Skip to main content

Advertisement

SpringerLink
Log in

microRNAs and lung cancer: tumors and 22-mers

  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

An Erratum to this article was published on 10 June 2010

Abstract

Work over the last decade has revealed novel regulatory mechanisms in pathological disease states that are mediated by microRNAs and has inspired researchers to begin elucidating the specific roles of miRNAs in the regulation of genes involved in cancer development and progression. Recently, miRNAs have been explored as therapeutic targets and diagnostic markers of cancer. In this paper, we review recent advances in the study of miRNAs involved in tumorigenesis, focusing on miRNA regulation of genes that have been demonstrated to play critical roles in lung cancer development. We discuss miRNA regulation of genes that play critical roles in the process of malignant transformation, angiogenesis and tumor metastasis, the dysregulation of miRNA expression in cancer development, and the development of miRNA-based diagnostics and therapeutics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Yekta, S., Shih, I. H., & Bartel, D. P. (2004). MicroRNA-directed cleavage of HOXB8 mRNA. Science, 304, 594–596.

    Article  PubMed  CAS  Google Scholar 

  2. Vasudevan, S., Tong, Y., & Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931–1934.

    Article  PubMed  CAS  Google Scholar 

  3. Novotny, G. W., Sonne, S. B., Nielsen, J. E., Jonstrup, S. P., Hansen, M. A., Skakkebaek, N. E., et al. (2007). Translational repression of E2F1 mRNA in carcinoma in situ and normal testis correlates with expression of the miR-17-92 cluster. Cell Death and Differentiation, 14, 879–882.

    Article  PubMed  CAS  Google Scholar 

  4. He, L., He, X., Lowe, S. W., & Hannon, G. J. (2007). microRNAs join the p53 network—Another piece in the tumour-suppression puzzle. Nature Reviews Cancer, 7, 819–822.

    Article  PubMed  CAS  Google Scholar 

  5. Cho, W. C. (2007). OncomiRs: The discovery and progress of microRNAs in cancers. Molecular Cancer, 6, 60.

    Article  PubMed  CAS  Google Scholar 

  6. Hwang, H. W., & Mendell, J. T. (2006). MicroRNAs in cell proliferation, cell death, and tumorigenesis. British Journal of Cancer, 94, 776–780.

    Article  PubMed  CAS  Google Scholar 

  7. Esquela-Kerscher, A., & Slack, F. J. (2006). Oncomirs—microRNAs with a role in cancer. Nature Reviews Cancer, 6, 259–269.

    Article  PubMed  CAS  Google Scholar 

  8. Hebert, C., Norris, K., Scheper, M. A., Nikitakis, N., & Sauk, J. J. (2007). High mobility group A2 is a target for miRNA-98 in head and neck squamous cell carcinoma. Molecular Cancer, 6, 5.

    Article  PubMed  CAS  Google Scholar 

  9. Lee, D. Y., Deng, Z., Wang, C. H., & Yang, B. B. (2007). MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proceedings of the National Academy of Sciences of the United States of America, 104, 20350–20355.

    Article  PubMed  Google Scholar 

  10. O’Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V., & Mendell, J. T. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 435, 839–843.

    Article  PubMed  CAS  Google Scholar 

  11. Mercatelli, N., Coppola, V., Bonci, D., Miele, F., Costantini, A., Guadagnoli, M., et al. (2008). The inhibition of the highly expressed miR-221 and miR-222 impairs the growth of prostate carcinoma xenografts in mice. PLoS ONE, 3, e4029.

    Article  PubMed  CAS  Google Scholar 

  12. Felicetti, F., Errico, M. C., Bottero, L., Segnalini, P., Stoppacciaro, A., Biffoni, M., et al. (2008). The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Research, 68, 2745–2754.

    Article  PubMed  CAS  Google Scholar 

  13. Wickramasinghe, N. S., Manavalan, T. T., Dougherty, S. M., Riggs, K. A., Li, Y., & Klinge, C. M. (2009). Estradiol downregulates miR-21 expression and increases miR-21 target gene expression in MCF-7 breast cancer cells. Nucleic Acids Research, 37, 2584–2595.

    Article  PubMed  CAS  Google Scholar 

  14. Yang, Y., Chaerkady, R., Beer, M. A., Mendell, J. T., & Pandey, A. (2009). Identification of miR-21 targets in breast cancer cells using a quantitative proteomic approach. Proteomics, 9, 1374–1384.

    Article  PubMed  CAS  Google Scholar 

  15. Si, M. L., Zhu, S., Wu, H., Lu, Z., Wu, F., & Mo, Y. Y. (2007). miR-21-mediated tumor growth. Oncogene, 26, 2799–2803.

