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1 Division of Molecular Oncology, Aichi Cancer Center Research Institute, Nagoya, Japan; Departments of 2 Anatomic and Molecular Diagnostic Pathology and 3 Thoracic Surgery, Aichi Cancer Center Hospital, Nagoya, Japan; 4 Division of Surgical Oncology, Department of Surgery, Nagoya University Graduate School of Medicine, Nagoya, Japan
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ABSTRACT |
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Introduction |
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70 nucleotide pre-miRNA with a characteristic hairpin structure from the longer nascent transcripts (pri-miRNA) and the following Dicer-mediated processing into mature forms (2, 3, 4, 5)
. Although thus far over 300 miRNA genes have been discovered in various organisms (6, 7, 8, 9, 10)
, including humans, their precise physiological functions are largely unknown except for a handful of miRNAs (11, 12, 13, 14, 15, 16, 17)
, and their potential pathological involvement including oncogenesis is yet to be explored. The Caenorhabditis elegans let-7miRNA is to date the best-studied example along with lin-4 of the same worm (11, 12, 13, 14, 15) , both of which were initially identified by genetic analysis of the developmental timing defects of mutants. The let-7 miRNA, which starts to be expressed during the late developmental stage, acts as a post-transcriptional repressor of lin-41, hbl-1/lin-57 and perhaps other genes that contain sequences imprecisely complementary to the miRNA in their 3' untranslated regions. The expression levels of the human let-7 gene have been shown to vary among various adult tissues, lung being one of the tissues with most abundant expression of let-7 (18) .
In this study, we show for the first time that expression levels of let-7 are frequently reduced in lung cancers both in vitro and in vivo. Furthermore, lung cancer patients with reduced let-7 expression were found to have significantly worse prognosis after potentially curative resection, and this prognostic impact of reduced let-7 expression appears to be independent of disease stage in multivariate COX regression analysis. In addition, we show that overexpression of let-7 inhibits growth of lung cancer cells in vitro.
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Materials and Methods |
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Preparation of Cell Line and Tissue Samples.
All of the human NSCLC cell lines analyzed were cultured with 5% (v/v) FCS-containing RPMI 1640 at 37°C with 5% CO2. BEAS-2B and HPL1D (19)
cells were cultured with 1% (v/v) FCS-containing Ham’s F-12 supplemented with bovine insulin (5 µg/ml), human transferrin (5 µg/ml), 10–7 M hydrocortisone, 2 x 10–10 M triiode thyronine, penicillin (100 IU/ml), and streptomycin (100 µg/ml) at 37°C with 5% CO2. The tumor specimens were homogenized in guanidine isothiocyanate homogenization buffer immediately after resection and stored at –30°C until use with the approval of the institutional review board. Processing of all cell lines and tissue samples for RNA extraction were performed according to the standard procedures.
Northern Blotting.
Ten µg of RNA were separated on a 15% denaturing polyacrylamide gel. The RNA was then transferred to Zeta-Probe GT Blotting Membranes electrophoretically overnight. Probes (let-7; 5'-TACTATACAACCTACTACCTCAATTTGCC and 5S; 5'-TTAGCTTCCGAGATCAGACGA) were generated by T4 polynucleotide kinase (New England Biolabs, Beverly, MA) mediated end-labeling of DNA oligonucleotides with [
-32P]ATP. Prehybridization and hybridization were carried out using hybridization buffer (0.25 M sodium phosphate (pH 7.2), 7% SDS, 0.5% sodium PPI). The most stringent wash was carried out in 2x SSC and 1% SDS at 37.5°C.
Real-Time Reverse Transcription-PCR.
Real-time reverse transcription-PCR was performed using an ABI Prism 7900 Sequence Detection System (Perkin-Elmer Applied Biosystems, Foster City, CA), the SYBR Green PCR Master Mix (Perkin-Elmer Applied Biosystems), and random-primed cDNAs (corresponding to 20 ng of total RNA extracted from tissue samples).
