Advertisement

Long Noncoding RNA and Its Role in the Control of Gene Expression in the Skin

  • Kevin C. Wang
  • Howard Y. ChangEmail author
Chapter
  • 391 Downloads
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Epithelial tissues in animals regulate life-sustaining processes at the boundary between the host and its environment. It is becoming evident that regulatory noncoding RNAs play fundamental roles in orchestrating the formation of the skin, including lineage-specific commitment and specialization, often operating at the interface between stemness and differentiation. In this review, we discuss the current understanding of how members of a specific class of RNAs, long noncoding RNAs (lncRNAs), function in the control of gene expression to regulate development and adult stem cell maintenance in the skin. Understanding the activities of lncRNAs will elucidate a novel mechanism that modulates gene expression in the skin, and could ultimately lead to targeted noncoding RNA-based therapies to improve effectiveness of current regenerative strategies and provide new avenues for repair.

Keywords

Noncoding RNA Epithelial development Chromatin Histone modifications Gene regulation 

References

  1. 1.
    Blanpain C, Horsley V, Fuchs E. Epithelial stem cells: turning over new leaves. Cell. 2007;128:445–58.  https://doi.org/10.1016/j.cell.2007.01.014.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Millington GWM. Epigenetics and dermatological disease. Pharmacogenomics. 2008;9:1835–50.  https://doi.org/10.2217/14622416.9.12.1835.CrossRefPubMedGoogle Scholar
  3. 3.
    Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25:1915–27.  https://doi.org/10.1101/gad.17446611.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest ARR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Gatta Della G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SPT, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schönbach C, Sekiguchi K, Semple CAM, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y, FANTOM Consortium, RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group). The transcriptional landscape of the mammalian genome. Science. 2005;309:1559–63.  https://doi.org/10.1126/science.1112014.
  5. 5.
    Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458:223–7.  https://doi.org/10.1038/nature07672.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106:11667–72.  https://doi.org/10.1073/pnas.0904715106.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136:629–41.  https://doi.org/10.1016/j.cell.2009.02.006.CrossRefPubMedGoogle Scholar
  8. 8.
    Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Röder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See L-H, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigo R, Gingeras TR. Landscape of transcription in human cells. Nature. 2012;489:101–8.  https://doi.org/10.1038/nature11233.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009;10:155–9.  https://doi.org/10.1038/nrg2521.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Clark MB, Mattick JS. Long noncoding RNAs in cell biology. Semin Cell Dev Biol. 2011;22:366–76.  https://doi.org/10.1016/j.semcdb.2011.01.001.CrossRefPubMedGoogle Scholar
  11. 11.
    Mattick JS, Amaral PP, Dinger ME, Mercer TR, Mehler MF. RNA regulation of epigenetic processes. BioEssays. 2009;31:51–9.  https://doi.org/10.1002/bies.080099.CrossRefPubMedGoogle Scholar
  12. 12.
    Nagano T, Fraser P. No-nonsense functions for long noncoding RNAs. Cell. 2011;145:178–81.  https://doi.org/10.1016/j.cell.2011.03.014.CrossRefPubMedGoogle Scholar
  13. 13.
    Wang KCK, Chang HYH. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011;43:904–14.  https://doi.org/10.1016/j.molcel.2011.08.018.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bernstein E, Allis CD. RNA meets chromatin. Genes Dev. 2005;19:1635–55.  https://doi.org/10.1101/gad.1324305.CrossRefPubMedGoogle Scholar
  15. 15.
    Bracken AP, Helin K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer. 2009;9:773–84.  https://doi.org/10.1038/nrc2736.CrossRefPubMedGoogle Scholar
  16. 16.
    Faghihi MA, Wahlestedt C. Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol. 2009;10:637–43.  https://doi.org/10.1038/nrm2738.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Whitehead J, Pandey GK, Kanduri C. Regulation of the mammalian epigenome by long noncoding RNAs. Biochim Biophys Acta. 2009;1790:936–47.  https://doi.org/10.1016/j.bbagen.2008.10.007.CrossRefPubMedGoogle Scholar
  18. 18.
    Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009;23:1494–504.  https://doi.org/10.1101/gad.1800909.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. Non-coding RNAs: regulators of disease. J Pathol. 2010;220:126–39.  https://doi.org/10.1002/path.2638.CrossRefPubMedGoogle Scholar
  20. 20.
    Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145–66.  https://doi.org/10.1146/annurev-biochem-051410-092902.CrossRefPubMedGoogle Scholar
  21. 21.
    Qureshi IA, Mattick JS, Mehler MF. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010;1338:20–35.  https://doi.org/10.1016/j.brainres.2010.03.110.CrossRefPubMedGoogle Scholar
  22. 22.
    Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol. 2011;21:354–61.  https://doi.org/10.1016/j.tcb.2011.04.001.CrossRefPubMedGoogle Scholar
  23. 23.
    Paul J, Duerksen JD. Chromatin-associated RNA content of heterochromatin and euchromatin. Mol Cell Biochem. 1975;9:9–16.CrossRefPubMedGoogle Scholar
  24. 24.
    Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315–26.  https://doi.org/10.1016/j.cell.2006.02.041.CrossRefPubMedGoogle Scholar
  25. 25.
    Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell. 2008;32:232–46.  https://doi.org/10.1016/j.molcel.2008.08.022.CrossRefPubMedGoogle Scholar
  26. 26.
    Rodríguez-Campos A, Azorín F. RNA is an integral component of chromatin that contributes to its structural organization. PLoS One. 2007;2:e1182.  https://doi.org/10.1371/journal.pone.0001182.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Clemson CM, McNeil JA, Willard HF, Lawrence JB. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol. 1996;132:259–75.CrossRefPubMedGoogle Scholar
  28. 28.
    Muchardt C, Guilleme M, Seeler J-S, Trouche D, Dejean A, Yaniv M. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 2002;3:975–81.  https://doi.org/10.1093/embo-reports/kvf194.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Majewski IJ, Blewitt ME, de Graaf CA, McManus EJ, Bahlo M, Hilton AA, Hyland CD, Smyth GK, Corbin JE, Metcalf D, Alexander WS, Hilton DJ. Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity. PLoS Biol. 2008;6:e93.  https://doi.org/10.1371/journal.pbio.0060093.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Spivakov M, Fisher AG. Epigenetic signatures of stem-cell identity. Nat Rev Genet. 2007;8:263–71.  https://doi.org/10.1038/nrg2046.CrossRefPubMedGoogle Scholar
  31. 31.
    Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell. 2007;128:747–62.  https://doi.org/10.1016/j.cell.2007.02.010.CrossRefPubMedGoogle Scholar
  32. 32.
    Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell. 2007;128:735–45.  https://doi.org/10.1016/j.cell.2007.02.009.CrossRefPubMedGoogle Scholar
  33. 33.
    Schwartz YB, Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet. 2007;8:9–22.  https://doi.org/10.1038/nrg1981.CrossRefPubMedGoogle Scholar
  34. 34.
    Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su I-H, Hannon G, Tarakhovsky A, Fuchs E. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell. 2009;136:1122–35.  https://doi.org/10.1016/j.cell.2008.12.043.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 2006;441:349–53.  https://doi.org/10.1038/nature04733.CrossRefPubMedGoogle Scholar
  36. 36.
    Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol Cell Biol. 2007;27:3769–79.  https://doi.org/10.1128/MCB.01432-06.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Chang HY, Chi J-T, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A. 2002;99:12877–82.  https://doi.org/10.1073/pnas.162488599.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Chi J-T, Chang HY, Wang NN, Chang DS, Dunphy N, Brown PO. Genomewide view of gene silencing by small interfering RNAs. Proc Natl Acad Sci U S A. 2003;100:6343–6.  https://doi.org/10.1073/pnas.1037853100.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Rinn JL, Bondre C, Gladstone HB, Brown PO, Chang HY. Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS Genet. 2006;2:e119.  https://doi.org/10.1371/journal.pgen.0020119.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Wang KC, Helms JA, Chang HY. Regeneration, repair and remembering identity: the three Rs of Hox gene expression. Trends Cell Biol. 2009;19:268–75.  https://doi.org/10.1016/j.tcb.2009.03.007.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lemons D, McGinnis W. Genomic evolution of Hox gene clusters. Science. 2006;313:1918–22.  https://doi.org/10.1126/science.1132040.CrossRefPubMedGoogle Scholar
  42. 42.
