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International Journal of Genomics
Volume 2017 (2017), Article ID 1926304, 9 pages
https://doi.org/10.1155/2017/1926304
Review Article

The Utilization of Formalin Fixed-Paraffin-Embedded Specimens in High Throughput Genomic Studies

1Department of Cancer Biology, Vanderbilt University, Nashville, TN, USA
2Department of Biochemistry, Vanderbilt University, Nashville, TN, USA
3Department of Biostatistics, Vanderbilt University, Nashville, TN, USA

Correspondence should be addressed to Yan Guo; ude.tlibrednav@oug.nay

Received 28 November 2016; Accepted 9 January 2017; Published 26 January 2017

Academic Editor: Marco Gerdol

Copyright © 2017 Pan Zhang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. T. P. Gilbert, T. Haselkorn, M. Bunce et al., “The isolation of nucleic acids from fixed, paraffin-embedded tissues-which methods are useful when?” PLoS ONE, vol. 2, no. 6, article no. e537, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. I. Daugaard, T. E. Kjeldsen, H. Hager, L. L. Hansen, and T. K. Wojdacz, “The influence of DNA degradation in formalin-fixed, paraffin-embedded (FFPE) tissue on locus-specific methylation assessment by MS-HRM,” Experimental and Molecular Pathology, vol. 99, no. 3, pp. 632–640, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Lewis, N. J. Maughan, V. Smith, K. Hillan, and P. Quirke, “Unlocking the archive—gene expression in paraffin-embedded tissue,” Journal of Pathology, vol. 195, no. 1, pp. 66–71, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. J.-Y. Chung, T. Braunschweig, and S. M. Hewitt, “Optimization of recovery of RNA from formalin-fixed, paraffin-embedded tissue,” Diagnostic Molecular Pathology, vol. 15, no. 4, pp. 229–236, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. D. McKinney, S. J. Moon, D. A. Kulesh, T. Larsen, and R. J. Schoepp, “Detection of viral RNA from paraffin-embedded tissues after prolonged formalin fixation,” Journal of Clinical Virology, vol. 44, no. 1, pp. 39–42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Masuda, T. Ohnishi, S. Kawamoto, M. Monden, and K. Okubo, “Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples,” Nucleic Acids Research, vol. 27, no. 22, pp. 4436–4443, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Auerbach, M. Moutschen-Dahmen, and J. Moutschen, “Genetic and cytogenetical effects of formaldehyde and related compounds,” Mutation Research/Reviews in Genetic Toxicology, vol. 39, no. 3-4, pp. 317–361, 1977. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Y. Feldman, “Reactions of nucleic acids and nucleodroteins with formaldehyde,” Progress in Nucleic Acid Research and Molecular Biology, vol. 13, pp. 1–49, 1973. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Karlsen, M. Kalantari, M. Chitemerere, B. Johansson, and B. Hagmar, “Modifications of human and viral deoxyribonucleic acid by formaldehyde fixation,” Laboratory Investigation, vol. 71, no. 4, pp. 604–611, 1994. View at Google Scholar · View at Scopus
  10. M. Srinivasan, D. Sedmak, and S. Jewell, “Effect of fixatives and tissue processing on the content and integrity of nucleic acids,” The American Journal of Pathology, vol. 161, no. 6, pp. 1961–1971, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. S. von Ahlfen, A. Missel, K. Bendrat, and M. Schlumpberger, “Determinants of RNA quality from FFPE samples,” PLoS ONE, vol. 2, no. 12, Article ID e1261, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. D. M. Carrick, M. G. Mehaffey, M. C. Sachs et al., “Robustness of next generation sequencing on older formalin-fixed paraffin-embedded tissue,” PLoS ONE, vol. 10, no. 7, Article ID e0127353, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. Q. Sheng, K. Vickers, S. Zhao et al., “Multi-perspective quality control of Illumina RNA sequencing data analysis,” Briefings in Functional Genomics, 2016. View at Publisher · View at Google Scholar
  14. Y. Guo, J. Wu, S. Zhao et al., “RNA sequencing of formalin-fixed, paraffin-embedded specimens for gene expression quantification and data mining,” International Journal of Genomics, vol. 2016, Article ID 9837310, 10 pages, 2016. View at Publisher · View at Google Scholar
