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Impact of MicroRNA in Normal and Pathological Respiratory Epithelia

  • Lisa Giovannini-Chami
  • Nathalie Grandvaux
  • Laure-Emmanuelle Zaragosi
  • Karine Robbe-Sermesant
  • Brice Marcet
  • Bruno Cardinaud
  • Christelle Coraux
  • Yves Berthiaume
  • Rainer Waldmann
  • Bernard Mari
  • Pascal BarbryEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 741)

Abstract

Extensive sequencing efforts, combined with ad hoc bioinformatics developments, have now led to the identification of 1222 distinct miRNAs in human (derived from 1368 distinct genomic loci) and of many miRNAs in other multicellular organisms. The present chapter is aimed at describing a general experimental strategy to identify specific miRNA expression profiles and to highlight the functional networks operating between them and their mRNA targets, including several miRNAs deregulated in cystic fibrosis and during differentiation of airway epithelial cells.

Key words

Lung microRNA cystic fibrosis cancer 

Notes

Acknowledgments

This work is supported by CNRS, “Vaincre la Mucoviscidose,” CHU of Nice, ANR-09-GENO-039, European Community (MICROENVIMET, FP7-HEALTH-F2-2008-201279), the Canceropole PACA, and the Association de Recherche contre le Cancer.

References

  1. 1.
    Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854.PubMedGoogle Scholar
  2. 2.
    Wightman, B., Ha, I., and Ruvkun, G. (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862.PubMedGoogle Scholar
  3. 3.
    Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., et al. (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37, 766–770.PubMedGoogle Scholar
  4. 4.
    Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401–1414.PubMedGoogle Scholar
  5. 5.
    Friedlander, M. R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., et al. (2008) Discovering microRNAs from deep sequencing data using mirdeep. Nat. Biotechnol. 26, 407–415.PubMedGoogle Scholar
  6. 6.
    Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A., and Enright, A. J. (2006) Mirbase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140–144.PubMedGoogle Scholar
  7. 7.
    Lee, R., Feinbaum, R., and Ambros, V. (2004) A short history of a short RNA. Cell 116, S89–92, 81 p following S96.PubMedGoogle Scholar
  8. 8.
    Bartel, D. P. (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281–297.PubMedGoogle Scholar
  9. 9.
    Borchert, G. M., Lanier, W., and Davidson, B. L. (2006) RNA polymerase iii transcribes human microRNAs. Nat. Struct. Mol. Biol. 13, 1097–1101.PubMedGoogle Scholar
  10. 10.
    Gu, T. J., Yi, X., Zhao, X. W., Zhao, Y., and Yin, J. Q. (2009) Alu-directed transcriptional regulation of some novel miRNAs. BMC Genomics 10, 563.PubMedGoogle Scholar
  11. 11.
    Bortolin-Cavaille, M. L., Dance, M., Weber, M., and Cavaille, J. (2009) C19mc microRNAs are processed from introns of large pol-ii, non-protein-coding transcripts. Nucleic Acids Res. 37, 3464–3473.PubMedGoogle Scholar
  12. 12.
    Berezikov, E., Chung, W. J., Willis, J., Cuppen, E., and Lai, E. C. (2007) Mammalian mirtron genes. Mol. Cell 28, 328–336.PubMedGoogle Scholar
  13. 13.
    Ruby, J. G., Jan, C. H., and Bartel, D. P. (2007) Intronic microRNA precursors that bypass drosha processing. Nature 448, 83–86.PubMedGoogle Scholar
  14. 14.
    Babiarz, J. E., Ruby, J. G., Wang, Y., Bartel, D. P., and Blelloch, R. (2008) Mouse es cells express endogenous shRNAs, siRNAs, and other microprocessor-independent, dicer-dependent small RNAs. Genes Dev. 22, 2773–2785.PubMedGoogle Scholar
  15. 15.
    Lee, Y., Jeon, K., Lee, J. T., Kim, S., and Kim, V. N. (2002) MicroRNA maturation: Stepwise processing and subcellular localization. EMBO J. 21, 4663–4670.PubMedGoogle Scholar
  16. 16.
    Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., et al. (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432, 235–240.PubMedGoogle Scholar
  17. 17.
    Denli, A. M., Tops, B. B., Plasterk, R. H., Ketting, R. F., and Hannon, G. J. (2004) Processing of primary microRNAs by the microprocessor complex. Nature 432, 231–235.PubMedGoogle Scholar
  18. 18.