    Article  PubMed  CAS  Google Scholar 

  16. Yanaihara, N., Caplen, N., Bowman, E., Seike, M., Kumamoto, K., Yi, M., et al. (2006). Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell, 9, 189–198.

    Article  PubMed  CAS  Google Scholar 

  17. Taylor, D. D., & Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecologic Oncology, 110, 13–21.

    Article  PubMed  CAS  Google Scholar 

  18. Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America, 105, 10513–10518.

    Article  PubMed  Google Scholar 

  19. Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., et al. (2008). Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Research, 18, 997–1006.

    Article  PubMed  CAS  Google Scholar 

  20. Hanahan, D., & Weinberg, R. A. (2000). The hallmarks of cancer. Cell, 100, 57–70.

    Article  PubMed  CAS  Google Scholar 

  21. Khosravi-Far, R., & Esposti, M. D. (2004). Death receptor signals to mitochondria. Cancer Biology and Therapy, 3, 1051–1057.

    Article  PubMed  CAS  Google Scholar 

  22. Holbro, T., Beerli, R. R., Maurer, F., Koziczak, M., Barbas, C. F., 3rd, & Hynes, N. E. (2003). The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proceedings of the National Academy of Sciences of the United States of America, 100, 8933–8938.

    Article  PubMed  CAS  Google Scholar 

  23. Scott, G. K., Goga, A., Bhaumik, D., Berger, C. E., Sullivan, C. S., & Benz, C. C. (2007). Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. Journal of Biological Chemistry, 282, 1479–1486.

    Article  PubMed  CAS  Google Scholar 

  24. Weiss, G. J., Bemis, L. T., Nakajima, E., Sugita, M., Birks, D. K., Robinson, W. A., et al. (2008). EGFR regulation by microRNA in lung cancer: Correlation with clinical response and survival to gefitinib and EGFR expression in cell lines. Annals of Oncology, 19, 1053–1059.

    Article  PubMed  CAS  Google Scholar 

  25. Webster, R. J., Giles, K. M., Price, K. J., Zhang, P. M., Mattick, J. S., & Leedman, P. J. (2009). Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. Journal of Biological Chemistry, 284, 5731–5741.

    Article  PubMed  CAS  Google Scholar 

  26. Eberhart, J. K., He, X., Swartz, M. E., Yan, Y. L., Song, H., Boling, T. C., et al. (2008). MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nature Genetics, 40, 290–298.

    Article  PubMed  CAS  Google Scholar 

  27. La Rocca, G., Badin, M., Shi, B., Xu, S. Q., Deangelis, T., Sepp-Lorenzinoi, L., et al. (2009). Mechanism of growth inhibition by MicroRNA 145: The role of the IGF-I receptor signaling pathway. Journal of Cellular Physiology, 220, 485–491.

    Article  PubMed  CAS  Google Scholar 

  28. Bos, J. L. (1989). ras oncogenes in human cancer: A review. Cancer Research, 49, 4682–4689.

    PubMed  CAS  Google Scholar 

  29. Downward, J. (2003). Targeting RAS signalling pathways in cancer therapy. Nature Reviews Cancer, 3, 11–22.

    Article  PubMed  CAS  Google Scholar 

  30. Zajac-Kaye, M. (2001). Myc oncogene: A key component in cell cycle regulation and its implication for lung cancer. Lung Cancer, 34(Suppl 2), S43–S46.

    Article  PubMed  Google Scholar 

  31. Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., et al. (2005). RAS is regulated by the let-7 microRNA family. Cell, 120, 635–647.

    Article  PubMed  CAS  Google Scholar 

  32. Kumar, M. S., Erkeland, S. J., Pester, R. E., Chen, C. Y., Ebert, M. S., Sharp, P. A., et al. (2008). Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proceedings of the National Academy of Sciences of the United States of America, 105, 3903–3908.

    Article  PubMed  Google Scholar 

  33. Sampson, V. B., Rong, N. H., Han, J., Yang, Q., Aris, V., Soteropoulos, P., et al. (2007). MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Research, 67, 9762–9770.

    Article  PubMed  CAS  Google Scholar 

  34. Mayr, C., Hemann, M. T., & Bartel, D. P. (2007). Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science, 315, 1576–1579.

    Article  PubMed  CAS  Google Scholar 

  35. Muntoni, A., & Reddel, R. R. (2005). The first molecular details of ALT in human tumor cells. Human Molecular Genetics, 14(Spec No. 2), R191–R196.