  15. R. Menon, M. Deng, D. Boehm et al., “Exome enrichment and SOLiD sequencing of formalin fixed paraffin embedded (FFPE) prostate cancer tissue,” International Journal of Molecular Sciences, vol. 13, no. 7, pp. 8933–8942, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. M. R. Schweiger, M. Kerick, B. Timmermann et al., “Genome-wide massively parallel sequencing of formaldehyde fixed-paraffin embedded (FFPE) tumor tissues for copy-number-and mutation-analysis,” PLoS ONE, vol. 4, no. 5, Article ID e5548, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Astolfi, M. Urbini, V. Indio et al., “Whole exome sequencing (WES) on formalin-fixed, paraffin-embedded (FFPE) tumor tissue in gastrointestinal stromal tumors (GIST),” BMC Genomics, vol. 16, no. 1, article no. 892, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Hedegaard, K. Thorsen, M. K. Lund et al., “Next-generation sequencing of RNA and DNA isolated from paired fresh-frozen and formalin-fixed paraffin-embedded samples of human cancer and normal tissue,” PLoS ONE, vol. 9, no. 5, Article ID e98187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Lassmann, C. Kreutz, A. Schoepflin, U. Hopt, J. Timmer, and M. Werner, “A novel approach for reliable microarray analysis of microdissected tumor cells from formalin-fixed and paraffin-embedded colorectal cancer resection specimens,” Journal of Molecular Medicine, vol. 87, no. 2, pp. 211–224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Abdueva, M. Wing, B. Schaub, T. Triche, and E. Davicioni, “Quantitative expression profiling in formalin-fixed paraffin-embedded samples by Affymetrix microarrays,” Journal of Molecular Diagnostics, vol. 12, no. 4, pp. 409–417, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. K. M. Linton, Y. Hey, E. Saunders et al., “Acquisition of biologically relevant gene expression data by affymetrix microarray analysis of archival formalin-fixed paraffin-embedded tumours (vol 98, pg 1403, 2008),” British Journal of Cancer, vol. 99, no. 2, article 383, 2008. View at Publisher · View at Google Scholar
  22. M. A. Walter, D. Seboek, P. Demougin et al., “Extraction of high-integrity RNA suitable for microarray gene expression analysis from long-term stored human thyroid tissues,” Pathology, vol. 38, no. 3, pp. 249–253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Fedorowicz, S. Guerrero, T. D. Wu, and Z. Modrusan, “Microarray analysis of RNA extracted from formalin-fixed, paraffin-embedded and matched fresh-frozen ovarian adenocarcinomas,” BMC Medical Genomics, vol. 2, article 23, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Frank, C. Döring, D. Metzler, S. Eckerle, and M.-L. Hansmann, “Global gene expression profiling of formalin-fixed paraffin-embedded tumor samples: a comparison to snap-frozen material using oligonucleotide microarrays,” Virchows Archiv, vol. 450, no. 6, pp. 699–711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. S. Scicchitano, D. A. Dalmas, M. A. Bertiaux et al., “Preliminary comparison of quantity, quality, and microarray performance of RNA extracted from formalin-fixed, paraffin-embedded, and unfixed frozen tissue samples,” Journal of Histochemistry & Cytochemistry, vol. 54, no. 11, pp. 1229–1237, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. W. H. Bradley, K. Eng, M. Le, A. C. Mackinnon, C. Kendziorski, and J. S. Rader, “Comparing gene expression data from formalin-fixed, paraffin embedded tissues and qPCR with that from snap-frozen tissue and microarrays for modeling outcomes of patients with ovarian carcinoma,” BMC Clinical Pathology, vol. 15, article 17, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Mittempergher, J. J. de Ronde, M. Nieuwland et al., “Gene expression profiles from formalin fixed paraffin embedded breast cancer tissue are largely comparable to fresh frozen matched tissue,” PLoS ONE, vol. 6, no. 2, Article ID e17163, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Roberts, J. Bowers, K. Sensinger, A. Lisowski, R. Getts, and M. G. Anderson, “Identification of methods for use of formalin-fixed, paraffin-embedded tissue samples in RNA expression profiling,” Genomics, vol. 94, no. 5, pp. 341–348, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Jacobs, E. R. Thompson, Y. Nannya et al., “Genome-wide, high-resolution detection of copy number, loss of heterozygosity, and genotypes from formalin-fixed, paraffin-embedded tumor tissue using microarrays,” Cancer Research, vol. 67, no. 6, pp. 2544–2551, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. E. H. Lips, J. W. F. Dierssen, R. Van Eijk et al., “Reliable high-throughput genotyping and loss-of-heterozygosity detection in formalin-fixed, paraffin-embedded tumors using single nucleotide polymorphism arrays,” Cancer Research, vol. 65, no. 22, pp. 10188–10191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. E. R. Thompson, S. C. Herbert, S. M. Forrest, and I. G. Campbell, “Whole genome SNP arrays using DNA derived from formalin-fixed, paraffin-embedded ovarian tumor tissue,” Human Mutation, vol. 26, no. 4, pp. 384–389, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. H. I. Vos, T. Van Der Straaten, M. J. H. Coenen, U. Flucke, D. M. W. M. Te Loo, and H.