The primer pairs used were let-7a-1S (sense; 5'-CCTGGATGTTCTCTTCACTG) and let-7a-1AS (antisense; 5'-GCCTGGATGCAGACTTTTCT); let-7a-2S (sense; 5'-TTCCAGCCATTGTGACTGCA) and let-7a-2AS (antisense; 5'-CTCACCATGTTGTTTAGTGC); let-7a-3S (sense; 5'-ACCAAGACCGACTGCCCTTT) and let-7a-3AS (antisense; 5'-CTCTGTCCACCGCAGATATT); let-7f-1S (sense; 5'-TGTACTTTCCATTCCAGAAG) and let-7f-1AS (antisense; 5'-TAATGCAGCAAGTCTACTCC); let-7f-2S (sense; 5'-TGAAGATGGACACTGGTGCT) and let-7f-2AS (antisense; 5'-CAGTCGGAGAAGAAGTGTAC); and 5S–S (sense; 5'-TACGGCCATACCACCCTGAA) and 5S-AS (antisense; 5'-TAACCAGGCCCGACCCTGCT). To quantify the expression level of the let-7 genes, standard curves were made using serially diluted pBluescriptIISK (–) inserted with each PCR product into the EcoRV site. PCR amplification consisted of 55 cycles (95°C for 30 s, 56°C to 60°C optimized for each primer set for 30 s and 72°C for 15 s) after the initial denaturation step (95°C for 10 min). Expression levels of the let-7 genes were based on the amount of the target message relative to the 5S rRNA control, to normalize the initial input of total RNA.
Hierarchical Clustering.
We used the Eisen CLUSTER and TREEVIEW programs for hierarchical clustering and visualization of data sets. Before applying the clustering algorithm, we log-transformed the fluorescence ratio for each expression and then average centered the data for all samples. Agglomerative hierarchical clustering was applied using the complete linkage method to investigate whether there was evidence for natural groupings of tumor samples based on correlations between gene-expression profiles.
Statistical Analysis.
The Kaplan-Meier method was used to estimate survival as a function of time, and survival differences were analyzed by the log-rank test. Cox regression analysis of factors potentially related to survival was performed to identify which independent factors might jointly have a significant influence on survival.
Colony Formation Assay.
The let-7 expression construct and a control plasmid were constructed by the cloning of annealed oligonucleotides of let-7a (sense, 5'-GATCCCCTGAGGTAGTAGGTTGTATAGTTTTT and antisense, 5'-AGCTAAAAACTATACAACCTACTACCTCAGGG), let-7f (sense, 5'-GATCCCCTGAGGTAGTAGATTGTATAGTTTTT and antisense, 5'-AGCTAAAAACTATACAATCTACTACCTCAGGG), or control (sense, 5'-GATCCCCTTTTTTTTGGAAA and antisense, 5'-AGCTTTTCCAAAAAAAAGGG) into pH1-RNApuro, in which expression of a gene is under the control of the RNA polymerase III H1-RNA gene promoter prepared by PCR amplification of human genomic DNA. The let-7a and -7f expression constructs were transfected into A549 lung adenocarcinoma cell line using the FuGENE 6 reagent (Roche, Inc. Basel, Switzerland) according to the manufacturer’s instructions. Cells were selected by the addition of puromycin (2 µg/ml) 3 days after the transfection and cultured at 37°C for 2 weeks. After 2 weeks of puromycin selection, the plates were stained with Giemsa and scored for the number of resistant colonies.
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Results |
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. The mature form of let-7 miRNA was readily detectable in both immortalized lung epithelial cell lines at a level comparable with that in normal lung tissues. In marked contrast, a significant reduction (>80%) in the expression levels of let-7 was observed in 60% (12 of 20) of lung cancer cell lines. Expression levels of let-7 in primary human lung cancer tissues taken directly from surgically treated patients, in which sufficient RNA were available, were further analyzed by Northern blot analysis. Consequently, 44% (7 of 16) of the cases examined were found to exhibit >80% reduction in let-7 expression when compared with that in the corresponding normal lung tissues (Fig. 1B)
. A more frequent occurrence of reduced let-7 expression in cell lines in vitro may be related to the inevitable contamination of normal stromal/inflammatory cells in tumor tissues in vivo or, alternatively, this may reflect in vitro selection of cells with reduced let-7 in the process of the establishment of cell lines. These findings thus clearly showed the frequent occurrence of a significant reduction in let-7 miRNA expression in lung cancers.
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. Except for a significant association between cluster 1 with low let-7 expression and higher disease stages (P = 0.004 by the
2 test), no other significant associations were found between the clusters and various clinicopathological features including age, sex, histology, primary tumor status (pT), and differentiation grade. Of special interest was a striking difference in the postoperative survival of patients between the two clusters. The Kaplan-Meier survival curves demonstrated that patients belonging to cluster 1 were at a significantly greater risk of an earlier death than those classified as cluster 2 (P = 0.0003 by the log-rank test; Fig. 2B
). A separate study analyzed the prognostic significance of let-7 in adenocarcinomas, which constitute the major proportion of lung cancers in Japan as well as in other countries such as the United States. We found that adenocarcinoma cases can also be divided into two major clusters, again showing that patients in cluster 1AD with low let-7 expression had significantly shorter survival than those in cluster 2AD with high let-7 expression (P = 0.03 by the log-rank test; Fig. 2, C and D
).
