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microRNA in Cutaneous Wound Healing

  • Chandan K. Sen
  • Sashwati Roy

Repair of a defect in the human skin is a highly orchestrated physiological process involving numerous factors that act in a temporally resolved synergistic manner to re-establish barrier function by regenerating new skin. The inducible expression and repression of genes represents a key component of this process. MicroRNAs (miRNAs) are powerful regulators of gene expression yet their significance in tissue repair remains largely unknown. Recent estimates suggest that the number of unique miRNA genes in humans exceeds 1000, and may be as high as 20,000. miRNAs are functionally versatile, with the capacity to specifically inhibit translation initiation or elongation, as well as, induce mRNA destabiliza-tion, through predominantly targeting the 3'-untranslated regions of mRNA. In this chapter, we address the potential significance of miRNA in cutaneous wound healing. The following specific areas related to cutaneous wound healing are addressed: skin structure and function, stem cell biology, infection, immunity, inflammation, angiogenesis and extracellular matrix. Furthermore, we discuss opportunities for miRNA-based therapeutics in addressing chronic wounds as a major public health concern in the United States and globally.

wound healing non-coding RNA skin Dicer stem cell infection immunity Inflammation angiogenesis miRNA-based therapeutics 

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References

  1. 1.
    Wasta V and Mehl V Micro-RNA’s function to maintain stem cell phenotype. Cancer Biol Ther 6: 305, 2007.Google Scholar
  2. 2.
    Andl T, Murchison EP, Liu F, Zhang Y, Yunta-Gonzalez M, Tobias JW, Andl CD, Seykora JT, Hannon GJ, and Millar SE. The miRNA-processing enzyme dicer is essential for the morpho-genesis and maintenance of hair follicles. Curr Biol 16: 1041-1049, 2006.CrossRefPubMedGoogle Scholar
  3. 3.
    Bazzini AA, Hopp HE, Beachy RN, and Asurmendi S. Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA 104: 12157-12162, 2007.CrossRefPubMedGoogle Scholar
  4. 4.
    Bernard BA. The biology of hair follicle. J Soc Biol 199: 343-348, 2005. CrossRefPubMedGoogle Scholar
  5. 5.
    Bieniek R, Lazar AJ, Photopoulos C, and Lyle S. Sebaceous tumours contain a subpopulation of cells expressing the keratin 15 stem cell marker. Br J Dermatol 156: 378-380, 2007.CrossRefPubMedGoogle Scholar
  6. 6.
    Brandvold KA, Neiman P, and Ruddell A. Angiogenesis is an early event in the generation of myc-induced lymphomas. Oncogene 19: 2780-2785, 2000.CrossRefPubMedGoogle Scholar
  7. 7.
    Branski LK, Pereira CT, Herndon DN, and Jeschke MG. Gene therapy in wound healing: present status and future directions. Gene Ther 14: 1-10, 2007.CrossRefPubMedGoogle Scholar
  8. 8.
    Broughton G, 2nd, Janis JE, and Attinger CE. The basic science of wound healing. Plast Reconstr Surg 117: 12S-34S, 2006.CrossRefPubMedGoogle Scholar
  9. 9.
    Broughton G, 2nd, Janis JE, and Attinger CE. Wound healing: an overview. Plast Reconstr Surg 117: 1e-S-32e-S, 2006.CrossRefPubMedGoogle Scholar
  10. 10.
    Brown BD, Venneri MA, Zingale A, Sergi Sergi L, and Naldini L. Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med 12: 585-591, 2006.CrossRefPubMedGoogle Scholar
  11. 11.
    Carrington JC and Ambros V. Role of microRNAs in plant and animal development. Science 301: 336-338, 2003.CrossRefPubMedGoogle Scholar
  12. 12.
    Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, and Shah AM. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 8: 691-728, 2006.CrossRefPubMedGoogle Scholar
  13. 13.