    Article  PubMed  CAS  Google Scholar 

  36. Mitomo, S., Maesawa, C., Ogasawara, S., Iwaya, T., Shibazaki, M., Yashima-Abo, A., et al. (2008). Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines. Cancer Science, 99, 280–286.

    Article  PubMed  CAS  Google Scholar 

  37. Gonzalo, S., Jaco, I., Fraga, M. F., Chen, T., Li, E., Esteller, M., et al. (2006). DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nature Cell Biology, 8, 416–424.

    Article  PubMed  CAS  Google Scholar 

  38. Benetti, R., Gonzalo, S., Jaco, I., Munoz, P., Gonzalez, S., Schoeftner, S., et al. (2008). A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nature Structural & Molecular Biology, 15, 268–279.

    Article  CAS  Google Scholar 

  39. Fabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N., Callegari, E., et al. (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proceedings of the National Academy of Sciences of the United States of America, 104, 15805–15810.

    Article  PubMed  Google Scholar 

  40. Hotchkiss, R. S., Strasser, A., McDunn, J. E., & Swanson, P. E. (2009). Cell death. New England Journal of Medicine, 361, 1570–1583.

    Article  PubMed  CAS  Google Scholar 

  41. Porkka, K. P., Pfeiffer, M. J., Waltering, K. K., Vessella, R. L., Tammela, T. L., & Visakorpi, T. (2007). MicroRNA expression profiling in prostate cancer. Cancer Research, 67, 6130–6135.

    Article  PubMed  CAS  Google Scholar 

  42. Bottoni, A., Piccin, D., Tagliati, F., Luchin, A., Zatelli, M. C., & degli Uberti, E. C. (2005). miR-15a and miR-16-1 down-regulation in pituitary adenomas. Journal of Cellular Physiology, 204, 280–285.

    Article  PubMed  CAS  Google Scholar 

  43. 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. Proceedings of the National Academy of Sciences of the United States of America, 102, 13944–13949.

    Article  PubMed  CAS  Google Scholar 

  44. Mott, J. L., Kobayashi, S., Bronk, S. F., & Gores, G. J. (2007). mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene, 26, 6133–6140.

    Article  PubMed  CAS  Google Scholar 

  45. Calin, G. A., Ferracin, M., Cimmino, A., Di Leva, G., Shimizu, M., Wojcik, S. E., et al. (2005). A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. New England Journal of Medicine, 353, 1793–1801.

    Article  PubMed  CAS  Google Scholar 

  46. Cummins, J. M., He, Y., Leary, R. J., Pagliarini, R., Diaz, L. A., Jr., Sjoblom, T., et al. (2006). The colorectal microRNAome. Proceedings of the National Academy of Sciences of the United States of America, 103, 3687–3692.

    Article  PubMed  CAS  Google Scholar 

  47. Chan, J. A., Krichevsky, A. M., & Kosik, K. S. (2005). MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Research, 65, 6029–6033.

    Article  PubMed  CAS  Google Scholar 

  48. Seike, M., Goto, A., Okano, T., Bowman, E. D., Schetter, A. J., Horikawa, I., et al. (2009). MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proceedings of the National Academy of Sciences of the United States of America, 106, 12085–12090.

    Article  PubMed  Google Scholar 

  49. Tarasov, V., Jung, P., Verdoodt, B., Lodygin, D., Epanchintsev, A., Menssen, A., et al. (2007). Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle, 6, 1586–1593.

    PubMed  CAS  Google Scholar 

  50. Hermeking, H. (2010). The miR-34 family in cancer and apoptosis. Cell Death and Differentiation, 17, 193–199.

    Article  PubMed  CAS  Google Scholar 

  51. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature, 447, 1130–1134.

    Article  PubMed  CAS  Google Scholar 

  52. le Sage, C., Nagel, R., Egan, D. A., Schrier, M., Mesman, E., Mangiola, A., et al. (2007). Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO Journal, 26, 3699–3708.

    Article  PubMed  CAS  Google Scholar 

  53. Gillies, J. K., & Lorimer, I. A. (2007). Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle, 6, 2005–2009.

    PubMed  CAS  Google Scholar 

  54. Galardi, S., Mercatelli, N., Giorda, E., Massalini, S., Frajese, G. V., Ciafre, S. A., et al. (2007). miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. Journal of Biological Chemistry, 282, 23716–23724.

    Article  PubMed  CAS  Google Scholar 

  55. Whang-Peng, J., Kao-Shan, C. S., Lee, E. C., Bunn, P. A., Carney, D. N., Gazdar, A. F., et al. (1982). Specific chromosome defect associated with human small-cell lung cancer; deletion 3p(14-23). Science, 215, 181–182.