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), classification into cluster 1 with characteristically low let-7 expression is a significant predictive factor for poor prognosis (P < 0.001). Cox proportional hazards modeling was then conducted to identify which independent factors would jointly have a significant influence on survival (Table 1)
. The inter-relationship of possible prognostic factors and survival was analyzed, using age, sex, histological type, smoking history, disease stage, and the let-7-defined cluster as variables, resulting in the identification of let-7-defined cluster as a significant, independent prognostic factor in surgically treated NSCLC patients after potentially curative resection (P = 0.009) in addition to disease stage (P < 0.001). The hazard ratio of earlier death was 2.17 (95% confidence interval, 1.21–3.89) for clusters 1 versus 2 and 3.49 (95% confidence interval, 1.89–6.42) for pathological stage II/III versus pathological stage I. Taken together, expression levels of let-7 seemed to have a significant impact on the postoperative survival of NSCLC patients.
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. Overexpression of let-7f in A549 lung adenocarcinoma cell line resulted in a 78.6% reduction in the number of colonies, whereas the introduction of let-7a also showed similar but a more modest growth-inhibitory effect (Figs. 3, B and C)
. Similar results were obtained in five independent experiments, which were done in triplicate using three independent preparations of plasmid DNAs.
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Discussion |
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Very little information is available at the moment with regard to the potential pathological roles of miRNAs. Two proteins (Gemin 3 and Gemin 4), which are components of the protein complex related to spinal muscular atrophy, are also known to be components of a ribonucleoprotein complex containing miRNAs (microRNP; Ref. 9 ), whereas the Drosophila homologue of fragile X mental retardation protein has been shown to be a component of RNA-induced silencing complex/microRNPs (20 , 21) . This circumstantial evidence suggests the possibility of the involvement of miRNA machineries in these diseases. As for links between cancer and miRNA, Calin et al. (22) reported frequent down-regulation of miR15 and miR16 in chronic lymphocytic leukemia, whereas Michael et al. (23) recently reported reduced expression of miR-143 and miR-145 in human colon cancers. In contrast to these studies, which did not address the question of whether reduced expression of miRNAs has any influence on clinicopathological features, this study clearly shows that reduced let-7 expression is indeed significantly associated with the shortened survival of patients. Because no changes in let-7 expression were reported in colon cancers (23) , it is possible that miRNAs may be distinctly involved in the pathogenesis of these two most common cancers of adults and possibly in other types of human cancers.
It has been shown that the let-7 gene regulates developmental timing in C. elegans and that mutant worms lacking let-7 fail to properly execute a larval-to-adult switch in hypodermal cell development (13) . Although lin-41 is known to be post-transcriptionally repressed by let-7 (24) , it is not inconceivable that other genes may also be targeted by let-7, because of the requirement of imprecise base-pairing for miRNA-mediated translational repression (1) . Indeed, hbl-1/lin-57 was recently reported to be targeted by let-7 (14 , 15) , whereas a few additional genes have also been predicted to be a potential target for let-7 (24 , 25) . Interestingly, such potential targets include LIM kinase 2 (25) , which belongs to a gene family having a role in the regulation of cell shape and motility as well as possibly in metastasis. One could speculate that the change in miRNA expression as is seen in this study might be an efficient strategy for cancer cells to simultaneously alter the expression profile of a series of genes. Alterations in miRNA expression may accordingly confer cancer cells with selective growth advantage, allowing them to form a distant metastasis and resulting in the consequential death of the patient. This scheme may be consistent with the present finding of the significant prognostic impact of let-7 expression. One might argue that reduced expression of let-7 in lung cancers may merely reflect its oncofetal regulation, because fetal lung exhibited considerably lower let-7 expression than adult lung (data not shown). However, growth-inhibitory effects of overexpressed let-7 in A549 adenocarcinoma cell line argue against this possibility. Taken together, these findings suggest the potential involvement of reduction in let-7 expression in the pathogenesis of this fatal disease, although the results obtained with overexpression of mature miRNA need to be interpreted cautiously and await further experimental clarification.