    Rinn JL, Wang JK, Allen N, Brugmann SA, Mikels AJ, Liu H, Ridky TW, Stadler HS, Nusse R, Helms JA, Chang HY. A dermal HOX transcriptional program regulates site-specific epidermal fate. Genes Dev. 2008;22:303–7.  https://doi.org/10.1101/gad.1610508.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 2007;129:1311–23.  https://doi.org/10.1016/j.cell.2007.05.022.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011;472:120–4.  https://doi.org/10.1038/nature09819.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Amaral PP, Neyt C, Wilkins SJ, Askarian-Amiri ME, Sunkin SM, Perkins AC, Mattick JS. Complex architecture and regulated expression of the Sox2ot locus during vertebrate development. RNA. 2009;15:2013–27.  https://doi.org/10.1261/rna.1705309.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Araki R, Fukumura R, Sasaki N, Kasama Y, Suzuki N, Takahashi H, Tabata Y, Saito T, Abe M. More than 40,000 transcripts, including novel and noncoding transcripts, in mouse embryonic stem cells. Stem Cells. 2006;24:2522–8.  https://doi.org/10.1634/stemcells.2006-0005.CrossRefPubMedGoogle Scholar
  47. 47.
    Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, Grimmond SM, Perkins AC, Mattick JS. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008;18:1433–45.  https://doi.org/10.1101/gr.078378.108.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A. 2008;105:716–21.  https://doi.org/10.1073/pnas.0706729105.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Pang KC, Dinger ME, Mercer TR, Malquori L, Grimmond SM, Chen W, Mattick JS. Genome-wide identification of long noncoding RNAs in CD8+ T cells. J Immunol. 2009;182:7738–48.  https://doi.org/10.4049/jimmunol.0900603.CrossRefPubMedGoogle Scholar
  50. 50.
    Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature. 2009;461:762–7.  https://doi.org/10.1038/nature08398.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Li L, Liu B, Wapinski OL, Tsai M-C, Qu K, Zhang J, Carlson JC, Lin M, Fang F, Gupta RA, Helms JA, Chang HY. Targeted disruption of hotair leads to homeotic transformation and gene derepression. Cell Rep. 2013;5:3–12.  https://doi.org/10.1016/j.celrep.2013.09.003.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai M-C, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010;464:1071–6.  https://doi.org/10.1038/nature08975.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell. 2010;40:939–53.  https://doi.org/10.1016/j.molcel.2010.12.011.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Sanyal A, Baù D, Martí-Renom MA, Dekker J. Chromatin globules: a common motif of higher order chromosome structure? Curr Opin Cell Biol. 2011;23:325–31.  https://doi.org/10.1016/j.ceb.2011.03.009.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Lupiáñez DG, Spielmann M, Mundlos S. Breaking TADs: how alterations of chromatin domains result in disease. Trends Genet. 2016;32:225–37.  https://doi.org/10.1016/j.tig.2016.01.003.CrossRefPubMedGoogle Scholar
  56. 56.
    Hu W, Dominguez JRA, Lodish HF. Regulation of mammalian cell differentiation by long non-coding RNAs. EMBO Rep. 2012;13:971–83.  https://doi.org/10.1038/embor.2012.145.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Yi R, Fuchs E. A miR image of stem cells and their lineages. Curr Top Dev Biol. 2012;99:175–99.  https://doi.org/10.1016/B978-0-12-387038-4.00007-0.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kretz M, Webster DE, Flockhart RJ, Lee CS, Zehnder A, Lopez-Pajares V, Qu K, Zheng GXY, Chow J, Kim GE, Rinn JL, Chang HY, Siprashvili Z, Khavari PA. Suppression of progenitor differentiation requires the long noncoding RNA ANCR. Genes Dev. 2012;26:338–43.  https://doi.org/10.1101/gad.182121.111.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature. 2011;477:295–300.  https://doi.org/10.1038/nature10398.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Kretz M, Siprashvili Z, Chu C, Webster DE, Zehnder A, Qu K, Lee CS, Flockhart RJ, Groff AF, Chow J, Johnston D, Kim GE, Spitale RC, Flynn RA, Zheng GXY, Aiyer S, Raj A, Rinn JL, Chang HY, Khavari PA. Control of somatic tissue differentiation by the long non-coding RNA TINCR. Nature. 2013;493:231–5.  https://doi.org/10.1038/nature11661.CrossRefPubMedGoogle Scholar
  61. 61.