    Wang, H. W., Noland, C., Siridechadilok, B., Taylor, D. W., Ma, E., Felderer, K., et al. (2009) Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol. 16, 1148–1153.PubMedGoogle Scholar
  19. 19.
    Peters, L., and Meister, G. (2007) Argonaute proteins: Mediators of RNA silencing. Mol. Cell 26, 611–623.PubMedGoogle Scholar
  20. 20.
    Wang, B., Li, S., Qi, H. H., Chowdhury, D., Shi, Y., and Novina, C. D. (2009) Distinct passenger strand and mRNA cleavage activities of human argonaute proteins. Nat. Struct. Mol. Biol. 16, 1259–1266.PubMedGoogle Scholar
  21. 21.
    Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20.PubMedGoogle Scholar
  22. 22.
    Brennecke, J., Stark, A., Russell, R. B., and Cohen, S. M. (2005) Principles of microRNA-target recognition. PLoS Biol. 3, e85.PubMedGoogle Scholar
  23. 23.
    Doench, J. G., and Sharp, P. A. (2004) Specificity of microRNA target selection in translational repression. Genes Dev. 18, 504–511.PubMedGoogle Scholar
  24. 23a.
    Le Brigand, K., Robbe-Sermesant, K., Mari, B., and Barbry, P. (2010) MiRonTop: mining microRNAs targets across large scale gene expression studies. Bioinformatics 26, 3131–3132.Google Scholar
  25. 24.
    Chi, S. W., Zang, J. B., Mele, A., and Darnell, R. B. (2009) Argonaute hits-clip decodes microRNA-mRNA interaction maps. Nature 460, 479–486.PubMedGoogle Scholar
  26. 25.
    Xie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., et al. (2005) Systematic discovery of regulatory motifs in human promoters and 3 UTRs by comparison of several mammals. Nature 434, 338–345.PubMedGoogle Scholar
  27. 26.
    Wu, L., Fan, J., and Belasco, J. G. (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA 103, 4034–4039.PubMedGoogle Scholar
  28. 27.
    Eulalio, A., Huntzinger, E., and Izaurralde, E. (2008) Gw182 interaction with argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 15, 346–353.PubMedGoogle Scholar
  29. 28.
    Chen, C. Y., Zheng, D., Xia, Z., and Shyu, A. B. (2009) Ago-tnrc6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat. Struct. Mol. Biol. 16, 1160–1166.PubMedGoogle Scholar
  30. 29.
    Pillai, R. S., Artus, C. G., and Filipowicz, W. (2004) Tethering of human ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 10, 1518–1525.PubMedGoogle Scholar
  31. 30.
    Kozak, M. (2008) Faulty old ideas about translational regulation paved the way for current confusion about how microRNAs function. Gene 423, 108–115.PubMedGoogle Scholar
  32. 31.
    Wang, Y., Juranek, S., Li, H., Sheng, G., Wardle, G. S., Tuschl, T., et al. (2009) Nucleation, propagation and cleavage of target RNAs in ago silencing complexes. Nature 461, 754–761.PubMedGoogle Scholar
  33. 32.
    Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet. 9, 102–114.PubMedGoogle Scholar
  34. 33.
    Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58–63.PubMedGoogle Scholar
  35. 34.
    Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D., and Sun, X. (2006) Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208–2213.PubMedGoogle Scholar
  36. 35.
    Williams, A. E., Perry, M. M., Moschos, S. A., and Lindsay, M. A. (2007) MicroRNA expression in the aging mouse lung. BMC Genomics 8, 172.PubMedGoogle Scholar
  37. 36.
    Navarro, A., Marrades, R. M., Vinolas, N., Quera, A., Agusti, C., Huerta, A., et al. (2009) MicroRNAs expressed during lung cancer development are expressed in human pseudoglandular lung embryogenesis. Oncology 76, 162–169.PubMedGoogle Scholar
  38. 36a.
    Marcet, B., Chevalier, B., Luxardi, G., Coraux, C., Zaragosi, L. E., Cibois, M., Robbe-Sermesant, K., Jolly, T., Cardinaud, B., Moreilhon, C., Giovannini-Chami, L., Nawrocki-Raby, B., Birembaut, P., Waldmann, R., Kodjabachian, L., and Barbry, P. (2011) Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat. Cell Biol. In Press.Google Scholar
  39. 37.