In this study, we observed that various let-7 pri-miRNA isoforms were coordinately regulated, let-7a-1 and let-7f-1 being the most predominant. In this connection, it should be noted that some of the let-7 pri-miRNAs give rise to identical mature miRNA isoforms, and the others may also have presumably very similar, if not identical, spectra of the target genes (6) . It is uncertain at the moment how the expression levels of various let-7 isoforms are coordinated, and this remains an intriguing question awaiting further investigation.
In conclusion, we have shown for the first time that let-7 expression is frequently reduced in lung cancers and that alterations in the miRNA expression may have a prognostic impact on the survival of surgically treated lung cancer patients. These findings warrant additional studies to investigate whether let-7 alterations are also involved in other types of human cancers and how altered miRNA expression would manifest the biological and biochemical consequences in the development of human cancers. Accordingly, future identification of the downstream targets for let-7 may provide clues to develop a novel therapeutic means. It is envisaged that such future studies may ultimately provide a foundation for a new paradigm of the involvement of noncoding small RNA species, miRNA, in human oncogenesis.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Note: J. Takamizawa and H. Konishi contributed equally to the present study. H. Konishi is currently at the Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD.
Requests for reprints: Takashi Takahashi, Division of Molecular Oncology, Aichi Cancer Center Research Institute, 1-1 Kanokoden, Chikusa-ku, Nagoya, 464-8681, Japan. Phone: 81-52-764-2983; Fax: 81-52-764-2983; E-mail: tak{at}aichi-cc.jp
Received 2/21/04. Revised 4/ 9/04. Accepted 4/19/04.
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 S. Kalscheuer, X. Zhang, Y. Zeng, and P. Upadhyaya Differential expression of microRNAs in early-stage neoplastic transformation in the lungs of F344 rats chronically treated with the tobacco carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone Carcinogenesis, December 1, 2008; 29(12): 2394 - 2399. [Abstract] [Full Text] [PDF]
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M. W. Nasser, J. Datta, G. Nuovo, H. Kutay, T. Motiwala, S. Majumder, B. Wang, S. Suster, S. T. Jacob, and K. Ghoshal Down-regulation of Micro-RNA-1 (miR-1) in Lung Cancer: SUPPRESSION OF TUMORIGENIC PROPERTY OF LUNG CANCER CELLS AND THEIR SENSITIZATION TO DOXORUBICIN-INDUCED APOPTOSIS BY miR-1 J. Biol. Chem., November 28, 2008; 283(48): 33394 - 33405. [Abstract] [Full Text] [PDF]
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M. L. Yeung, J.-i. Yasunaga, Y. Bennasser, N. Dusetti, D. Harris, N. Ahmad, M. Matsuoka, and K.-T. Jeang Roles for MicroRNAs, miR-93 and miR-130b, and Tumor Protein 53-Induced Nuclear Protein 1 Tumor Suppressor in Cell Growth Dysregulation by Human T-Cell Lymphotrophic Virus 1 Cancer Res., November 1, 2008; 68(21): 8976 - 8985. [Abstract] [Full Text] [PDF]
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L.-X. Yan, X.-F. Huang, Q. Shao, M.-Y. Huang, L. Deng, Q.-L. Wu, Y.-X. Zeng, and J.-Y. Shao MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis RNA, November 1, 2008; 14(11): 2348 - 2360. [Abstract] [Full Text] [PDF]
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S. Tokumaru, M. Suzuki, H. Yamada, M. Nagino, and T. Takahashi let-7 regulates Dicer expression and constitutes a negative feedback loop Carcinogenesis, November 1, 2008; 29(11): 2073 - 2077. [Abstract] [Full Text] [PDF]
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L. J. Chin, E. Ratner, S. Leng, R. Zhai, S. Nallur, I. Babar, R.-U. Muller, E. Straka, L. Su, E. A. Burki, et al. A SNP in a let-7 microRNA Complementary Site in the KRAS 3' Untranslated Region Increases Non-Small Cell Lung Cancer Risk Cancer Res., October 15, 2008; 68(20): 8535 - 8540. [Abstract] [Full Text] [PDF]
