MicroRNAs accurately identify cancer tissue origin (original) (raw)

References

1. Pimiento, J.M., Teso, D., Malkan, A., Dudrick, S.J. & Palesty, J.A. Cancer of unknown primary origin: a decade of experience in a community-based hospital. Am. J. Surg. 194, 833–7, discussion 837–8 (2007).
   Article PubMed Google Scholar
2. Shaw, P.H., Adams, R., Jordan, C. & Crosby, T.D. A clinical review of the investigation and management of carcinoma of unknown primary in a single cancer network. Clin. Oncol. (R. Coll. Radiol.) 19, 87–95 (2007).
   Article CAS Google Scholar
3. Hainsworth, J.D. & Greco, F.A. Treatment of patients with cancer of an unknown primary site. N. Engl. J. Med. 329, 257–263 (1993).
   Article CAS PubMed Google Scholar
4. Blaszyk, H., Hartmann, A. & Bjornsson, J. Cancer of unknown primary: clinicopathologic correlations. APMIS 111, 1089–1094 (2003).
   Article PubMed Google Scholar
5. Varadhachary, G.R., Abbruzzese, J.L. & Lenzi, R. Diagnostic strategies for unknown primary cancer. Cancer 100, 1776–1785 (2004).
   Article CAS PubMed Google Scholar
6. Ramaswamy, S. et al. Multiclass cancer diagnosis using tumor gene expression signatures. Proc. Natl. Acad. Sci. USA 98, 15149–15154 (2001).
   Article CAS PubMed PubMed Central Google Scholar
7. Bloom, G. et al. Multi-platform, multi-site, microarray-based human tumor classification. Am. J. Pathol. 164, 9–16 (2004).
   Article CAS PubMed PubMed Central Google Scholar
8. Ma, X.J. et al. Molecular classification of human cancers using a 92-gene real-time quantitative polymerase chain reaction assay. Arch. Pathol. Lab. Med. 130, 465–473 (2006).
   CAS PubMed Google Scholar
9. Talantov, D. et al. A quantitative reverse transcriptase-polymerase chain reaction assay to identify metastatic carcinoma tissue of origin. J. Mol. Diagn. 8, 320–329 (2006).
   Article CAS PubMed PubMed Central Google Scholar
10. Tothill, R.W. et al. An expression-based site of origin diagnostic method designed for clinical application to cancer of unknown origin. Cancer Res. 65, 4031–4040 (2005).
    Article CAS PubMed Google Scholar
11. Shedden, K.A. et al. Accurate molecular classification of human cancers based on gene expression using a simple classifier with a pathological tree-based framework. Am. J. Pathol. 163, 1985–1995 (2003).
    Article CAS PubMed PubMed Central Google Scholar
12. Baskerville, S. & Bartel, D.P. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11, 241–247 (2005).
    Article CAS PubMed PubMed Central Google Scholar
13. Farh, K.K. et al. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310, 1817–1821 (2005).
    Article CAS PubMed Google Scholar
14. Landgraf, P. et al. A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing. Cell 129, 1401–1414 (2007).
    Article CAS PubMed PubMed Central Google Scholar
15. He, L. et al. A microRNA polycistron as a potential human oncogene. Nature 435, 828–833 (2005).
    Article CAS PubMed PubMed Central Google Scholar
16. Lu, J. et al. MicroRNA expression profiles classify human cancers. Nature 435, 834–838 (2005).
    Article CAS PubMed Google Scholar
17. Volinia, S. et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103, 2257–2261 (2006).
    Article CAS PubMed PubMed Central Google Scholar
18. Raver-Shapira, N. et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 26, 731–743 (2007).
    Article CAS PubMed Google Scholar
19. Bentwich, I. et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37, 766–770 (2005).
    Article CAS PubMed Google Scholar
20. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A. & Enright, A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140–D144 (2006).
    Article CAS PubMed Google Scholar
21. Xiao, C. et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131, 146–159 (2007).
    Article CAS PubMed Google Scholar
22. Hornstein, E. et al. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 438, 671–674 (2005).
    Article CAS PubMed Google Scholar
23. Lee, Y.S., Kim, H.K., Chung, S., Kim, K.S. & Dutta, A. Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. J. Biol. Chem. 280, 16635–16641 (2005).
    Article CAS PubMed Google Scholar
24. Sempere, L.F. et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13 (2004).
    Article PubMed PubMed Central Google Scholar
25. Ein-Dor, L., Kela, I., Getz, G., Givol, D. & Domany, E. Outcome signature genes in breast cancer: is there a unique set? Bioinformatics 21, 171–178 (2005).
    Article CAS PubMed Google Scholar
26. Paik, S. et al. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J. Clin. Oncol. 24, 3726–3734 (2006).
    Article CAS PubMed Google Scholar
27. van de Vijver, M.J. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999–2009 (2002).
    Article CAS PubMed Google Scholar
28. Li, J. et al. Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells. BMC Biotechnol. 7, 36 (2007).
    Article PubMed PubMed Central Google Scholar
29. Parker, D.C. et al. Potential utility of uroplakin III, thrombomodulin, high molecular weight cytokeratin, and cytokeratin 20 in noninvasive, invasive, and metastatic urothelial (transitional cell) carcinomas. Am. J. Surg. Pathol. 27, 1–10 (2003).
    Article PubMed Google Scholar
30. Thomson, J.M., Parker, J., Perou, C.M. & Hammond, S.M. A custom microarray platform for analysis of microRNA gene expression. Nat. Methods 1, 47–53 (2004).
    Article CAS PubMed Google Scholar
31. Shi, R. & Chiang, V.L. Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39, 519–525 (2005).
    Article CAS PubMed Google Scholar
32. Thomson, J.M. et al. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 20, 2202–2207 (2006).
    Article CAS PubMed PubMed Central Google Scholar
33. Hino, K., Fukao, T. & Watanabe, M. Regulatory interaction of HNF1α to microRNA194 gene during intestinal epithelial cell differentiation. Nucleic Acids Symp. Ser. (Oxf.), 415–416 (2007).
34. van Duin, M. et al. High-resolution array comparative genomic hybridization of chromosome 8q: evaluation of putative progression markers for gastroesophageal junction adenocarcinomas. Cytogenet. Genome Res. 118, 130–137 (2007).
    Article CAS PubMed Google Scholar