    Williams, A. E., Larner-Svensson, H., Perry, M. M., Campbell, G. A., Herrick, S. E., Adcock, I. M., et al. (2009) MicroRNA expression profiling in mild asthmatic human airways and effect of corticosteroid therapy. PLoS One 4, e5889.PubMedGoogle Scholar
  40. 38.
    Baltimore, D., Boldin, M. P., O’Connell, R. M., Rao, D. S., and Taganov, K. D. (2008) MicroRNAs: New regulators of immune cell development and function. Nat. Immunol. 9, 839–845.PubMedGoogle Scholar
  41. 39.
    Sheedy, F. J., and O’Neill, L. A. (2008) Adding fuel to fire: MicroRNAs as a new class of mediators of inflammation. Ann. Rheum. Dis. 67(Suppl 3), iii50–55.PubMedGoogle Scholar
  42. 40.
    Busacca, S., Germano, S., De Cecco, L., Rinaldi, M., Comoglio, F., Favero, F., et al. (2010) MicroRNA signature of malignant mesothelioma with potential diagnostic and prognostic implications. Am. J. Respir. Cell. Mol. Biol. 42, 312–319.PubMedGoogle Scholar
  43. 41.
    Qian, S., Ding, J. Y., Xie, R., An, J. H., Ao, X. J., Zhao, Z. G., et al. (2008) MicroRNA expression profile of bronchioalveolar stem cells from mouse lung. Biochem. Biophys. Res. Commun. 377, 668–673.PubMedGoogle Scholar
  44. 42.
    Melkamu, T., Zhang, X., Tan, J., Zeng, Y., and Kassie, F. (2010) Alteration of microRNA expression in vinyl-carbamate-induced mouse lung tumors and modulation by the chemopreventive agent indole-3-carbinol. Carcinogenesis 31, 252–258.PubMedGoogle Scholar
  45. 43.
    Chen, J. F., Mandel, E. M., Thomson, J. M., Wu, Q., Callis, T. E., Hammond, S. M., et al. (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38, 228–233.PubMedGoogle Scholar
  46. 44.
    Chiba, Y., Tanabe, M., Goto, K., Sakai, H., and Misawa, M. (2009) Down-regulation of mir-133a contributes to up-regulation of rhoA in bronchial smooth muscle cells. Am. J. Respir. Crit. Care Med. 180, 713–719.PubMedGoogle Scholar
  47. 45.
    Tam, W., Ben-Yehuda, D., and Hayward, W. S. (1997) Bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Mol. Cell. Biol. 17, 1490–1502.PubMedGoogle Scholar
  48. 46.
    Tam, W. (2001) Identification and characterization of human bic, a gene on chromosome 21 that encodes a noncoding RNA. Gene 274, 157–167.PubMedGoogle Scholar
  49. 47.
    Iorio, M. V., Ferracin, M., Liu, C. G., Veronese, A., Spizzo, R., Sabbioni, S., et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65, 7065–7070.PubMedGoogle Scholar
  50. 48.
    Eis, P. S., Tam, W., Sun, L., Chadburn, A., Li, Z., Gomez, M. F., et al. (2005) Accumulation of mir-155 and bic RNA in human b cell lymphomas. Proc. Natl. Acad. Sci. USA 102, 3627–3632.PubMedGoogle Scholar
  51. 49.
    Kluiver, J., Poppema, S., de Jong, D., Blokzijl, T., Harms, G., Jacobs, S., et al. (2005) Bic and mir-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large b cell lymphomas. J. Pathol. 207, 243–249.PubMedGoogle Scholar
  52. 50.
    Jung, I., and Aguiar, R. C. (2009) MicroRNA-155 expression and outcome in diffuse large b-cell lymphoma. Br. J. Haematol. 144, 138–140.PubMedGoogle Scholar
  53. 51.
    Yin, Q., McBride, J., Fewell, C., Lacey, M., Wang, X., Lin, Z., et al. (2008) MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J. Virol. 82, 5295–5306.PubMedGoogle Scholar
  54. 52.
    Thai, T. H., Calado, D. P., Casola, S., Ansel, K. M., Xiao, C., Xue, Y., et al. (2007) Regulation of the germinal center response by microRNA-155. Science 316, 604–608.PubMedGoogle Scholar
  55. 53.
    Vigorito, E., Perks, K. L., Abreu-Goodger, C., Bunting, S., Xiang, Z., Kohlhaas, S. et al. (2007) MicroRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27, 847–859.PubMedGoogle Scholar
  56. 54.