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S.-P. Chan, G. Ramaswamy, E.-Y. Choi, and F. J. Slack Identification of specific let-7 microRNA binding complexes in Caenorhabditis elegans RNA, October 1, 2008; 14(10): 2104 - 2114. [Abstract] [Full Text] [PDF]
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 A. Markou, E. G. Tsaroucha, L. Kaklamanis, M. Fotinou, V. Georgoulias, and E. S. Lianidou Prognostic Value of Mature MicroRNA-21 and MicroRNA-205 Overexpression in Non-Small Cell Lung Cancer by Quantitative Real-Time RT-PCR Clin. Chem., October 1, 2008; 54(10): 1696 - 1704. [Abstract] [Full Text] [PDF]
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M. Yamakuchi, M. Ferlito, and C. J. Lowenstein miR-34a repression of SIRT1 regulates apoptosis PNAS, September 9, 2008; 105(36): 13421 - 13426. [Abstract] [Full Text] [PDF]
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M. Wu, N. Jolicoeur, Z. Li, L. Zhang, Y. Fortin, D. L'Abbe, Z. Yu, and S.-H. Shen Genetic variations of microRNAs in human cancer and their effects on the expression of miRNAs Carcinogenesis, September 1, 2008; 29(9): 1710 - 1716. [Abstract] [Full Text] [PDF]
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W. Tam The Emergent Role of MicroRNAs in Molecular Diagnostics of Cancer J. Mol. Diagn., September 1, 2008; 10(5): 411 - 414. [Abstract] [Full Text] [PDF]
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 Z. Yu, C. Wang, M. Wang, Z. Li, M. C. Casimiro, M. Liu, K. Wu, J. Whittle, X. Ju, T. Hyslop, et al. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation J. Cell Biol., August 11, 2008; 182(3): 509 - 517. [Abstract] [Full Text] [PDF]
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E. Piskounova, S. R. Viswanathan, M. Janas, R. J. LaPierre, G. Q. Daley, P. Sliz, and R. I. Gregory Determinants of MicroRNA Processing Inhibition by the Developmentally Regulated RNA-binding Protein Lin28 J. Biol. Chem., August 1, 2008; 283(31): 21310 - 21314. [Abstract] [Full Text] [PDF]
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A. Taguchi, K. Yanagisawa, M. Tanaka, K. Cao, Y. Matsuyama, H. Goto, and T. Takahashi Identification of Hypoxia-Inducible Factor-1{alpha} as a Novel Target for miR-17-92 MicroRNA Cluster Cancer Res., July 15, 2008; 68(14): 5540 - 5545. [Abstract] [Full Text] [PDF]
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M. Jongen-Lavrencic, S. M. Sun, M. K. Dijkstra, P. J. M. Valk, and B. Lowenberg MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia Blood, May 15, 2008; 111(10): 5078 - 5085. [Abstract] [Full Text] [PDF]
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Y. Wang, A. T. C. Lee, J. Z. I. Ma, J. Wang, J. Ren, Y. Yang, E. Tantoso, K.-B. Li, L. L. P. J Ooi, P. Tan, et al. Profiling MicroRNA Expression in Hepatocellular Carcinoma Reveals MicroRNA-224 Up-regulation and Apoptosis Inhibitor-5 as a MicroRNA-224-specific Target J. Biol. Chem., May 9, 2008; 283(19): 13205 - 13215. [Abstract] [Full Text] [PDF]
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J.-W. Lee, C. H. Choi, J.-J. Choi, Y.-A. Park, S.-J. Kim, S. Y. Hwang, W. Y. Kim, T.-J. Kim, J.-H. Lee, B.-G. Kim, et al. Altered MicroRNA Expression in Cervical Carcinomas Clin. Cancer Res., May 1, 2008; 14(9): 2535 - 2542. [Abstract] [Full Text] [PDF]
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E. J. Nam, H. Yoon, S. W. Kim, H. Kim, Y. T. Kim, J. H. Kim, J. W. Kim, and S. Kim MicroRNA Expression Profiles in Serous Ovarian Carcinoma Clin. Cancer Res., May 1, 2008; 14(9): 2690 - 2695. [Abstract] [Full Text] [PDF]
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S. Sengupta, J. A. den Boon, I-H. Chen, M. A. Newton, S. A. Stanhope, Y.-J. Cheng, C.-J. Chen, A. Hildesheim, B. Sugden, and P. Ahlquist MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins PNAS, April 15, 2008; 105(15): 5874 - 5878. [Abstract] [Full Text] [PDF]