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Acknowledgements

We thank Jung-Hwan Yoon of Seoul National University College of Medicine, Seoul, South Korea. N.R. dedicates this work to the memory of Yasha (Yaakov) Rosenfeld.

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Author notes

1. Nitzan Rosenfeld, Ranit Aharonov, Eti Meiri and Shai Rosenwald: These authors contributed equally to this work.

Authors and Affiliations

1. Rosetta Genomics Ltd., Rehovot, 76706, Israel
   Nitzan Rosenfeld, Ranit Aharonov, Eti Meiri, Shai Rosenwald, Yael Spector, Merav Zepeniuk, Hila Benjamin, Norberto Shabes, Sarit Tabak, Asaf Levy, Danit Lebanony, Yaron Goren, Erez Silberschein, Nurit Targan, Alex Ben-Ari, Shlomit Gilad, Amir Avniel, Isaac Bentwich, Zvi Bentwich, Dalia Cohen & Ayelet Chajut
2. Soroka University Medical Center, Beer-Sheva, 84101, Israel
   Netta Sion-Vardy
3. Department of Pathology, Beilinson Hospital, Rabin Medical Center, Petah-Tikva, 49100, Israel
   Ana Tobar & Meora Feinmesser
4. Pathology Institute, Sourasky Medical Center, Tel Aviv, 64239, Israel
   Oleg Kharenko
5. Bnai-Zion Medical Center, Haifa, 31048, Israel
   Ofer Nativ
6. Department of Pathology, Sheba Medical Center, Tel-Hashomer, 52621, Israel
   Dvora Nass, Marina Perelman, Ady Yosepovich, Bruria Shalmon, Sylvie Polak-Charcon, Eddie Fridman & Iris Barshack
7. Sackler School of Medicine, Tel Aviv University, Tel Aviv, 69978, Israel
   Dvora Nass, Marina Perelman, Ady Yosepovich, Bruria Shalmon, Sylvie Polak-Charcon, Eddie Fridman & Iris Barshack

Authors

1. Nitzan Rosenfeld
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2. Ranit Aharonov
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3. Eti Meiri
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4. Shai Rosenwald
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5. Yael Spector
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6. Merav Zepeniuk
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7. Hila Benjamin
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8. Norberto Shabes
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9. Sarit Tabak
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10. Asaf Levy
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11. Danit Lebanony
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12. Yaron Goren
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13. Erez Silberschein
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14. Nurit Targan
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15. Alex Ben-Ari
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16. Shlomit Gilad
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17. Netta Sion-Vardy
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18. Ana Tobar
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19. Meora Feinmesser
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20. Oleg Kharenko
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21. Ofer Nativ
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22. Dvora Nass
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23. Marina Perelman
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24. Ady Yosepovich
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25. Bruria Shalmon
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26. Sylvie Polak-Charcon
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27. Eddie Fridman
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28. Amir Avniel
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29. Isaac Bentwich
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30. Zvi Bentwich
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31. Dalia Cohen
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32. Ayelet Chajut
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33. Iris Barshack
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Contributions

R.A., A.A., I. Bentwich, Z.B., D.C., A.C. and I. Barshack directed research; N.R., R.A., E.M., S.R., Y.S., S.G., A.C. and I. Barshack designed experiments; N.S.-V., A.T., M.F., O.K., O.N., D.N., M.P., A.Y., B.S., S.P.-C., E.F. and I. Barshack provided samples and performed pathological analysis; E.M., M.Z., N.S., S.T., D.L. and S.G. performed experiments; N.R., R.A., S.R., Y.G. and E.S. developed algorithms; N.R., S.R., H.B. and Y.G. analyzed data; Y.S., A.L., N.T. and A.B.-A. provided bioinformatic and database support; N.R., R.A., A.C. and I. Barschack wrote the paper.

Corresponding authors

Correspondence toRanit Aharonov or Iris Barshack.

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Competing interests

All authors affiliated with Rosetta Genomics, except E.S., are full-time employees of Rosetta Genomics Ltd. and hold equity in the company, the value of which may be influenced by this publication. E.S. was engaged as an external consultant to Rosetta Genomics. O.N. is a paid consultant to Rosetta Genomics. All other authors declare that they have no competing interests.

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Rosenfeld, N., Aharonov, R., Meiri, E. et al. MicroRNAs accurately identify cancer tissue origin.Nat Biotechnol 26, 462–469 (2008). https://doi.org/10.1038/nbt1392

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• Received: 02 January 2008
• Accepted: 03 March 2008
• Published: 23 March 2008
• Issue Date: April 2008
• DOI: https://doi.org/10.1038/nbt1392