    Rodriguez, A., Vigorito, E., Clare, S., Warren, M. V., Couttet, P., Soond, D. R., et al. (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316, 608–611.PubMedGoogle Scholar
  57. 55.
    Kohlhaas, S., Garden, O. A., Scudamore, C., Turner, M., Okkenhaug, K., and Vigorito, E. (2009) Cutting edge: The foxp3 target mir-155 contributes to the development of regulatory t cells. J. Immunol. 182, 2578–2582.PubMedGoogle Scholar
  58. 56.
    O’Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., and Baltimore, D. (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104, 1604–1609.PubMedGoogle Scholar
  59. 57.
    Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., et al. (2007) 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. 179, 5082–5089.PubMedGoogle Scholar
  60. 58.
    Ceppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A., et al. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. USA 106, 2735–2740.PubMedGoogle Scholar
  61. 59.
    Kluiver, J., van den Berg, A., de Jong, D., Blokzijl, T., Harms, G., Bouwman, E., et al. (2007) Regulation of pri-microRNA bic transcription and processing in Burkitt lymphoma. Oncogene 26, 3769–3776.PubMedGoogle Scholar
  62. 60.
    Yin, Q., Wang, X., McBride, J., Fewell, C., and Flemington, E. (2008) B-cell receptor activation induces bic/mir-155 expression through a conserved ap-1 element. J. Biol. Chem. 283, 2654–2662.PubMedGoogle Scholar
  63. 61.
    Stanczyk, J., Pedrioli, D. M., Brentano, F., Sanchez-Pernaute, O., Kolling, C., Gay, R. E., et al. (2008) Altered expression of microRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum. 58, 1001–1009.PubMedGoogle Scholar
  64. 62.
    Martin, M. M., Lee, E. J., Buckenberger, J. A., Schmittgen, T. D., and Elton, T. S. (2006) MicroRNA-155 regulates human angiotensin ii type 1 receptor expression in fibroblasts. J. Biol. Chem. 281, 18277–18284.PubMedGoogle Scholar
  65. 63.
    Pottier, N., Maurin, T., Chevalier, B., Puissegur, M. P., Lebrigand, K., Robbe-Sermesant, K., et al. (2009) Identification of keratinocyte growth factor as a target of microRNA-155 in lung fibroblasts: Implication in epithelial-mesenchymal interactions. PLoS One 4, e6718.PubMedGoogle Scholar
  66. 64.
    Rai, D., Karanti, S., Jung, I., Dahia, P. L., and Aguiar, R. C. (2008) Coordinated expression of microRNA-155 and predicted target genes in diffuse large b-cell lymphoma. Cancer Genet. Cytogenet. 181, 8–15.PubMedGoogle Scholar
  67. 65.
    Dorsett, Y., McBride, K. M., Jankovic, M., Gazumyan, A., Thai, T. H., Robbiani, D. F., et al. (2008) MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated myc-igh translocation. Immunity 28, 630–638.PubMedGoogle Scholar
  68. 66.
    Teng, G., Hakimpour, P., Landgraf, P., Rice, A., Tuschl, T., Casellas, R., et al. (2008) MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28, 621–629.PubMedGoogle Scholar
  69. 67.
    Kong, W., Yang, H., He, L., Zhao, J. J., Coppola, D., Dalton, W. S., et al. (2008) MicroRNA-155 is regulated by the transforming growth factor beta/smad pathway and contributes to epithelial cell plasticity by targeting rhoA. Mol. Cell. Biol. 28, 6773–6784.PubMedGoogle Scholar
  70. 67a.
    Bhattacharyya, S., Balakathiresan, N. S., Dalgard, C., Gutti, U., Armistead, D., Jozwik, C., Srivastava, M., Pollard, H. B., and Biswas, R. (2011) Elevated miR-155 promotes inflammation in cystic fibrosis by driving hyper-expression of interleukin-8. J. Biol. Chem. In Press.Google Scholar
  71. 68.
    Gitlin, L., and Andino, R. (2003) Nucleic acid-based immune system: The antiviral potential of mammalian RNA silencing. J. Virol. 77, 7159–7165.PubMedGoogle Scholar
  72. 69.
    Samuel, C. E. (2001) Antiviral actions of interferons. Clin. Microbiol. Rev. 14, 778–809.PubMedGoogle Scholar
  73. 70.
    Grandvaux, N., TenOever, B. R., Servant, M. J., and Hiscott, J. (2002) The interferon antiviral response: From viral invasion to evasion. Curr. Opin. Infect. Dis. 15, 259–267.PubMedGoogle Scholar
  74. 71.