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K. Motoyama, H. Inoue, Y. Nakamura, H. Uetake, K. Sugihara, and M. Mori Clinical Significance of High Mobility Group A2 in Human Gastric Cancer and Its Relationship to let-7 MicroRNA Family Clin. Cancer Res., April 15, 2008; 14(8): 2334 - 2340. [Abstract] [Full Text] [PDF]
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 G. A. Calin and C. M. Croce MicroRNA-Cancer Connection: The Beginning of a New Tale Am. Assoc. Cancer Res. Educ. Book, April 12, 2008; 2008(1): 667 - 675. [Abstract] [Full Text] [PDF]
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 S.-M. Park, A. B. Gaur, E. Lengyel, and M. E. Peter The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2 Genes & Dev., April 1, 2008; 22(7): 894 - 907. [Abstract] [Full Text] [PDF]
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Y. Peng, J. Laser, G. Shi, K. Mittal, J. Melamed, P. Lee, and J.-J. Wei Antiproliferative Effects by Let-7 Repression of High-Mobility Group A2 in Uterine Leiomyoma Mol. Cancer Res., April 1, 2008; 6(4): 663 - 673. [Abstract] [Full Text] [PDF]
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M. S. Kumar, S. J. Erkeland, R. E. Pester, C. Y. Chen, M. S. Ebert, P. A. Sharp, and T. Jacks Suppression of non-small cell lung tumor development by the let-7 microRNA family PNAS, March 11, 2008; 105(10): 3903 - 3908. [Abstract] [Full Text] [PDF]
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D. Landi, F. Gemignani, A. Naccarati, B. Pardini, P. Vodicka, L. Vodickova, J. Novotny, A. Forsti, K. Hemminki, F. Canzian, et al. Polymorphisms within micro-RNA-binding sites and risk of sporadic colorectal cancer Carcinogenesis, March 1, 2008; 29(3): 579 - 584. [Abstract] [Full Text] [PDF]
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K. Huppi, N. Volfovsky, T. Runfola, T. L. Jones, M. Mackiewicz, S. E. Martin, J. F. Mushinski, R. Stephens, and N. J. Caplen The Identification of MicroRNAs in a Genomically Unstable Region of Human Chromosome 8q24 Mol. Cancer Res., February 1, 2008; 6(2): 212 - 221. [Abstract] [Full Text] [PDF]
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H. Yang, W. Kong, L. He, J.-J. Zhao, J. D. O'Donnell, J. Wang, R. M. Wenham, D. Coppola, P. A. Kruk, S. V. Nicosia, et al. MicroRNA Expression Profiling in Human Ovarian Cancer: miR-214 Induces Cell Survival and Cisplatin Resistance by Targeting PTEN Cancer Res., January 15, 2008; 68(2): 425 - 433. [Abstract] [Full Text] [PDF]
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J. Jiang, Y. Gusev, I. Aderca, T. A. Mettler, D. M. Nagorney, D. J. Brackett, L. R. Roberts, and T. D. Schmittgen Association of MicroRNA Expression in Hepatocellular Carcinomas with Hepatitis Infection, Cirrhosis, and Patient Survival Clin. Cancer Res., January 15, 2008; 14(2): 419 - 427. [Abstract] [Full Text] [PDF]
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Y. Guo, Z. Chen, L. Zhang, F. Zhou, S. Shi, X. Feng, B. Li, X. Meng, X. Ma, M. Luo, et al. Distinctive MicroRNA Profiles Relating to Patient Survival in Esophageal Squamous Cell Carcinoma Cancer Res., January 1, 2008; 68(1): 26 - 33. [Abstract] [Full Text] [PDF]
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J. B. Weidhaas, I. Babar, S. M. Nallur, P. Trang, S. Roush, M. Boehm, E. Gillespie, and F. J. Slack MicroRNAs as Potential Agents to Alter Resistance to Cytotoxic Anticancer Therapy Cancer Res., December 1, 2007; 67(23): 11111 - 11116. [Abstract] [Full Text] [PDF]
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D. Ovcharenko, K. Kelnar, C. Johnson, N. Leng, and D. Brown Genome-Scale MicroRNA and Small Interfering RNA Screens Identify Small RNA Modulators of TRAIL-Induced Apoptosis Pathway Cancer Res., November 15, 2007; 67(22): 10782 - 10788. [Abstract] [Full Text] [PDF]
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S. U. Mertens-Talcott, S. Chintharlapalli, X. Li, and S. Safe The Oncogenic microRNA-27a Targets Genes That Regulate Specificity Protein Transcription Factors and the G2-M Checkpoint in MDA-MB-231 Breast Cancer Cells Cancer Res., November 15, 2007; 67(22): 11001 - 11011. [Abstract] [Full Text] [PDF]