    Article  PubMed  CAS  Google Scholar 

  56. Zabarovsky, E. R., Lerman, M. I., & Minna, J. D. (2002). Tumor suppressor genes on chromosome 3p involved in the pathogenesis of lung and other cancers. Oncogene, 21, 6915–6935.

    Article  PubMed  CAS  Google Scholar 

  57. Lerman, M. I., & Minna, J. D. (2000). The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: Identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Research, 60, 6116–6133.

    PubMed  CAS  Google Scholar 

  58. Ji, L., Nishizaki, M., Gao, B., Burbee, D., Kondo, M., Kamibayashi, C., et al. (2002). Expression of several genes in the human chromosome 3p21.3 homozygous deletion region by an adenovirus vector results in tumor suppressor activities in vitro and in vivo. Cancer Research, 62, 2715–2720.

    PubMed  CAS  Google Scholar 

  59. Du, L., Schageman, J. J., Subauste, M. C., Saber, B., Hammond, S. M., Prudkin, L., et al. (2009). miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Molecular Cancer Research, 7, 1234–1243.

    Article  PubMed  CAS  Google Scholar 

  60. Prudkin, L., Behrens, C., Liu, D. D., Zhou, X., Ozburn, N. C., Bekele, B. N., et al. (2008). Loss and reduction of FUS1 protein expression is a frequent phenomenon in the pathogenesis of lung cancer. Clinical Cancer Research, 14, 41–47.

    Article  PubMed  CAS  Google Scholar 

  61. Kondo, M., Ji, L., Kamibayashi, C., Tomizawa, Y., Randle, D., Sekido, Y., et al. (2001). Overexpression of candidate tumor suppressor gene FUS1 isolated from the 3p21.3 homozygous deletion region leads to G1 arrest and growth inhibition of lung cancer cells. Oncogene, 20, 6258–6262.

    Article  PubMed  CAS  Google Scholar 

  62. Hanahan, D., & Folkman, J. (1996). Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353–364.

    Article  PubMed  CAS  Google Scholar 

  63. Horn, L., & Sandler, A. B. (2009). Angiogenesis in the treatment of non-small cell lung cancer. The Proceedings of the American Thoracic Society, 6, 206–217.

    Article  CAS  Google Scholar 

  64. Kerbel, R. S. (2008). Tumor angiogenesis. New England Journal of Medicine, 358, 2039–2049.

    Article  PubMed  CAS  Google Scholar 

  65. Yang, W. J., Yang, D. D., Na, S., Sandusky, G. E., Zhang, Q., & Zhao, G. (2005). Dicer is required for embryonic angiogenesis during mouse development. Journal of Biological Chemistry, 280, 9330–9335.

    Article  PubMed  CAS  Google Scholar 

  66. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., et al. (2003). Dicer is essential for mouse development. Nature Genetics, 35, 215–217.

    Article  PubMed  CAS  Google Scholar 

  67. Suarez, Y., Fernandez-Hernando, C., Pober, J. S., & Sessa, W. C. (2007). Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circulation Research, 100, 1164–1173.

    Article  PubMed  CAS  Google Scholar 

  68. Kuehbacher, A., Urbich, C., Zeiher, A. M., & Dimmeler, S. (2007). Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circulation Research, 101, 59–68.

    Article  PubMed  CAS  Google Scholar 

  69. Suarez, Y., Fernandez-Hernando, C., Yu, J., Gerber, S. A., Harrison, K. D., Pober, J. S., et al. (2008). Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proceedings of the National Academy of Sciences of the United States of America, 105, 14082–14087.

    Article  PubMed  Google Scholar 

  70. Otsuka, M., Zheng, M., Hayashi, M., Lee, J. D., Yoshino, O., Lin, S., et al. (2008). Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. Journal of Clinical Investigation, 118, 1944–1954.

    Article  PubMed  CAS  Google Scholar 

  71. Shilo, S., Roy, S., Khanna, S., & Sen, C. K. (2008). Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 28, 471–477.

    Article  PubMed  CAS  Google Scholar 

  72. Fish, J. E., Santoro, M. M., Morton, S. U., Yu, S., Yeh, R. F., Wythe, J. D., et al. (2008). miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell, 15, 272–284.

    Article  PubMed  CAS  Google Scholar 

  73. Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., et al. (2008). The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell, 15, 261–271.

    Article  PubMed  CAS  Google Scholar 

  74. Kuhnert, F., Mancuso, M. R., Hampton, J., Stankunas, K., Asano, T., Chen, C. Z., et al. (2008). Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development, 135, 3989–3993.