    Barral, P. M., Sarkar, D., Su, Z. Z., Barber, G. N., DeSalle, R., Racaniello, V. R., et al. (2009) Functions of the cytoplasmic RNA sensors rig-i and mda-5: Key regulators of innate immunity. Pharmacol. Ther. 124, 219–234.PubMedGoogle Scholar
  75. 72.
    Kawai, T., and Akira, S. (2008) Toll-like receptor and rig-i-like receptor signaling. Ann. N Y Acad. Sci. 1143, 1–20.PubMedGoogle Scholar
  76. 73.
    Kumar, H., Kawai, T., and Akira, S. (2009) Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388, 621–625.PubMedGoogle Scholar
  77. 74.
    Otsuka, M., Jing, Q., Georgel, P., New, L., Chen, J., Mols, J., et al. (2007) Hypersusceptibility to vesicular stomatitis virus infection in dicer1-deficient mice is due to impaired mir24 and mir93 expression. Immunity 27, 123–134.PubMedGoogle Scholar
  78. 75.
    Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M., and Sarnow, P. (2005) Modulation of hepatitis c virus RNA abundance by a liver-specific microRNA. Science 309, 1577–1581.PubMedGoogle Scholar
  79. 76.
    Wang, Y., Brahmakshatriya, V., Zhu, H., Lupiani, B., Reddy, S. M., Yoon, B. J., et al. (2009) Identification of differentially expressed miRNAs in chicken lung and trachea with avian influenza virus infection by a deep sequencing approach. BMC Genomics 10, 512.PubMedGoogle Scholar
  80. 77.
    Mallick, B., Ghosh, Z., and Chakrabarti, J. (2009) MicroRNome analysis unravels the molecular basis of sars infection in bronchoalveolar stem cells. PLoS One 4, e7837.PubMedGoogle Scholar
  81. 78.
    Izzotti, A., Calin, G. A., Arrigo, P., Steele, V. E., Croce, C. M., and De Flora, S. (2009) Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J. 23, 806–812.PubMedGoogle Scholar
  82. 79.
    Izzotti, A., Calin, G. A., Steele, V. E., Croce, C. M., and De Flora, S. (2009) Relationships of microRNA expression in mouse lung with age and exposure to cigarette smoke and light. FASEB J. 23, 3243–3250.PubMedGoogle Scholar
  83. 80.
    Schembri, F., Sridhar, S., Perdomo, C., Gustafson, A. M., Zhang, X., Ergun, A., et al. (2009) MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc. Natl. Acad. Sci. USA 106, 2319–2324.PubMedGoogle Scholar
  84. 81.
    van Rooij, E., Sutherland, L. B., Liu, N., Williams, A. H., McAnally, J., Gerard, R. D., et al. (2006) A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl. Acad. Sci. USA 103, 18255–18260.PubMedGoogle Scholar
  85. 82.
    Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., et al. (2002) Frequent deletions and down-regulation of micro- RNA genes mir15 and mir16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 99, 15524–15529.PubMedGoogle Scholar
  86. 83.
    Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs – microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259–269.PubMedGoogle Scholar
  87. 84.
    Croce, C. M. (2009) Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10, 704–714.PubMedGoogle Scholar
  88. 85.
    Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., et al. (2005) MicroRNA expression profiles classify human cancers. Nature 435, 834–838.PubMedGoogle Scholar
  89. 86.
    Volinia, S., Calin, G. A., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., et al. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103, 2257–2261.PubMedGoogle Scholar
  90. 87.
    Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., et al. (2008) Cancer statistics 2008. CA Cancer J. Clin. 58, 71–96.PubMedGoogle Scholar
  91. 88.
    D’Amico, T. A. (2008) Molecular biologic staging of lung cancer. Ann. Thorac. Surg. 85, S737–742.PubMedGoogle Scholar
  92. 89.
    Harpole, D. H, Jr. (2007) Prognostic modeling in early stage lung cancer: An evolving process from histopathology to genomics. Thorac. Surg. Clin. 17, 167–173.PubMedGoogle Scholar
  93. 90.
    Ortholan, C., Puissegur, M. P., Ilie, M., Barbry, P., Mari, B., and Hofman, P. (2009) MicroRNAs and lung cancer: New oncogenes and tumor suppressors, new prognostic factors and potential therapeutic targets. Curr. Med. Chem. 16, 1047–1061.PubMedGoogle Scholar
  94. 91.
