 2007;21(11):2785-94. doi: 10.1210/me.2007-0167 PMID: 17652184.
32. Cheng J, Wang Y, Wang D, Wu Y. Identification of collagen 1 as a post-transcriptional target of miR-29b in skin fibroblasts: therapeutic implication for scar reduction. The American journal of the medical sciences. 2013;346(2):98-103. doi: 10.1097/MAJ.0b013e318267680d PMID: 23221517.
33. Madhyastha R, Madhyastha H, Nakajima Y, Omura S, Maruyama M. MicroRNA signature in diabetic wound healing: promotive role of miR-21 in fibroblast migration. Int Wound J. 2012;9(4):355-61. doi: 10.1111/j.1742-481X.2011.00890.x PMID: 22067035.
34. Xu N, Meisgen F, Butler LM, Han G, Wang XJ, Soderberg-Naucler C, et al. MicroRNA-31 is overexpressed in psoriasis and modulates inflammatory cytokine and chemokine production in keratinocytes via targeting serine/threonine kinase 40. Journal of immunology. 2013;190(2):678-88. doi: 10.4049/jimmunol.1202695 PMID: 23233723.
35. LL HR, IP HAL, MSN CDA, et al. miR-31 sustains activated keratinocytes and modulates a complex LATS2-centered protein network. JID (submitted). 2015.
36. Peng H, Kaplan N, Hamanaka RB, Katsnelson J, Blatt H, Yang W, et al. microRNA-31/factor-inhibiting hypoxia-inducible factor 1 nexus regulates keratinocyte differentiation. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(35):14030-4. doi: 10.1073/pnas. 1111292109 PMID: 22891326; PubMed Central PMCID: PMC3435188.
37. Li T, Luo W, Liu K, Lv X, Xi T. miR-31 promotes proliferation of colon cancer cells by targeting E2F2. Biotechnology letters. 2014. doi: 10.1007/s10529-014-1715-y PMID: 25362258.
38. Akin C, Soto D, Brittain E, Chhabra A, Schwartz LB, Caughey GH, et al. Tryptase haplotype in mastocytosis: relationship to disease variant and diagnostic utility of total tryptase levels. Clinical immunology. 2007;123(3):268-71. doi: 10.1016/j.clim.2007.02.007 PMID: 17449330; PubMed Central PMCID: PMC1949411.
39. Jin S, Park CO, Shin JU, Noh JY, Lee YS, Lee NR, et al. DAMP molecules S100A9 and S100A8 activated by IL-17A and house-dust mites are increased in atopic dermatitis. Experimental dermatology. 2014;23(12):938-41. doi: 10.1111/exd.12563 PMID: 25308296.
40. Gebhardt C, Breitenbach U, Tuckermann JP, Dittrich BT, Richter KH, Angel P. Calgranulins S100A8 and S100A9 are negatively regulated by glucocorticoids in a c-Fos-dependent manner and overexpressed throughout skin carcinogenesis. Oncogene. 2002;21(27):4266-76. doi: 10.1038/sj.onc. 1205521 PMID: 12082614.
41. Sivaprasad U, Kinker KG, Ericksen MB, Lindsey M, Gibson AM, Bass SA, et al. SERPINB3/B4 contributes to early inflammation and barrier dysfunction in an experimental murine model of atopic dermatitis. The Journal of investigative dermatology. 2015;135(1):160-9. doi: 10.1038/jid.2014.353 PMID: 25111616; PubMed Central PMCID: PMC4268075.
42. Stojadinovic O, Pastar I, Vukelic S, Mahoney MG, Brennan D, Krzyzanowska A, et al. Deregulation of keratinocyte differentiation and activation: a hallmark of venous ulcers. Journal of cellular and molecular medicine. 2008;12(6 B):2675-90. Epub 2008/04/01. doi: 10.1111/j.1582-4934.2008.00321.x PMID: 18373736.
43. Benoit S, Toksoy A, Ahlmann M, Schmidt M, Sunderkotter C, Foell D, et al. Elevated serum levels of calcium-binding S100 proteins A8 and A9 reflect disease activity and abnormal differentiation of keratinocytes in psoriasis. The British journal of dermatology. 2006;155(1):62-6. doi: 10.1111/j.1365-2133. 2006.07198.x PMID: 16792753.
44. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. Journal of leukocyte biology. 2009;86(3):557-66. doi: 10.1189/jlb.1008647 PMID: 19451397.
45. Zhang X, Bedigian AV, Wang W, Eggert US. G protein-coupled receptors participate in cytokinesis. Cytoskeleton. 2012;69(10):810-8. doi: 10.1002/cm.21055 PMID: 22888021; PubMed Central PMCID: PMC4137143.
46. Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A, Han J, et al. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(11):4410-5. doi: 10.1073/pnas.1215927110 PMID: 23401498; PubMed Central PMCID: PMC3600440.
47. Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(28):11452-7. doi: 10.1073/pnas.1106083108 PMID: 21693646; PubMed Central PMCID: PMC3136304.
48. Jaks V, Barker N, Kasper M, Van Es JH, Snippert HJ, Clevers H, et al. Lgr5 marks cycling, yet longlived, hair follicle stem cells. Nature genetics. 2008;40(11):1291-9. doi: 10.1038/ng.239 PMID: 18849992.
49. Haemmerle M, Keller T, Egger G, Schachner H, Steiner CW, Stokic D, et al. Enhanced lymph vessel density, remodeling, and inflammation are reflected by gene expression signatures in dermal lymphatic endothelial cells in type 2 diabetes. Diabetes. 2013;62(7):2509-29. doi: 10.2337/db12-0844 PMID: 23423575; PubMed Central PMCID: PMC3712036.
50. Ge K, Wu JJ, Qian L, Wu MJ, Wang FL, Xu B, et al. Bioinformatic analysis of the effect of type II diabetes on skin wound healing. Genet Mol Res. 2015;14(2):4802-11. doi: 10.4238/2015. May.11.12 PMID: 25966254.
51. Tellechea A, Kafanas A, Leal EC, Tecilazich F, Kuchibhotla S, Auster ME, et al. Increased skin inflammation and blood vessel density in human and experimental diabetes. The international journal of lower extremity wounds. 2013;12(1):4-11. doi: 10.1177/1534734612474303 PMID: 23446362; PubMed Central PMCID: PMC3688045.
52. Lantis JC 2nd, Marston WA, Farber A, Kirsner RS, Zhang Y, Lee TD, et al. The influence of patient and wound variables on healing of venous leg ulcers in a randomized controlled trial of growth-arrested allogeneic keratinocytes and fibroblasts. Journal of vascular surgery. 2013;58(2):433-9. doi: 10.1016/j.jvs.2012.12.055 PMID: 23588112.
53. 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(10):1339-49. doi: 10.4161/15592294.2014.967584 PMID: 25437049.
54. Charles CA, Tomic-Canic M, Vincek V, Nassiri M, Stojadinovic O, Eaglstein WH, et al. A gene signature of nonhealing venous ulcers: potential diagnostic markers. J Am Acad Dermatol. 2008;59(5):758-71. doi: 10.1016/j.jaad.2008.07.018 PMID: 18718692.
55. Harsha A, Stojadinovic O, Brem H, Sehara-Fujisawa A, Wewer U, Loomis CA, et al. ADAM12: a potential target for the treatment of chronic wounds. Journal of molecular medicine. 2008;86(8):961-9. doi: 10.1007/s00109-008-0353-z PMID: 18604515; PubMed Central PMCID: PMC2674959.