    Article  PubMed  CAS  Google Scholar 

  75. Liu, B., Peng, X. C., Zheng, X. L., Wang, J., & Qin, Y. W. (2009). MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer, 66, 169–175.

    Article  PubMed  Google Scholar 

  76. Fish, J. E., & Srivastava, D. (2009). MicroRNAs: Opening a new vein in angiogenesis research. Science Signaling, 2, pe1.

    Article  PubMed  Google Scholar 

  77. Hua, Z., Lv, Q., Ye, W., Wong, C. K., Cai, G., Gu, D., et al. (2006). MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS ONE, 1, e116.

    Article  PubMed  CAS  Google Scholar 

  78. Dews, M., Homayouni, A., Yu, D., Murphy, D., Sevignani, C., Wentzel, E., et al. (2006). Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nature Genetics, 38, 1060–1065.

    Article  PubMed  CAS  Google Scholar 

  79. Poliseno, L., Tuccoli, A., Mariani, L., Evangelista, M., Citti, L., Woods, K., et al. (2006). MicroRNAs modulate the angiogenic properties of HUVECs. Blood, 108, 3068–3071.

    Article  PubMed  CAS  Google Scholar 

  80. Ruan, K., Fang, X., & Ouyang, G. (2009). MicroRNAs: Novel regulators in the hallmarks of human cancer. Cancer Letters, 285, 116–126.

    Article  PubMed  CAS  Google Scholar 

  81. Chen, Y., & Gorski, D. H. (2008). Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood, 111, 1217–1226.

    Article  PubMed  CAS  Google Scholar 

  82. Hurst, D. R., Edmonds, M. D., & Welch, D. R. (2009). Metastamir: The field of metastasis-regulatory microRNA is spreading. Cancer Research, 69, 7495–7498.

    Article  PubMed  CAS  Google Scholar 

  83. Savagner, P., Kusewitt, D. F., Carver, E. A., Magnino, F., Choi, C., Gridley, T., et al. (2005). Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. Journal of Cellular Physiology, 202, 858–866.

    Article  PubMed  CAS  Google Scholar 

  84. Liu, Y. (2004). Epithelial to mesenchymal transition in renal fibrogenesis: Pathologic significance, molecular mechanism, and therapeutic intervention. Journal of the American Society of Nephrology, 15, 1–12.

    Article  PubMed  CAS  Google Scholar 

  85. Thiery, J. P. (2002). Epithelial–mesenchymal transitions in tumour progression. Nature Reviews Cancer, 2, 442–454.

    Article  PubMed  CAS  Google Scholar 

  86. Ma, L., Teruya-Feldstein, J., & Weinberg, R. A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature, 449, 682–688.

    Article  PubMed  CAS  Google Scholar 

  87. Clark, E. A., Golub, T. R., Lander, E. S., & Hynes, R. O. (2000). Genomic analysis of metastasis reveals an essential role for RhoC. Nature, 406, 532–535.

    Article  PubMed  CAS  Google Scholar 

  88. Ma, L., & Weinberg, R. A. (2008). Micromanagers of malignancy: Role of microRNAs in regulating metastasis. Trends in Genetics, 24, 448–456.

    Article  PubMed  CAS  Google Scholar 

  89. Ciafre, S. A., Galardi, S., Mangiola, A., Ferracin, M., Liu, C. G., Sabatino, G., et al. (2005). Extensive modulation of a set of microRNAs in primary glioblastoma. Biochemical and Biophysical Research Communications, 334, 1351–1358.

    Article  PubMed  CAS  Google Scholar 

  90. Bloomston, M., Frankel, W. L., Petrocca, F., Volinia, S., Alder, H., Hagan, J. P., et al. (2007). MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA, 297, 1901–1908.

    Article  PubMed  CAS  Google Scholar 

  91. Roldo, C., Missiaglia, E., Hagan, J. P., Falconi, M., Capelli, P., Bersani, S., et al. (2006). MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. Journal of Clinical Oncology, 24, 4677–4684.

    Article  PubMed  CAS  Google Scholar 

  92. Huang, Q., Gumireddy, K., Schrier, M., le Sage, C., Nagel, R., Nair, S., et al. (2008). The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nature Cell Biology, 10, 202–210.

    Article  PubMed  CAS  Google Scholar 

  93. Goodison, S., Urquidi, V., & Tarin, D. (1999). CD44 cell adhesion molecules. Molecular Pathology, 52, 189–196.

    Article  PubMed  CAS  Google Scholar 

  94. Park, S. M., Gaur, A. B., Lengyel, E., & Peter, M. E. (2008). The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes and Development, 22, 894–907.