    Wang, Q. Z., Xu, W., Habib, N., and Xu, R. (2009) Potential uses of microRNA in lung cancer diagnosis, prognosis, and therapy. Curr. Cancer Drug Targets 9, 572–594.PubMedGoogle Scholar
  95. 92.
    Wu, X., Piper-Hunter, M. G., Crawford, M., Nuovo, G. J., Marsh, C. B., Otterson, G. A., et al. (2009) MicroRNAs in the pathogenesis of lung cancer. J. Thorac. Oncol. 4, 1028–1034.PubMedGoogle Scholar
  96. 92a.
    Puisségur, M. P., Mazure, N. M., Bertero, T., Pradelli, L., Grosso, S., Robbe-Sermesant, K., Maurin, T., Lebrigand, K., Cardinaud, B., Hofman, V., Fourre, S., Magnone, V., Ricci, J. E., Pouysségur, J., Gounon, P., Hofman, P., Barbry, P., and Mari, B. (2010) miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death Differ. 18, 465–478.Google Scholar
  97. 93.
    Oglesby, I. K., Bray, I. M., Chotirmall, S. H., Stallings, R. L., O’Neill, S. J., McElvaney, N. G., et al. (2010) Mir-126 is downregulated in cystic fibrosis airway epithelial cells and regulates tom1 expression. J. Immunol. 184, 1702–1709.PubMedGoogle Scholar
  98. 94.
    Triboulet, R., Mari, B., Lin, Y. L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., et al. (2007) Suppression of microRNA-silencing pathway by hiv-1 during virus replication. Science 315, 1579–1582.PubMedGoogle Scholar
  99. 95.
    Saumet, A., Vetter, G., Bouttier, M., Portales-Casamar, E., Wasserman, W. W., Maurin, T., et al. (2009) Transcriptional repression of microRNA genes by pml-rara increases expression of key cancer proteins in acute promyelocytic leukemia. Blood 113, 412–421.PubMedGoogle Scholar
  100. 96.
    Shi, R., and Chiang, V. L. (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39, 519–525.PubMedGoogle Scholar
  101. 97.
    Liu, C. G., Calin, G. A., Meloon, B., Gamliel, N., Sevignani, C., Ferracin, M., et al. (2004) An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proc. Natl. Acad. Sci. USA 101, 9740–9744.PubMedGoogle Scholar
  102. 98.
    Liu, C. G., Calin, G. A., Volinia, S., and Croce, C. M. (2008) MicroRNA expression profiling using microarrays. Nat. Protoc. 3, 563–578.PubMedGoogle Scholar
  103. 99.
    Shingara, J., Keiger, K., Shelton, J., Laosinchai-Wolf, W., Powers, P., Conrad, R., et al. (2005) An optimized isolation and labeling platform for accurate microRNA expression profiling. RNA 11, 1461–1470.PubMedGoogle Scholar
  104. 100.
    Sun, Y., Koo, S., White, N., Peralta, E., Esau, C., Dean, N. M., and Perera, R. J. (2004) Development of a micro-array to detect human and mouse microRNAs and characterization of expression in human organs. Nucleic Acids Res. 32, e188.PubMedGoogle Scholar
  105. 101.
    Wang, H., Ach, R. A., and Curry, B. (2007) Direct and sensitive miRNA profiling from low-input total RNA. RNA 13, 151–159.PubMedGoogle Scholar
  106. 102.
    Castoldi, M., Schmidt, S., Benes, V., Noerholm, M., Kulozik, A. E., Hentze, M. W., et al. (2006) A sensitive array for microRNA expression profiling (michip) based on locked nucleic acids (lna). RNA 12, 913–920.PubMedGoogle Scholar
  107. 103.
    Nelson, P. T., Baldwin, D. A., Scearce, L. M., Oberholtzer, J. C., Tobias, J. W., and Mourelatos, Z. (2004) Microarray-based, high-throughput gene expression profiling of microRNAs. Nat. Methods 1, 155–161.PubMedGoogle Scholar
  108. 104.
    Jonstrup, S. P., Koch, J., and Kjems, J. (2006) A microRNA detection system based on padlock probes and rolling circle amplification. RNA 12, 1747–1752.PubMedGoogle Scholar
  109. 105.
    Ansorge, W. J. (2009) Next-generation DNA sequencing techniques. Nat. Biotechnol. 25, 195–203.Google Scholar
  110. 106.
    Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5, R80.PubMedGoogle Scholar
  111. 107.
    Thompson, R. C., Deo, M., and Turner, D. L. (2007) Analysis of microRNA expression by in situ hybridization with RNA oligonucleotide probes. Methods 43, 153–161.PubMedGoogle Scholar
  112. 108.
    Lassalle, S., Bonnetaud, C., Hofman, V., Puisségur, M. P., Brest, P., Loubatier, C., et al. (2009) MicroRNA signature of thyroid tumors of uncertain malignancy (ttump). Submitted.Google Scholar
  113. 109.
    Pena, J. T., Sohn-Lee, C., Rouhanifard, S. H., Ludwig, J., Hafner, M., Mihailovic, A., et al. (2009) MiRNA in situ hybridization in formaldehyde and edc-fixed tissues. Nat. Methods 6, 139–141.PubMedGoogle Scholar
  114. 110.
    Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., et al. (2005) MicroRNA expression in zebrafish embryonic development. Science 309, 310–311.PubMedGoogle Scholar
  115. 111.
    Kloosterman, W. P., Wienholds, E., de Bruijn, E., Kauppinen, S., and Plasterk, R. H. (2006) In situ detection of miRNAs in animal embryos using lna-modified oligonucleotide probes. Nat. Methods 3, 27–29.PubMedGoogle Scholar
  116. 112.
    Darnell, D. K., Kaur, S., Stanislaw, S., Konieczka, J. H., Yatskievych, T. A., and Antin, P. B. (2006) MicroRNA expression during chick embryo development. Dev. Dyn. 235, 3156–3165.PubMedGoogle Scholar
  117. 113.
    Nelson, P. T., Baldwin, D. A., Kloosterman, W. P., Kauppinen, S., Plasterk, R. H., and Mourelatos, Z. (2006) Rake and lna-ish reveal microRNA expression and localization in archival human brain. RNA 12, 187–191.PubMedGoogle Scholar
  118. 114.
    Wulczyn, F. G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., et al. (2007) Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 21, 415–426.PubMedGoogle Scholar
  119. 115.
    Deo, M., Yu, J. Y., Chung, K. H., Tippens, M., and Turner, D. L. (2006) Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides. Dev. Dyn. 235, 2538–2548.PubMedGoogle Scholar
  120. 116.
    Obernosterer, G., Leuschner, P. J., Alenius, M., and Martinez, J. (2006) Post-transcriptional regulation of microRNA expression. RNA 12, 1161–1167.PubMedGoogle Scholar
  121. 117.
    Kiriakidou, M., Nelson, P. T., Kouranov, A., Fitziev, P., Bouyioukos, C., Mourelatos, Z., et al. (2004) A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 18, 1165–1178.PubMedGoogle Scholar
  122. 118.
    Krek, A., Grun, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., et al. (2005) Combinatorial microRNA target predictions. Nat. Genet. 37, 495–500.PubMedGoogle Scholar
  123. 119.
    Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell 115, 787–798.PubMedGoogle Scholar
  124. 120.
    Miranda, K. C., Huynh, T., Tay, Y., Ang, Y. S., Tam, W. L., Thomson, A. M., et al. (2006) A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203–1217.PubMedGoogle Scholar
  125. 121.
    Rajewsky, N., and Socci, N. D. (2004) Computational identification of microRNA targets. Dev. Biol. 267, 529–535.PubMedGoogle Scholar
  126. 122.
    Rajewsky, N. (2006) MicroRNA target predictions in animals. Nat. Genet 38(Suppl), S8–13.PubMedGoogle Scholar
  127. 123.
    Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., et al. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769–773.PubMedGoogle Scholar
  128. 124.
    Khan, A. A., Betel, D., Miller, M. L., Sander, C., Leslie, C. S., and Marks, D. S. (2009) Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nat. Biotechnol. 27, 549–555.PubMedGoogle Scholar
  129. 125.
    Wang, W. X., Wilfred, B. R., Hu, Y., Stromberg, A. J., and Nelson, P. T. (2010) Anti-argonaute rip-chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 16, 394–404.PubMedGoogle Scholar
  130. 126.
    Huang, J., Liang, Z., Yang, B., Tian, H., Ma, J., and Zhang, H. (2007) Derepression of microRNA-mediated protein translation inhibition by apolipoprotein b mRNA-editing enzyme catalytic polypeptide-like 3 g (apobec3g) and its family members. J. Biol. Chem. 282, 33632–33640.PubMedGoogle Scholar
  131. 127.