    Lopez-Pajares V, Qu K, Zhang J, Webster DE, Barajas BC, Siprashvili Z, Zarnegar BJ, Boxer LD, Rios EJ, Tao S, Kretz M, Khavari PA. A LncRNA-MAF:MAFB transcription factor network regulates epidermal differentiation. Dev Cell. 2015;32:693–706.  https://doi.org/10.1016/j.devcel.2015.01.028.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou M-M. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010;38:662–74.  https://doi.org/10.1016/j.molcel.2010.03.021.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Pasmant E, Sabbagh A, Vidaud M, Bièche I. ANRIL, a long, noncoding RNA, is an unexpected major hotspot in GWAS. FASEB J. 2011;25:444–8.  https://doi.org/10.1096/fj.10-172452.CrossRefPubMedGoogle Scholar
  64. 64.
    Khaitan D, Dinger ME, Mazar J, Crawford J, Smith MA, Mattick JS, Perera RJ. The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Res. 2011;71:3852–62.  https://doi.org/10.1158/0008-5472.CAN-10-4460.CrossRefPubMedGoogle Scholar
  65. 65.
    Flockhart RJ, Webster DE, Qu K, Mascarenhas N, Kovalski J, Kretz M, Khavari PA. BRAFV600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res. 2012;22:1006–14.  https://doi.org/10.1101/gr.140061.112.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Lee CS, Ungewickell A, Bhaduri A, Qu K, Webster DE, Armstrong R, Weng WK, Aros CJ, Mah A, Chen RO, Lin M, Sundram U, Chang HY, Kretz M, Kim YH, Khavari PA. Transcriptome sequencing in Sezary syndrome identifies Sezary cell and mycosis fungoides-associated LncRNAs and novel transcripts. Blood. 2012;120:3288.  https://doi.org/10.1182/blood-2012-04-423061.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Sonkoly E, Bata-Csörgő Z, Pivarcsi A, Polyanka H, Kenderessy-Szabo A, Molnar G, Szentpali K, Bari L, Megyeri K, Mandi Y, Dobozy A, Kemény L, Széll M. Identification and characterization of a novel, psoriasis susceptibility-related noncoding RNA gene, PRINS. J Biol Chem. 2005;280:24159–67.  https://doi.org/10.1074/jbc.M501704200.CrossRefPubMedGoogle Scholar
  68. 68.
    Tsoi LC, Iyer MK, Stuart PE, Swindell WR, Gudjonsson JE, Tejasvi T, Sarkar MK, Li B, Ding J, Voorhees JJ, Kang HM, Nair RP, Chinnaiyan AM, Abecasis GR, Elder JT. Analysis of long non-coding RNAs highlights tissue-specific expression patterns and epigenetic profiles in normal and psoriatic skin. Genome Biol. 2015;16:24.  https://doi.org/10.1186/s13059-014-0570-4.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, Martinez L, Greidinger EL, Yu BD, Gallo RL. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med. 2012;18:1286–90.  https://doi.org/10.1038/nm.2861.CrossRefPubMedGoogle Scholar
  70. 70.
    Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, Wang Y, Kong B, Langerød A, Børresen-Dale A-L, Kim SK, van de Vijver M, Sukumar S, Whitfield ML, Kellis M, Xiong Y, Wong DJ, Chang HY. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet. 2011;43:621.  https://doi.org/10.1038/ng.848.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Schmitt AM, Garcia JT, Hung T, Flynn RA, Shen Y, Qu K, Payumo AY, Peres-da-Silva A, Broz DK, Baum R, Guo S, Chen JK, Attardi LD, Chang HY. An inducible long noncoding RNA amplifies DNA damage signaling. Nat Genet. 2016;48:1370–6.  https://doi.org/10.1038/ng.3673.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Chang ALS, Bitter PH, Qu K, Lin M, Rapicavoli NA, Chang HY. Rejuvenation of gene expression pattern of aged human skin by broadband light treatment: a pilot study. J Invest Dermatol. 2013;133:394–402.  https://doi.org/10.1038/jid.2012.287.CrossRefPubMedGoogle Scholar
  73. 73.
    Sand M, Bechara FG, Sand D, Gambichler T, Hahn SA, Bromba M, Stockfleth E, Hessam S. Long-noncoding RNAs in basal cell carcinoma. Tumour Biol. 2016;37:10595–608.  https://doi.org/10.1007/s13277-016-4927-z.CrossRefPubMedGoogle Scholar
  74. 74.
    Wang S, Fan W, Wan B, Tu M, Jin F, Liu F, Xu H, Han P. Characterization of long noncoding RNA and messenger RNA signatures in melanoma tumorigenesis and metastasis. PLoS One. 2017;12:e0172498.  https://doi.org/10.1371/journal.pone.0172498.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Piipponen M, Nissinen L, Farshchian M, Riihilä P, Kivisaari A, Kallajoki M, Peltonen J, Peltonen S, Kähäri V-M. Long noncoding RNA PICSAR promotes growth of cutaneous squamous cell carcinoma by regulating ERK1/2 activity. J Invest Dermatol. 2016;136:1701–10.  https://doi.org/10.1016/j.jid.2016.03.028.CrossRefPubMedGoogle Scholar
  76. 76.
    Ponzio G, Rezzonico R, Bourget I, Allan R, Nottet N, Popa A, Magnone V, Rios G, Mari B, Barbry P. A new long noncoding RNA (LncRNA) is induced in cutaneous squamous cell carcinoma and downregulates several anticancer and cell-differentiation genes in mouse. J Biol Chem. 2017.  https://doi.org/10.1074/jbc.M117.776260.
  77. 77.
    Wang Z, Jinnin M, Nakamura K, Harada M, Kudo H, Nakayama W, Inoue K, Nakashima T, Honda N, Fukushima S, Ihn H. Long non-coding RNA TSIX is upregulated in scleroderma dermal fibroblasts and controls collagen mRNA stabilization. Exp Dermatol. 2016;25:131–6.  https://doi.org/10.1111/exd.12900.CrossRefPubMedGoogle Scholar
  78. 78.
    Sun X-J, Wang Q, Guo B, Liu X-Y, Wang B. Identification of skin-related lncRNAs as potential biomarkers that involved in Wnt pathways in keloids. Oncotarget. 2017;8:34236–44.  https://doi.org/10.18632/oncotarget.15880.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Gupta R, Ahn R, Lai K, Mullins E, Debbaneh M, Dimon M, Arron S, Liao W. Landscape of long noncoding RNAs in psoriatic and healthy skin. J Invest Dermatol. 2016;136:603–9.  https://doi.org/10.1016/j.jid.2015.12.009.CrossRefPubMedGoogle Scholar
  80. 80.
    Chu CC, Qu KK, Zhong FLF, Artandi SES, Chang HYH. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell. 2011;44:667–78.  https://doi.org/10.1016/j.molcel.2011.08.027.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Siprashvili Z, Webster DE, Kretz M, Johnston D, Rinn JL, Chang HY, Khavari PA. Identification of proteins binding coding and non-coding human RNAs using protein microarrays. BMC Genomics. 2012;13:633.  https://doi.org/10.1186/1471-2164-13-633.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Program in Epithelial BiologyStanford University School of MedicineStanfordUSA
  2. 2.Veterans Affairs Palo Alto Healthcare SystemPalo AltoUSA

Personalised recommendations