    Article  PubMed  CAS  Google Scholar 

  95. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., et al. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature Cell Biology, 10, 593–601.

    Article  PubMed  CAS  Google Scholar 

  96. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., et al. (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Reports, 9, 582–589.

    Article  PubMed  CAS  Google Scholar 

  97. Korpal, M., Lee, E. S., Hu, G., & Kang, Y. (2008). The miR-200 family inhibits epithelial–mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. Journal of Biological Chemistry, 283, 14910–14914.

    Article  PubMed  CAS  Google Scholar 

  98. Gibbons, D. L., Lin, W., Creighton, C. J., Rizvi, Z. H., Gregory, P. A., Goodall, G. J., et al. (2009). Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes and Development, 23, 2140–2151.

    Article  PubMed  CAS  Google Scholar 

  99. Tavazoie, S. F., Alarcon, C., Oskarsson, T., Padua, D., Wang, Q., Bos, P. D., et al. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature, 451, 147–152.

    Article  PubMed  CAS  Google Scholar 

  100. Crawford, M., Brawner, E., Batte, K., Yu, L., Hunter, M. G., Otterson, G. A., et al. (2008). MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochemical and Biophysical Research Communications, 373, 607–612.

    Article  PubMed  CAS  Google Scholar 

  101. Feller, S. M. (2001). Crk family adaptors-signalling complex formation and biological roles. Oncogene, 20, 6348–6371.

    Article  PubMed  CAS  Google Scholar 

  102. Kobashigawa, Y., Sakai, M., Naito, M., Yokochi, M., Kumeta, H., Makino, Y., et al. (2007). Structural basis for the transforming activity of human cancer-related signaling adaptor protein CRK. Nature Structural & Molecular Biology, 14, 503–510.

    Article  CAS  Google Scholar 

  103. Jansen, A. P., Camalier, C. E., & Colburn, N. H. (2005). Epidermal expression of the translation inhibitor programmed cell death 4 suppresses tumorigenesis. Cancer Research, 65, 6034–6041.

    Article  PubMed  CAS  Google Scholar 

  104. Chen, Y., Knosel, T., Kristiansen, G., Pietas, A., Garber, M. E., Matsuhashi, S., et al. (2003). Loss of PDCD4 expression in human lung cancer correlates with tumour progression and prognosis. Journal of Pathology, 200, 640–646.

    Article  PubMed  CAS  Google Scholar 

  105. Mudduluru, G., Medved, F., Grobholz, R., Jost, C., Gruber, A., Leupold, J. H., et al. (2007). Loss of programmed cell death 4 expression marks adenoma–carcinoma transition, correlates inversely with phosphorylated protein kinase B, and is an independent prognostic factor in resected colorectal cancer. Cancer, 110, 1697–1707.

    Article  PubMed  CAS  Google Scholar 

  106. Talotta, F., Cimmino, A., Matarazzo, M. R., Casalino, L., De Vita, G., D'Esposito, M., et al. (2009). An autoregulatory loop mediated by miR-21 and PDCD4 controls the AP-1 activity in RAS transformation. Oncogene, 28, 73–84.

    Article  PubMed  CAS  Google Scholar 

  107. Lee, Y. S., & Dutta, A. (2007). The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes and Development, 21, 1025–1030.

    Article  PubMed  CAS  Google Scholar 

  108. Wang, Y., & Lee, C. G. (2009). MicroRNA and cancer—Focus on apoptosis. Journal of Cellular and Molecular Medicine, 13, 12–23.

    Article  PubMed  CAS  Google Scholar 

  109. Hayashita, Y., Osada, H., Tatematsu, Y., Yamada, H., Yanagisawa, K., Tomida, S., et al. (2005). A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Research, 65, 9628–9632.

    Article  PubMed  CAS  Google Scholar 

  110. He, L., Thomson, J. M., Hemann, M. T., Hernando-Monge, E., Mu, D., Goodson, S., et al. (2005). A microRNA polycistron as a potential human oncogene. Nature, 435, 828–833.

    Article  PubMed  CAS  Google Scholar 

  111. Mendell, J. T. (2008). miRiad roles for the miR-17-92 cluster in development and disease. Cell, 133, 217–222.

    Article  PubMed  CAS  Google Scholar 

  112. Xiao, C., Srinivasan, L., Calado, D. P., Patterson, H. C., Zhang, B., Wang, J., et al. (2008). Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nature Immunology, 9, 405–414.

    Article  PubMed  CAS  Google Scholar 

  113. Sylvestre, Y., De Guire, V., Querido, E., Mukhopadhyay, U. K., Bourdeau, V., Major, F., et al. (2007). An E2F/miR-20a autoregulatory feedback loop. Journal of Biological Chemistry, 282, 2135–2143.