    Chen CZ, Li L, Lodish HF, and Bartel DP. MicroRNAs modulate hematopoietic lineage dif-ferentiation. Science 303: 83-86, 2004.CrossRefPubMedGoogle Scholar
  14. 14.
    Chen CZ and Lodish HF. MicroRNAs as regulators of mammalian hematopoiesis. Semin Immunol 17: 155-165, 2005.CrossRefPubMedGoogle Scholar
  15. 15.
    Croce CM and Calin GA. miRNAs, cancer, and stem cell division. Cell 122: 6-7, 2005.CrossRefPubMedGoogle Scholar
  16. 16.
    Cullen BR. Immunology. Outwitted by viral RNAs. Science 317: 329-330, 2007.CrossRefPubMedGoogle Scholar
  17. 17.
    Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, and Thomas-Tikhonenko A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38: 1060-1065, 2006.CrossRefPubMedGoogle Scholar
  18. 18.
    Dunoyer P, Himber C, and Voinnet O. Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nat Genet 38: 258-263, 2006.CrossRefPubMedGoogle Scholar
  19. 19.
    Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, Watts L, Booten SL, Graham M, McKay R, Subramaniam A, Propp S, Lollo BA, Freier S, Bennett CF, Bhanot S, and Monia BP. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3: 87-98, 2006.CrossRefPubMedGoogle Scholar
  20. 20.
    Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F, Liuzzi F, Lulli V, Morsilli O, Santoro S, Valtieri M, Calin GA, Liu CG, Sorrentino A, Croce CM, and Peschle C. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci USA 102: 18081-18086, 2005.CrossRefPubMedGoogle Scholar
  21. 21.
    Fontana L, Pelosi E, Greco P, Racanicchi S, Testa U, Liuzzi F, Croce CM, Brunetti E, Grignani F, and Peschle C. MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 9: 775-787, 2007.CrossRefPubMedGoogle Scholar
  22. 22.
    Fritz JH, Girardin SE, and Philpott DJ. Innate immune defense through RNA interference. Sci STKE 2006: pe27, 2006.CrossRefGoogle Scholar
  23. 23.
    Gantier MP, Sadler AJ, and Williams BR. Fine-tuning of the innate immune response by microRNAs. Immunol Cell Biol 85: 458-462, 2007.CrossRefPubMedGoogle Scholar
  24. 24.
    Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, Volinia S, Bhatt D, Alder H, Marcucci G, Calin GA, Liu CG, Bloomfield CD, Andreeff M, and Croce CM. MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA 103: 5078-5083, 2006.CrossRefPubMedGoogle Scholar
  25. 25.
    Georgantas RW, 3rd, Hildreth R, Morisot S, Alder J, Liu CG, Heimfeld S, Calin GA, Croce CM, and Civin CI. CD34+ hematopoietic stem-progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci USA 104: 2750-2755, 2007.CrossRefPubMedGoogle Scholar
  26. 26.
    Goldberg S, Roy S, Khanna S, and Sen CK. Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Atheroscler Thromb Vasc Biol 28: 471-477, 2008.CrossRefGoogle Scholar
  27. 27.
    Goodrich JA and Kugel JF. Non-coding-RNA regulators of RNA polymerase II transcription. Nat Rev Mol Cell Biol 7: 612-616, 2006.CrossRefPubMedGoogle Scholar
  28. 28.
    Gu J and Iyer VR. PI3K signaling and miRNA expression during the response of quiescent human fibroblasts to distinct proliferative stimuli. Genome Biol 7: R42, 2006.CrossRefPubMedGoogle Scholar
  29. 29.
    Harvey C. Wound healing. Orthop Nurs 24: 143-157; quiz 158-149, 2005.Google Scholar
  30. 30.
    Hatfield SD, Shcherbata HR, Fischer KA, Nakahara K, Carthew RW, and Ruohola-Baker H. Stem cell division is regulated by the microRNA pathway. Nature 435: 974-978, 2005.CrossRefPubMedGoogle Scholar
  31. 31.