-J. Guchelaar, “High-quality genotyping data from formalin-fixed, paraffin-embedded tissue on the drug metabolizing enzymes and transporters plus array,” The Journal of Molecular Diagnostics, vol. 17, no. 1, pp. 4–9, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Wang, V. E. Carlton, G. Karlin-Neumann et al., “High quality copy number and genotype data from FFPE samples using Molecular Inversion Probe (MIP) microarrays,” BMC Medical Genomics, vol. 2, no. 1, article 8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Wang, V. E. Carlton, G. Karlin-Neumann et al., “High quality copy number and genotype data from FFPE samples using Molecular Inversion Probe (MIP) microarrays,” BMC Medical Genomics, vol. 2, article no. 8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Tuefferd, A. De Bondt, I. Van Den Wyngaert et al., “Genome-wide copy number alterations detection in fresh frozen and matched FFPE samples using SNP 6.0 arrays,” Genes Chromosomes and Cancer, vol. 47, no. 11, pp. 957–964, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Oosting, E. H. Lips, R. Van Eijk et al., “High-resolution copy number analysis of paraffin-embedded archival tissue using SNP BeadArrays,” Genome Research, vol. 17, no. 3, pp. 368–376, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Alvarez, S. F. Kash, M. A. Lyons-Weiler et al., “Reproducibility and performance of virtual karyotyping with SNP microarrays for the detection of chromosomal imbalances in formalin-fixed paraffin-embedded tissues,” Diagnostic Molecular Pathology, vol. 19, no. 3, pp. 127–134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. E. A. Mc Sherry, A. Mc Goldrick, E. W. Kay, A. M. Hopkins, W. Gallagher, and P. A. Dervan, “Formalin-fixed paraffin-embedded clinical tissues show spurious copy number changes in array-CGH profiles,” Clinical Genetics, vol. 72, no. 5, pp. 441–447, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. N. A. Johnson, R. A. Hamoudi, K. Ichimura et al., “Application of array CGH on archival formalin-fixed paraffin-embedded tissues including small numbers of microdissected cells,” Laboratory Investigation, vol. 86, no. 9, pp. 968–978, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. S. DeVries, S. Nyante, J. Korkola et al., “Array-based comparative genomic hybridization from formalin-fixed, paraffin-embedded breast tumors,” The Journal of Molecular Diagnostics, vol. 7, no. 1, pp. 65–71, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. S. A. Joosse, E. H. van Beers, and P. M. Nederlof, “Automated array-CGH optimized for archival formalin-fixed, paraffin-embedded tumor material,” BMC Cancer, vol. 7, article no. 43, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. S. E. Little, R. Vuononvirta, J. S. Reis-Filho et al., “Array CGH using whole genome amplification of fresh-frozen and formalin-fixed, paraffin-embedded tumor DNA,” Genomics, vol. 87, no. 2, pp. 298–306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Fensterer, B. Radlwimmer, J. Sträter et al., “Matrix-comparative genomic hybridization from multicenter formalin-fixed paraffin-embedded colorectal cancer tissue blocks,” BMC Cancer, vol. 7, article no. 58, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. P. A. Lennon, Y. Zhuang, D. Pierson et al., “Bacterial artificial chromosome array-based comparative genomic hybridization using paired formalin-fixed, paraffin-embedded and fresh frozen tissue specimens in multiple myeloma,” Cancer, vol. 115, no. 2, pp. 345–354, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Mohapatra, R. A. Betensky, E. R. Miller et al., “Glioma test array for use with formalin-fixed, paraffin-embedded tissue: array comparative genomic hybridization correlates with loss of heterozygosity and fluorescence in situ hybridization,” The Journal of Molecular Diagnostics, vol. 8, no. 2, pp. 268–276, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. J. D. Harvell, S. Kohler, S. Zhu, T. Hernandez-Boussard, J. R. Pollack, and