    Le Brigand, K., and Barbry, P. (2007) Mediante A web-based microarray data manager. Bioinformatics 23, 1304–1306.PubMedGoogle Scholar
  132. 128.
    Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264.PubMedGoogle Scholar
  133. 129.
    Bartel, D. P. (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136, 215–233.PubMedGoogle Scholar
  134. 130.
    van Dongen, S., Abreu-Goodger, C., and Enright, A. J. (2008) Detecting microRNA binding and siRNA off-target effects from expression data. Nat. Methods 5, 1023–1025.PubMedGoogle Scholar
  135. 131.
    Beitzinger, M., Peters, L., Zhu, J. Y., Kremmer, E., and Meister, G. (2007) Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 4, 76–84.PubMedGoogle Scholar
  136. 132.
    Karginov, F. V., Conaco, C., Xuan, Z., Schmidt, B. H., Parker, J. S., Mandel, G., et al. (2007) A biochemical approach to identifying microRNA targets. Proc. Natl. Acad. Sci. USA 104, 19291–19296.PubMedGoogle Scholar
  137. 133.
    Keene, J. D., Komisarow, J. M., and Friedersdorf, M. B. (2006) Rip-chip: The isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat. Protoc. 1, 302–307.PubMedGoogle Scholar
  138. 134.
    Hendrickson, D. G., Hogan, D. J., Herschlag, D., Ferrell, J. E., and Brown, P. O. (2008) Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance. PLoS One 3, e2126.PubMedGoogle Scholar
  139. 135.
    Easow, G., Teleman, A. A., and Cohen, S. M. (2007) Isolation of microRNA targets by mirnp immunopurification. RNA 13, 1198–1204.PubMedGoogle Scholar
  140. 136.
    Landthaler, M., Gaidatzis, D., Rothballer, A., Chen, P. Y., Soll, S. J., Dinic, L., et al. (2008) Molecular characterization of human argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14, 2580–2596.PubMedGoogle Scholar
  141. 137.
    Chi, S. W., Zang, J. B., Mele, A., and Darnell, R. B. (2009) Argonaute hits-clip decodes microRNA-mRNA interaction maps. Nature 460, 479–486.PubMedGoogle Scholar
  142. 138.
    Azuma-Mukai, A., Oguri, H., Mituyama, T., Qian, Z. R., Asai, K., Siomi, H., et al. (2008) Characterization of endogenous human argonautes and their miRNA partners in RNA silencing. Proc. Natl. Acad. Sci. USA 105, 7964–7969.PubMedGoogle Scholar
  143. 139.
    Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008) The impact of microRNAs on protein output. Nature 455, 64–71.PubMedGoogle Scholar
  144. 140.
    Cimmino, A., Calin, G. A., Fabbri, M., Iorio, M. V., Ferracin, M., Shimizu, M., et al. (2005) Mir-15 and mir-16 induce apoptosis by targeting bcl2. Proc. Natl. Acad. Sci. USA 102, 13944–13949.PubMedGoogle Scholar
  145. 141.
    Mattick, J. S., and Makunin, I. V. (2005) Small regulatory RNAs in mammals. Hum. Mol. Genet. 14(S 1), R121–132.PubMedGoogle Scholar
  146. 142.
    Kapranov, P. (2009) From transcription start site to cell biology. Genome Biol. 10, 217.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Lisa Giovannini-Chami
    • 1
    • 2
  • Nathalie Grandvaux
    • 3
  • Laure-Emmanuelle Zaragosi
    • 1
  • Karine Robbe-Sermesant
    • 1
  • Brice Marcet
    • 1
  • Bruno Cardinaud
    • 1
  • Christelle Coraux
    • 4
  • Yves Berthiaume
    • 5
  • Rainer Waldmann
    • 1
  • Bernard Mari
    • 1
  • Pascal Barbry
    • 1
    Email author
  1. 1.CNRS, Université de Nice Sophia Antipolis, IPMC, UMR6097Sophia AntipolisFrance
  2. 2.Service de Pédiatrie, Unité de Pneumo-AllergologieCHU de NiceFrance
  3. 3.Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Université de Montréal, Hôpital Saint-Luc, PEAMontréalCanada
  4. 4.INSERM UMRS 903, CHU Maison BlancheReimsFrance
  5. 5.Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Université de Montréal, Hôtel DieuMontréalCanada

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