    Healy B. Skin deep. As the body’s largest organ, skin is a powerful yet unappreciated veneer. US News World Rep 139: 66-68, 2005.PubMedGoogle Scholar
  32. 32.
    Kanitakis J. Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol 12: 390-399; quiz 400-391, 2002.Google Scholar
  33. 33.
    Kanzaki LI, Ornelas SS, and Arganaraz ER. RNA interference and HIV-1 infection. Rev Med Virol, 18: 5-18, 2008.CrossRefPubMedGoogle Scholar
  34. 34.
    Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, and Natarajan R. MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhi-bition of E-box repressors. Proc Natl Acad Sci USA 104: 3432-3437, 2007.CrossRefPubMedGoogle Scholar
  35. 35.
    Khabar KS. Rapid transit in the immune cells: the role of mRNA turnover regulation. J Leukoc Biol 81: 1335-1344, 2007.CrossRefPubMedGoogle Scholar
  36. 36.
    Kruger J and Rehmsmeier M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 34: W451-W454, 2006.CrossRefPubMedGoogle Scholar
  37. 37.
    Krutzfeldt J, Poy MN, and Stoffel M. Strategies to determine the biological function of micro-RNAs. Nat Genet 38 (Suppl): S14-S19, 2006.CrossRefPubMedGoogle Scholar
  38. 38.
    Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, and Stoffel M. Silencing of microRNAs in vivo with ‘antagomirs’. Nature 438: 685-689, 2005.CrossRefPubMedGoogle Scholar
  39. 39.
    Kuehbacher A, Urbich C, Zeiher AM, and Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 101: 59-68, 2007.CrossRefPubMedGoogle Scholar
  40. 40.
    Kuehn BM. Chronic wound care guidelines issued. Jama 297: 938-939, 2007.CrossRefPubMedGoogle Scholar
  41. 41.
    Lavker RM, Sun TT, Oshima H, Barrandon Y, Akiyama M, Ferraris C, Chevalier G, Favier B, Jahoda CA, Dhouailly D, Panteleyev AA, and Christiano AM. Hair follicle stem cells. J Investig Dermatol Symp Proc 8: 28-38, 2003.CrossRefPubMedGoogle Scholar
  42. 42.
    Lewis BP, Burge CB, and Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20, 2005.CrossRefPubMedGoogle Scholar
  43. 43.
    Li QJ, Chau J, Ebert PJ, Sylvester G, Min H, Liu G, Braich R, Manoharan M, Soutschek J, Skare P, Klein LO, Davis MM, and Chen CZ. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129: 147-161, 2007.CrossRefPubMedGoogle Scholar
  44. 44.
    Lingen MW. Role of leukocytes and endothelial cells in the development of angiogenesis in inflammation and wound healing. Arch Pathol Lab Med 125: 67-71, 2001.PubMedGoogle Scholar
  45. 45.
    Litz J and Krystal GW. Imatinib inhibits c-Kit-induced hypoxia-inducible factor-1alpha activ-ity and vascular endothelial growth factor expression in small cell lung cancer cells. Mol Cancer Ther 5: 1415-1422, 2006.CrossRefPubMedGoogle Scholar
  46. 46.
    Ma DR, Yang EN, and Lee ST. A review: the location, molecular characterisation and multipo-tency of hair follicle epidermal stem cells. Ann Acad Med Singapore 33: 784-788, 2004.PubMedGoogle Scholar
  47. 47.
    Mattick JS and Makunin IV. Non-coding RNA. Hum Mol Genet 15 Spec No 1: R17-R29, 2006.CrossRefGoogle Scholar
  48. 48.
    Meng F, Henson R, Wehbe-Janek H, Smith H, Ueno Y, and Patel T. The MicroRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangi-ocytes. J Biol Chem 282: 8256-8264, 2007.CrossRefPubMedGoogle Scholar
  49. 49.