    Article  PubMed  CAS  Google Scholar 

  114. Bandi, N., Zbinden, S., Gugger, M., Arnold, M., Kocher, V., Hasan, L., et al. (2009). miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Research, 69, 5553–5559.

    Article  PubMed  CAS  Google Scholar 

  115. Chen, R. W., Bemis, L. T., Amato, C. M., Myint, H., Tran, H., Birks, D. K., et al. (2008). Truncation in CCND1 mRNA alters miR-16-1 regulation in mantle cell lymphoma. Blood, 112, 822–829.

    Article  PubMed  CAS  Google Scholar 

  116. Liu, Q., Fu, H., Sun, F., Zhang, H., Tie, Y., Zhu, J., et al. (2008). miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Research, 36, 5391–5404.

    Article  PubMed  CAS  Google Scholar 

  117. Bonci, D., Coppola, V., Musumeci, M., Addario, A., Giuffrida, R., Memeo, L., et al. (2008). The miR-15a–miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nature Medicine, 14, 1271–1277.

    Article  PubMed  CAS  Google Scholar 

  118. Garofalo, M., Quintavalle, C., Di Leva, G., Zanca, C., Romano, G., Taccioli, C., et al. (2008). MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer. Oncogene, 27, 3845–3855.

    Article  PubMed  CAS  Google Scholar 

  119. Frankel, L. B., Christoffersen, N. R., Jacobsen, A., Lindow, M., Krogh, A., & Lund, A. H. (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. Journal of Biological Chemistry, 283, 1026–1033.

    Article  PubMed  CAS  Google Scholar 

  120. Lu, Z., Liu, M., Stribinskis, V., Klinge, C. M., Ramos, K. S., Colburn, N. H., et al. (2008). MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene, 27, 4373–4379.

    Article  PubMed  CAS  Google Scholar 

  121. Calin, G. A., & Croce, C. M. (2006). MicroRNA signatures in human cancers. Nature Reviews Cancer, 6, 857–866.

    Article  PubMed  CAS  Google Scholar 

  122. Schetter, A. J., Leung, S. Y., Sohn, J. J., Zanetti, K. A., Bowman, E. D., Yanaihara, N., et al. (2008). MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA, 299, 425–436.

    Article  PubMed  CAS  Google Scholar 

  123. Takamizawa, J., Konishi, H., Yanagisawa, K., Tomida, S., Osada, H., Endoh, H., et al. (2004). Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Research, 64, 3753–3756.

    Article  PubMed  CAS  Google Scholar 

  124. Yu, S. L., Chen, H. Y., Chang, G. C., Chen, C. Y., Chen, H. W., Singh, S., et al. (2008). MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cells, 13, 48–57.

    Article  CAS  Google Scholar 

  125. Wang, Q. Z., Xu, W., Habib, N., & Xu, R. (2009). Potential uses of microRNA in lung cancer diagnosis, prognosis, and therapy. Current Cancer Drug Targets, 9, 572–594.

    Article  PubMed  CAS  Google Scholar 

  126. Weidhaas, J. B., Babar, I., Nallur, S. M., Trang, P., Roush, S., Boehm, M., et al. (2007). MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Research, 67, 11111–11116.

    Article  PubMed  CAS  Google Scholar 

  127. Ji, J., Shi, J., Budhu, A., Yu, Z., Forgues, M., Roessler, S., et al. (2009). MicroRNA expression, survival, and response to interferon in liver cancer. New England Journal of Medicine, 361, 1437–1447.

    Article  PubMed  CAS  Google Scholar 

  128. Ng, E. K., Chong, W. W., Jin, H., Lam, E. K., Shin, V. Y., Yu, J., et al. (2009). Differential expression of microRNAs in plasma of patients with colorectal cancer: A potential marker for colorectal cancer screening. Gut, 58, 1375–1381.

    Article  PubMed  CAS  Google Scholar 

  129. Lawrie, C. H., Gal, S., Dunlop, H. M., Pushkaran, B., Liggins, A. P., Pulford, K., et al. (2008). Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. British Journal Haematology, 141, 672–675.

    Article  Google Scholar 

  130. Lebanony, D., Benjamin, H., Gilad, S., Ezagouri, M., Dov, A., Ashkenazi, K., et al. (2009). Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. Journal of Clinical Oncology, 27, 2030–2037.

    Article  PubMed  CAS  Google Scholar 

  131. Liang, Y. (2008). An expression meta-analysis of predicted microRNA targets identifies a diagnostic signature for lung cancer. BMC Med Genomics, 1, 61.