M. Van De Rijn, “High-resolution array-based comparative genomic hybridization for distinguishing paraffin-embedded Spitz nevi and melanomas,” Diagnostic Molecular Pathology, vol. 13, no. 1, pp. 22–25, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Moran, M. Vizoso, A. Martinez-Cardús et al., “Validation of DNA methylation profiling in formalin-fixed paraffin-embedded samples using the Infinium HumanMethylation450 Microarray,” Epigenetics, vol. 9, no. 6, pp. 829–833, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Thirlwell, M. Eymard, A. Feber et al., “Genome-wide DNA methylation analysis of archival formalin-fixed paraffin-embedded tissue using the Illumina Infinium HumanMethylation27 BeadChip,” Methods, vol. 52, no. 3, pp. 248–254, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. J. K. Killian, S. Bilke, S. Davis et al., “Large-scale profiling of archival lymph nodes reveals pervasive remodeling of the follicular lymphoma methylome,” Cancer Research, vol. 69, no. 3, pp. 758–764, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. T. C. de Ruijter, J. P. de Hoon, J. Slaats et al., “Formalin-fixed, paraffin-embedded (FFPE) tissue epigenomics using Infinium HumanMethylation450 BeadChip assays,” Laboratory Investigation, vol. 95, no. 7, pp. 833–842, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Jasmine, R. Rahaman, S. Roy et al., “Interpretation of genome-wide infinium methylation data from ligated DNA in formalin-fixed, paraffin-embedded paired tumor and normal tissue,” BMC Research Notes, vol. 5, article 117, 2012. View at Publisher · View at Google Scholar
  52. C. Thirlwell, A. Feber, M. Lechner, A. E. Teschendorff, and S. Beck, “Comments on: interpretation of genome-wide infinium methylation data from ligated DNA in formalin-fixed paraffin-embedded paired tumor and normal tissue,” BMC Research Notes, vol. 5, article no. 631, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. M. G. Kibriya, M. Raza, F. Jasmine et al., “A genome-wide DNA methylation study in colorectal carcinoma,” BMC Medical Genomics, vol. 4, article no. 50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. T. D. Dumenil, L. F. Wockner, M. Bettington et al., “Genome-wide DNA methylation analysis of formalin-fixed paraffin embedded colorectal cancer tissue,” Genes Chromosomes & Cancer, vol. 53, no. 7, pp. 537–548, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. Z. Wang, M. Gerstein, and M. Snyder, “RNA-seq: a revolutionary tool for transcriptomics,” Nature Reviews Genetics, vol. 10, no. 1, pp. 57–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. J. C. Marioni, C. E. Mason, S. M. Mane, M. Stephens, and Y. Gilad, “RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays,” Genome Research, vol. 18, no. 9, pp. 1509–1517, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. W. Asmann, E. W. Klee, E. A. Thompson et al., “3' tag digital gene expression profiling of human brain and universal reference RNA using Illumina Genome Analyzer,” BMC genomics, vol. 10, p. 531, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. N. Cloonan, A. R. R. Forrest, G. Kolle et al., “Stem cell transcriptome profiling via massive-scale mRNA sequencing,” Nature Methods, vol. 5, no. 7, pp. 613–619, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Guo, Q. Sheng, J. Li, F. Ye, D. C. Samuels, and Y. Shyr, “Large scale comparison of gene expression levels by microarrays and RNAseq using TCGA data,” PLoS ONE, vol. 8, no. 8, Article ID e71462, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Norton, Z. Sun, Y. W. Asmann et al., “Gene expression, single nucleotide variant and fusion transcript discovery in archival material from breast tumors,” PLoS ONE, vol. 8, no. 11, Article ID e81925, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Graw, R. Meier, K. Minn et al., “Robust gene expression and mutation analyses of RNA-sequencing of formalin-fixed diagnostic tumor samples,” Scientific Reports, vol. 5, Article ID 12335, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. S. D. Hester, V. Bhat, B. N. Chorley et al., “Editor’s highlight: dose–response analysis of RNA-Seq profiles in archival formalin-fixed paraffin-embedded samples,” Toxicological Sciences, vol. 154, no. 2, pp. 202–213, 2016. View at Publisher · View at Google Scholar