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L. Lu, D. Katsaros, I. A. Rigault de la Longrais, O. Sochirca, and H. Yu Hypermethylation of let-7a-3 in Epithelial Ovarian Cancer Is Associated with Low Insulin-like Growth Factor-II Expression and Favorable Prognosis Cancer Res., November 1, 2007; 67(21): 10117 - 10122. [Abstract] [Full Text] [PDF]
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J.-W. Cui, Y.-J. Li, A. Sarkar, J. Brown, Y.-H. Tan, M. Premyslova, C. Michaud, N. Iscove, G.-J. Wang, and Y. Ben-David Retroviral insertional activation of the Fli-3 locus in erythroleukemias encoding a cluster of microRNAs that convert Epo-induced differentiation to proliferation Blood, October 1, 2007; 110(7): 2631 - 2640. [Abstract] [Full Text] [PDF]
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M. Kruhoffer, L. Dyrskjot, T. Voss, R. L.P. Lindberg, R. Wyrich, T. Thykjaer, and T. F. Orntoft Isolation of Microarray-Grade Total RNA, MicroRNA, and DNA from a Single PAXgene Blood RNA Tube J. Mol. Diagn., September 1, 2007; 9(4): 452 - 458. [Abstract] [Full Text] [PDF]
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W. Zhang, J. E. Dahlberg, and W. Tam MicroRNAs in Tumorigenesis: A Primer Am. J. Pathol., September 1, 2007; 171(3): 728 - 738. [Abstract] [Full Text] [PDF]
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C. D. Johnson, A. Esquela-Kerscher, G. Stefani, M. Byrom, K. Kelnar, D. Ovcharenko, M. Wilson, X. Wang, J. Shelton, J. Shingara, et al. The let-7 MicroRNA Represses Cell Proliferation Pathways in Human Cells Cancer Res., August 15, 2007; 67(16): 7713 - 7722. [Abstract] [Full Text] [PDF]
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S. Galardi, N. Mercatelli, E. Giorda, S. Massalini, G. V. Frajese, S. A. Ciafre, and M. G. Farace miR-221 and miR-222 Expression Affects the Proliferation Potential of Human Prostate Carcinoma Cell Lines by Targeting p27Kip1 J. Biol. Chem., August 10, 2007; 282(32): 23716 - 23724. [Abstract] [Full Text] [PDF]
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Z. Yu, Z. Li, N. Jolicoeur, L. Zhang, Y. Fortin, E. Wang, M. Wu, and S.-H. Shen Aberrant allele frequencies of the SNPs located in microRNA target sites are potentially associated with human cancers Nucleic Acids Res., July 26, 2007; 35(13): 4535 - 4541. [Abstract] [Full Text] [PDF]
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S. Shell, S.-M. Park, A. R. Radjabi, R. Schickel, E. O. Kistner, D. A. Jewell, C. Feig, E. Lengyel, and M. E. Peter Let-7 expression defines two differentiation stages of cancer PNAS, July 3, 2007; 104(27): 11400 - 11405. [Abstract] [Full Text] [PDF]
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W.-O. Lui, N. Pourmand, B. K. Patterson, and A. Fire Patterns of Known and Novel Small RNAs in Human Cervical Cancer Cancer Res., July 1, 2007; 67(13): 6031 - 6043. [Abstract] [Full Text] [PDF]
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L. Gramantieri, M. Ferracin, F. Fornari, A. Veronese, S. Sabbioni, C.-G. Liu, G. A. Calin, C. Giovannini, E. Ferrazzi, G. L. Grazi, et al. Cyclin G1 Is a Target of miR-122a, a MicroRNA Frequently Down-regulated in Human Hepatocellular Carcinoma Cancer Res., July 1, 2007; 67(13): 6092 - 6099. [Abstract] [Full Text] [PDF]
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K. P. Porkka, M. J. Pfeiffer, K. K. Waltering, R. L. Vessella, T. L.J. Tammela, and T. Visakorpi MicroRNA Expression Profiling in Prostate Cancer Cancer Res., July 1, 2007; 67(13): 6130 - 6135. [Abstract] [Full Text] [PDF]
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S. Landais, S. Landry, P. Legault, and E. Rassart Oncogenic Potential of the miR-106-363 Cluster and Its Implication in Human T-Cell Leukemia Cancer Res., June 15, 2007; 67(12): 5699 - 5707. [Abstract] [Full Text] [PDF]