    Article  PubMed  CAS  Google Scholar 

  132. Pavlidis, N., & Fizazi, K. (2005). Cancer of unknown primary (CUP). Critical Reviews in Oncology/Hematology, 54, 243–250.

    Article  PubMed  Google Scholar 

  133. 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.

    Article  PubMed  CAS  Google Scholar 

  134. Negrini, M., Nicoloso, M. S., & Calin, G. A. (2009). MicroRNAs and cancer—New paradigms in molecular oncology. Current Opinion in Cell Biology, 21, 470–479.

    Article  PubMed  CAS  Google Scholar 

  135. Wu, M., Jolicoeur, N., Li, Z., Zhang, L., Fortin, Y., L’Abbe, D., et al. (2008). Genetic variations of microRNAs in human cancer and their effects on the expression of miRNAs. Carcinogenesis, 29, 1710–1716.

    Article  PubMed  CAS  Google Scholar 

  136. Calin, G. A., Cimmino, A., Fabbri, M., Ferracin, M., Wojcik, S. E., Shimizu, M., et al. (2008). MiR-15a and miR-16-1 cluster functions in human leukemia. Proceedings of the National Academy of Sciences of the United States of America, 105, 5166–5171.

    Article  PubMed  Google Scholar 

  137. Krutzfeldt, J., Kuwajima, S., Braich, R., Rajeev, K. G., Pena, J., Tuschl, T., et al. (2007). Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Research, 35, 2885–2892.

    Article  PubMed  CAS  Google Scholar 

  138. Fontana, L., Fiori, M. E., Albini, S., Cifaldi, L., Giovinazzi, S., Forloni, M., et al. (2008). Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS ONE, 3, e2236.

    Article  PubMed  CAS  Google Scholar 

  139. Elmen, J., Lindow, M., Schutz, S., Lawrence, M., Petri, A., Obad, S., et al. (2008). LNA-mediated microRNA silencing in non-human primates. Nature, 452, 896–899.

    Article  PubMed  CAS  Google Scholar 

  140. Kota, J., Chivukula, R. R., O'Donnell, K. A., Wentzel, E. A., Montgomery, C. L., Hwang, H. W., et al. (2009). Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell, 137, 1005–1017.

    Article  PubMed  CAS  Google Scholar 

  141. Zhu, S., Si, M. L., Wu, H., & Mo, Y. Y. (2007). MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). Journal of Biological Chemistry, 282, 14328–14336.

    Article  PubMed  CAS  Google Scholar 

  142. Garofalo, M., Di Leva, G., Romano, G., Nuovo, G., Suh, S. S., Ngankeu, A., et al. (2009). miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell, 16, 498–509.

    Article  PubMed  CAS  Google Scholar 

  143. Sun, F., Fu, H., Liu, Q., Tie, Y., Zhu, J., Xing, R., et al. (2008). Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Letters, 582, 1564–1568.

    Article  PubMed  CAS  Google Scholar 

  144. Bommer, G. T., Gerin, I., Feng, Y., Kaczorowski, A. J., Kuick, R., Love, R. E., et al. (2007). p53-Mediated activation of miRNA34 candidate tumor-suppressor genes. Current Biology, 17, 1298–1307.

    Article  PubMed  CAS  Google Scholar 

  145. Welch, C., Chen, Y., & Stallings, R. L. (2007). MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene, 26, 5017–5022.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the technical assistance of Paul Card and thank Robert Borkowski for thoughtful insights and discussions and critical reading of the manuscript. This work was supported in part by Public Health Service grant no. P50 CA70907 from the UT Southwestern/MD Anderson Cancer Center Lung Specialized Program of Research Excellence (UTSW/MDACC Lung SPORE) and the National Cancer Institute and grant no. R01 CA129632 from the National Institutes of Health and the National Cancer Institute.

Author information

Authors and Affiliations

  1. Harold C. Simmons Comprehensive Cancer Center, The University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX, 75390-8807, USA

    Liqin Du

  2. Eugene McDermott Center for Human Growth and Development, The University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX, 75390-8591, USA

    Alexander Pertsemlidis

Authors
  1. Liqin Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Pertsemlidis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander Pertsemlidis.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s10555-010-9230-7

Rights and permissions

Reprints and permissions

About this article

Cite this article

Du, L., Pertsemlidis, A. microRNAs and lung cancer: tumors and 22-mers. Cancer Metastasis Rev 29, 109–122 (2010). https://doi.org/10.1007/s10555-010-9204-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-010-9204-9

Keywords

Search

Navigation