  63. W. Zhao, X. He, K. A. Hoadley, J. S. Parker, D. N. Hayes, and C. M. Perou, “Comparison of RNA-Seq by poly (A) capture, ribosomal RNA depletion, and DNA microarray for expression profiling,” BMC Genomics, vol. 15, no. 1, article 419, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. O. Eikrem, C. Beisland, K. Hjelle et al., “Transcriptome sequencing (RNAseq) enables utilization of formalin-fixed, paraffin-embedded biopsies with clear cell renal cell carcinoma for exploration of disease biology and biomarker development,” PLoS ONE, vol. 11, no. 2, Article ID e0149743, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Li, A. Conley, H. Zhang, and H. L. Kim, “Whole-Transcriptome profiling of formalin-fixed, paraffin-embedded renal cell carcinoma by RNA-seq,” BMC Genomics, vol. 15, no. 1, article no. 1087, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. L. Han, K. C. Vickers, D. C. Samuels, and Y. Guo, “Alternative applications for distinct RNA sequencing strategies,” Briefings in Bioinformatics, vol. 16, no. 4, pp. 629–639, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. K. J. Brayer, C. A. Frerich, H. Kang, and S. A. Ness, “Recurrent fusions in MYB and MYBL1 define a common, transcription factor-driven oncogenic pathway in salivary gland adenoid cystic carcinoma,” Cancer Discovery, vol. 6, no. 2, pp. 176–187, 2016. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Erdem-Eraslan, M. J. Van Den Bent, Y. Hoogstrate et al., “Identification of patients with recurrent glioblastoma who may benefit from combined bevacizumab and CCNU Therapy: a report from the BELOB Trial,” Cancer Research, vol. 76, no. 3, pp. 525–534, 2016. View at Publisher · View at Google Scholar · View at Scopus
  69. P.-A. Just, F. Letourneur, C. Pouliquen et al., “Identification by FFPE RNA-Seq of a new recurrent inversion leading to RBM10-TFE3 fusion in renal cell carcinoma with subtle TFE3 break-apart FISH pattern,” Genes Chromosomes and Cancer, vol. 55, no. 6, pp. 541–548, 2016. View at Publisher · View at Google Scholar · View at Scopus
  70. X. S. Lin, L. Hu, K. Sandy et al., “Differentiating progressive from nonprogressive T1 bladder cancer by gene expression profiling: applying RNA-sequencing analysis on archived specimens,” Urologic Oncology, vol. 23, no. 3, pp. 327–336, 2014. View at Publisher · View at Google Scholar
  71. Y. Liu, A. P. Noon, E. Aguiar Cabeza et al., “Next-generation RNA sequencing of archival formalin-fixed paraffin-embedded urothelial bladder cancer,” European Urology, vol. 66, no. 6, pp. 982–986, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Ma, R. Ambannavar, J. Stephans et al., “Fusion transcript discovery in formalin-fixed paraffin-embedded human breast cancer tissues reveals a link to tumor progression,” PLoS ONE, vol. 9, no. 4, Article ID 0094202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. M. L. Morton, X. Bai, C. R. Merry et al., “Identification of mRNAs and lincRNAs associated with lung cancer progression using next-generation RNA sequencing from laser micro-dissected archival FFPE tissue specimens,” Lung Cancer, vol. 85, no. 1, pp. 31–39, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Sinicropi, K. Qu, F. Collin et al., “Whole transcriptome RNA-seq analysis of breast cancer recurrence risk using formalin-fixed paraffin-embedded tumor tissue,” PLoS ONE, vol. 7, no. 7, Article ID e40092, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. C. Walther, J. Hofvander, J. Nilsson et al., “Gene fusion detection in formalin-fixed paraffin-embedded benign fibrous histiocytomas using fluorescence in situ hybridization and RNA sequencing,” Laboratory Investigation, vol. 95, no. 9, pp. 1071–1076, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. K. C. Vickers, L. A. Roteta, H. Hucheson-Dilks, L. Han, and Y. Guo, “Mining diverse small RNA species in the deep transcriptome,” Trends in Biochemical Sciences, vol. 40, no. 1, pp. 4–7, 2015. View at Publisher · View at Google Scholar
  77. X. Chen, Y. Ba, L. Ma et al., “Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases,” Cell Research, vol. 18, no. 10, pp. 997–1006, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Jung, A. Schaefer, I. Steiner et al., “Robust MicroRNA stability in degraded RNA preparations from human tissue and cell samples,” Clinical Chemistry, vol. 56, no. 6, pp. 998–1006, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. P. S. Mitchell, R. K. Parkin, E. M. Kroh et al., “Circulating microRNAs as stable blood-based markers for cancer detection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10513–10518, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Kakimoto, M. Tanaka, H. Kamiguchi, E. Ochiai, M. Osawa, and A. van Wijnen, “MicroRNA stability in FFPE tissue samples: dependence on GC content,” PLoS ONE, vol. 11, no. 9, Article ID e0163125, 2016. View at Publisher · View at Google Scholar