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Y. M. Shah, K. Morimura, Q. Yang, T. Tanabe, M. Takagi, and F. J. Gonzalez Peroxisome Proliferator-Activated Receptor {alpha} Regulates a MicroRNA-Mediated Signaling Cascade Responsible for Hepatocellular Proliferation Mol. Cell. Biol., June 15, 2007; 27(12): 4238 - 4247. [Abstract] [Full Text] [PDF]
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 M. Negrini, M. Ferracin, S. Sabbioni, and C. M. Croce MicroRNAs in human cancer: from research to therapy J. Cell Sci., June 1, 2007; 120(11): 1833 - 1840. [Abstract] [Full Text] [PDF]
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S. Zhu, M.-L. Si, H. Wu, and Y.-Y. Mo MicroRNA-21 Targets the Tumor Suppressor Gene Tropomyosin 1 (TPM1) J. Biol. Chem., May 11, 2007; 282(19): 14328 - 14336. [Abstract] [Full Text] [PDF]
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C. Sevignani, G. A. Calin, S. C. Nnadi, M. Shimizu, R. V. Davuluri, T. Hyslop, P. Demant, C. M. Croce, and L. D. Siracusa MicroRNA genes are frequently located near mouse cancer susceptibility loci PNAS, May 8, 2007; 104(19): 8017 - 8022. [Abstract] [Full Text] [PDF]
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A. R.J. Young and M. Narita Oncogenic HMGA2: short or small? Genes & Dev., May 1, 2007; 21(9): 1005 - 1009. [Full Text] [PDF]
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Y. S. Lee and A. Dutta The tumor suppressor microRNA let-7 represses the HMGA2 oncogene Genes & Dev., May 1, 2007; 21(9): 1025 - 1030. [Abstract] [Full Text] [PDF]
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B. Zhou, S. Wang, C. Mayr, D. P. Bartel, and H. F. Lodish miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely PNAS, April 24, 2007; 104(17): 7080 - 7085. [Abstract] [Full Text] [PDF]
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N. Yanaihara, M. Seike, A. Schetter, C.M. Croce, and C.C. Harris MicroRNA Molecular Profiles in Cancer Diagnosis and Prognosis Am. Assoc. Cancer Res. Educ. Book, April 14, 2007; 2007(1): 125 - 126. [Full Text] [PDF]
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F. Meng, R. Henson, H. Wehbe-Janek, H. Smith, Y. Ueno, and T. Patel The MicroRNA let-7a Modulates Interleukin-6-dependent STAT-3 Survival Signaling in Malignant Human Cholangiocytes J. Biol. Chem., March 16, 2007; 282(11): 8256 - 8264. [Abstract] [Full Text] [PDF]
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 C. Mayr, M. T. Hemann, and D. P. Bartel Disrupting the Pairing Between let-7 and Hmga2 Enhances Oncogenic Transformation Science, March 16, 2007; 315(5818): 1576 - 1579. [Abstract] [Full Text] [PDF]
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B. Brueckner, C. Stresemann, R. Kuner, C. Mund, T. Musch, M. Meister, H. Sultmann, and F. Lyko The Human let-7a-3 Locus Contains an Epigenetically Regulated MicroRNA Gene with Oncogenic Function Cancer Res., February 15, 2007; 67(4): 1419 - 1423. [Abstract] [Full Text] [PDF]
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N. Yosef, Z. Yakhini, A. Tsalenko, V. Kristensen, A.-L. Borresen-Dale, E. Ruppin, and R. Sharan A supervised approach for identifying discriminating genotype patterns and its application to breast cancer data Bioinformatics, January 15, 2007; 23(2): e91 - e98. [Abstract] [Full Text] [PDF]
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K. V. Prasanth and D. L. Spector Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum Genes & Dev., January 1, 2007; 21(1): 11 - 42. [Abstract] [Full Text] [PDF]
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H. Osada and T. Takahashi MicroRNAs in biological processes and carcinogenesis Carcinogenesis, January 1, 2007; 28(1): 2 - 12. [Abstract] [Full Text] [PDF]
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N. Sugito, H. Ishiguro, Y. Kuwabara, M. Kimura, A. Mitsui, H. Kurehara, T. Ando, R. Mori, N. Takashima, R. Ogawa, et al. RNASEN Regulates Cell Proliferation and Affects Survival in Esophageal Cancer Patients Clin. Cancer Res., December 15, 2006; 12(24): 7322 - 7328. [Abstract] [Full Text] [PDF]
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