    Meng F, Wehbe-Janek H, Henson R, Smith H, and Patel T. Epigenetic regulation of microRNA-370 by interleukin-6 in malignant human cholangiocytes. Oncogene, 27: 378-386, 2007.CrossRefPubMedGoogle Scholar
  50. 50.
    Moffett HF and Novina CD. A small microRNA makes a Big difference. Genome Biol 8: 221, 2007.CrossRefPubMedGoogle Scholar
  51. 51.
    Monticelli S, Ansel KM, Xiao C, Socci ND, Krichevsky AM, Thai TH, Rajewsky N, Marks DS, Sander C, Rajewsky K, Rao A, and Kosik KS. MicroRNA profiling of the murine hemat-opoietic system. Genome Biol 6: R71, 2005.CrossRefPubMedGoogle Scholar
  52. 52.
    Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, and Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysac- charide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 8: 240, 2007.CrossRefPubMedGoogle Scholar
  53. 53.
    Muller S and Imler JL. Dicing with viruses: microRNAs as antiviral factors. Immunity 27: 1-3, 2007.CrossRefPubMedGoogle Scholar
  54. 54.
    Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M, Hui CC, Clevers H, Dotto GP, and Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 33: 416-421, 2003.CrossRefPubMedGoogle Scholar
  55. 55.
    O’Connell RM, Taganov KD, Boldin MP, Cheng G, and Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 104: 1604-1609, 2007.CrossRefPubMedGoogle Scholar
  56. 56.
    O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, and Mendell JT. c-Myc-regulated microR-NAs modulate E2F1 expression. Nature 435: 839-843, 2005.CrossRefPubMedGoogle Scholar
  57. 57.
    Otsuka M, Jing Q, Georgel P, New L, Chen J, Mols J, Kang YJ, Jiang Z, Du X, Cook R, Das SC, Pattnaik AK, Beutler B, and Han J. Hypersusceptibility to vesicular stomatitis virus infec-tion in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27: 123-134, 2007.CrossRefPubMedGoogle Scholar
  58. 58.
    Perera RJ and Ray A. MicroRNAs in the search for understanding human diseases. BioDrugs 21: 97-104, 2007.CrossRefPubMedGoogle Scholar
  59. 59.
    Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, and Rainaldi G. MicroRNAs modulate the angiogenic properties of HUVEC. Blood 108: 3068-3071, 2006.CrossRefPubMedGoogle Scholar
  60. 60.
    Proweller A, Tu L, Lepore JJ, Cheng L, Lu MM, Seykora J, Millar SE, Pear WS, and Parmacek MS. Impaired notch signaling promotes de novo squamous cell carcinoma forma-tion. Cancer Res 66: 7438-7444, 2006.CrossRefPubMedGoogle Scholar
  61. 61.
    Racz Z and Hamar P. Can siRNA technology provide the tools for gene therapy of the future? Curr Med Chem 13: 2299-2307, 2006.CrossRefPubMedGoogle Scholar
  62. 62.
    Raftopoulou M. microRNA signals cell fate. Nat Cell Biol 8: 112, 2006.CrossRefPubMedGoogle Scholar
  63. 63.
    Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, Pfeffer S, Landthaler M, Landgraf P, Kan S, Lindenbach BD, Chien M, Weir DB, Russo JJ, Ju J, Brownstein MJ, Sheridan R, Sander C, Zavolan M, Tuschl T, and Rice CM. Cellular cofactors affecting hepa-titis C virus infection and replication. Proc Natl Acad Sci USA 104: 12884-12889, 2007.CrossRefPubMedGoogle Scholar
  64. 64.
    Ro S, Park C, Young D, Sanders KM, and Yan W. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 35: 5944-5953, 2007.CrossRefPubMedGoogle Scholar
  65. 65.
    Roboz GJ, Giles FJ, List AF, Cortes JE, Carlin R, Kowalski M, Bilic S, Masson E, Rosamilia M, Schuster MW, Laurent D, and Feldman EJ. Phase 1 study of PTK787/ZK 222584, a small molecule tyrosine kinase receptor inhibitor, for the treatment of acute myeloid leukemia and myelodysplastic syndrome. Leukemia 20: 952-957, 2006.CrossRefPubMedGoogle Scholar
  66. 66.
    Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, and Bradley A. Requirement of bic/microRNA-155 for normal immune function. Science 316: 608-611, 2007.CrossRefPubMedGoogle Scholar
  67. 67.
    Ross FP and Christiano AM. Nothing but skin and bone. J Clin Invest 116: 1140-1149, 2006.CrossRefPubMedGoogle Scholar
  68. 68.
    Roy S, Khanna S, Nallu K, Hunt TK, and Sen CK. Dermal wound healing is subject to redox control. Mol Ther 13: 211-220, 2006.CrossRefPubMedGoogle Scholar
  69. 69.
    Schouwey K, Delmas V, Larue L, Zimber-Strobl U, Strobl LJ, Radtke F, and Beermann F. Notch1 and Notch2 receptors influence progressive hair graying in a dose-dependent manner. Dev Dyn 236: 282-289, 2007.CrossRefPubMedGoogle Scholar
  70. 70.
    Segre J. Complex redundancy to build a simple epidermal permeability barrier. Curr Opin Cell Biol 15: 776-782, 2003.CrossRefPubMedGoogle Scholar
  71. 71.
    Segre JA. Epidermal barrier formation and recovery in skin disorders. J Clin Invest 116: 1150-1158, 2006.CrossRefPubMedGoogle Scholar
  72. 72.
    Sen CK. The general case for redox control of wound repair. Wound Repair Regen 11: 431-438, 2003.CrossRefPubMedGoogle Scholar
  73. 73.
    Sen CK, Khanna S, Babior BM, Hunt TK, Ellison EC, and Roy S. Oxidant-induced vascular endothelial growth factor expression in human keratinocytes and cutaneous wound healing. J Biol Chem 277: 33284-33290, 2002. CrossRefPubMedGoogle Scholar
  74. 74.
    Shi Y, Sun G, Zhao C, and Stewart R. Neural stem cell self-renewal. Crit Rev Oncol Hematol’ 65: 43-53, 2008.CrossRefPubMedGoogle Scholar
  75. 75.
    Smalheiser NR and Torvik VI. Complications in mammalian microRNA target prediction. Methods Mol Biol 342: 115-127, 2006.PubMedGoogle Scholar
  76. 76.
    Soifer HS, Rossi JJ, and Saetrom P. MicroRNAs in disease and potential therapeutic applica-tions. Mol Ther 15: 2070-2079, 2007.CrossRefPubMedGoogle Scholar
  77. 77.
    Song L and Tuan RS. MicroRNAs and cell differentiation in mammalian development. Birth Defects Res C Embryo Today 78: 140-149, 2006.CrossRefPubMedGoogle Scholar
  78. 78.
    Sonkoly E, Wei T, Janson PC, Saaf A, Lundeberg L, Tengvall-Linder M, Norstedt G, Alenius H, Homey B, Scheynius A, Stahle M, and Pivarcsi A. MicroRNAs: novel regulators involved in the pathogenesis of Psoriasis? PLoS ONE 2: e610, 2007.CrossRefPubMedGoogle Scholar
  79. 79.
    Sood P, Krek A, Zavolan M, Macino G, and Rajewsky N. Cell-type-specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci USA 103: 2746-2751, 2006.CrossRefPubMedGoogle Scholar
  80. 80.
    Stenn KS. Molecular insights into the hair follicle and its pathology: a review of recent devel-opments. Int J Dermatol 42: 40-43, 2003.CrossRefPubMedGoogle Scholar
  81. 81.
    Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, Horwitz E, Prokocimer Z, Prichard M, Hahn G, Goldman-Wohl D, Greenfield C, Yagel S, Hengel H, Altuvia Y, Margalit H, and Mandelboim O. Host immune system gene targeting by a viral miRNA. Science 317: 376-381, 2007.CrossRefPubMedGoogle Scholar
  82. 82.
    Strumberg D. Preclinical and clinical development of the oral multikinase inhibitor sorafenib in cancer treatment. Drugs Today (Barc) 41: 773-784, 2005.CrossRefGoogle Scholar
  83. 83.
    Suarez Y, Fernandez-Hernando C, Pober JS, and Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 100: 1164-1173, 2007.CrossRefPubMedGoogle Scholar
  84. 84.
    Taganov KD, Boldin MP, and Baltimore D. MicroRNAs and immunity: tiny players in a big field. Immunity 26: 133-137, 2007.CrossRefPubMedGoogle Scholar
  85. 85.
    Tang G. siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30: 106-114, 2005.CrossRefPubMedGoogle Scholar
  86. 86.
    Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, Fabbri M, Alder H, Liu CG, Calin GA, and Croce CM. Modulation of miR-155 and miR-125b Levels following Lipopolysaccharide/TNF-{alpha} stimulation and their possible roles in regulating the vre-sponse to endotoxin shock. J Immunol 179: 5082-5089, 2007.PubMedGoogle Scholar
  87. 87.
    Tomaru Y and Hayashizaki Y. Cancer research with non-coding RNA. Cancer Sci 97: 1285-1290, 2006.CrossRefPubMedGoogle Scholar
  88. 88.
    Ushio-Fukai M. VEGF signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 9: 731-739, 2007.CrossRefPubMedGoogle Scholar
  89. 89.
    Vauclair S, Nicolas M, Barrandon Y, and Radtke F. Notch1 is essential for postnatal hair folli-cle development and homeostasis. Dev Biol 284: 184-193, 2005.CrossRefPubMedGoogle Scholar
  90. 90.
    Weiler J, Hunziker J, and Hall J. Anti-miRNA oligonucleotides (AMOs): ammunition to tar-get miRNAs implicated in human disease? Gene Ther 13: 496-502, 2006.CrossRefPubMedGoogle Scholar
  91. 91.
    Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, and Zhao G. Dicer is required for embry-onic angiogenesis during mouse development. J Biol Chem 280: 9330-9335, 2005.CrossRefPubMedGoogle Scholar
  92. 92.
    Yang Z and Wu J. MicroRNAs and regenerative medicine. DNA Cell Biol 26: 257-264, 2007.CrossRefPubMedGoogle Scholar
  93. 93.
    Yi R, O’Carroll D, Pasolli HA, Zhang Z, Dietrich FS, Tarakhovsky A, and Fuchs E. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat Genet 38: 356-362, 2006.CrossRefPubMedGoogle Scholar
  94. 94.
    Yi R, Qin Y, Macara IG, and Cullen BR. Exportin-5 mediates the nuclear export of pre-micro-RNAs and short hairpin RNAs. Genes Dev 17: 3011-3016, 2003.CrossRefPubMedGoogle Scholar
  95. 95.
    Zavadil J, Narasimhan M, Blumenberg M, and Schneider RJ. Transforming growth factor-beta and microRNA:mRNA regulatory networks in epithelial plasticity. Cells Tissues Organs 185: 157-161, 2007.CrossRefPubMedGoogle Scholar
  96. 96.
    Zhao Y, Samal E, and Srivastava D. Serum response factor regulates a muscle-specific micro-RNA that targets Hand2 during cardiogenesis. Nature 436: 214-220, 2005.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Chandan K. Sen
    • 1
  • Sashwati Roy
    • 1
  1. 1.Laboratory of Molecular Medicine, Department of Surgery, 512 Davis Heart and Lung Research InstituteThe Ohio State University Medical CenterColumbusUSA

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