  81. W. Meng, J. P. McElroy, S. Volinia et al., “Comparison of microRNA deep sequencing of matched formalin-fixed paraffin-embedded and fresh frozen cancer tissues,” PLoS ONE, vol. 8, no. 5, Article ID e64393, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Tam, R. De Borja, M.-S. Tsao, and J. D. Mcpherson, “Robust global microRNA expression profiling using next-generation sequencing technologies,” Laboratory Investigation, vol. 94, no. 3, pp. 350–358, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. L. Weng, X. Wu, H. Gao et al., “MicroRNA profiling of clear cell renal cell carcinoma by whole-genome small RNA deep sequencing of paired frozen and formalin-fixed, paraffin-embedded tissue specimens,” The Journal of Pathology, vol. 222, no. 1, pp. 41–51, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. J. L. Plieskatt, G. Rinaldi, Y. Feng et al., “Methods and matrices: approaches to identifying miRNAs for Nasopharyngeal carcinoma,” Journal of Translational Medicine, vol. 12, no. 1, article 3, 2014. View at Publisher · View at Google Scholar · View at Scopus
  85. S. M. Riester, J. Torres-Mora, A. Dudakovic et al., “Hypoxia-related microRNA-210 is a diagnostic marker for discriminating osteoblastoma and osteosarcoma,” Journal of Orthopaedic Research, 2016. View at Publisher · View at Google Scholar · View at Scopus
  86. R. De Paoli-Iseppi, P. A. Johansson, A. M. Menzies et al., “Comparison of whole-exome sequencing of matched fresh and formalin fixed paraffin embedded melanoma tumours: implications for clinical decision making,” Pathology, vol. 48, no. 3, pp. 261–266, 2016. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Holley, E. Lenkiewicz, L. Evers et al., “Deep clonal profiling of formalin fixed paraffin embedded clinical samples,” PLoS ONE, vol. 7, no. 11, Article ID e50586, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Kerick, M. Isau, B. Timmermann et al., “Targeted high throughput sequencing in clinical cancer settings: formaldehyde fixed-paraffin embedded (FFPE) tumor tissues, input amount and tumor heterogeneity,” BMC Medical Genomics, vol. 4, article no. 68, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Munchel, Y. Hoang, Y. Zhao et al., “Targeted or whole genome sequencing of formalin fixed tissue samples: potential applications in cancer genomics,” Oncotarget, vol. 6, no. 28, pp. 25943–25961, 2015. View at Publisher · View at Google Scholar · View at Scopus
  90. E. Oh, Y.-L. Choi, M. J. Kwon et al., “Comparison of accuracy of whole-exome sequencing with formalin-fixed paraffin-embedded and fresh frozen tissue samples,” PLoS ONE, vol. 10, no. 12, Article ID e0144162, 2015. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Q. Wong, J. Li, R. Salemi et al., “Targeted-capture massively-parallel sequencing enables robust detection of clinically informative mutations from formalin-fixed tumours,” Scientific Reports, vol. 3, article no. 3494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Mafficini, E. Amato, M. Fassan et al., “Reporting tumor molecular heterogeneity in histopathological diagnosis,” PLoS ONE, vol. 9, no. 8, Article ID e104979, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Bourgon, S. Lu, Y. Yan et al., “High-throughput detection of clinically relevant mutations in archived tumor samples by multiplexed PCR and next-generation sequencing,” Clinical Cancer Research, vol. 20, no. 8, pp. 2080–2091, 2014. View at Publisher · View at Google Scholar · View at Scopus
  94. J. Ahn, K. S. Han, J. H. Heo et al., “FOXC2 and CLIP4: a potential biomarker for synchronous metastasis of ≤7-cm clear cell renal cell carcinomas,” Oncotarget, vol. 7, no. 32, 2016. View at Publisher · View at Google Scholar · View at Scopus
  95. X. Castells, S. Karanović, M. Ardin et al., “Low-coverage exome sequencing screen in formalin-fixed paraffin-embedded tumors reveals evidence of exposure to carcinogenic aristolochic acid,” Cancer Epidemiology Biomarkers & Prevention, vol. 24, no. 12, pp. 1873–1881, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Collazo-Lorduy, M. Castillo-Martin, L. Wang et al., “Urachal carcinoma shares genomic alterations with colorectal carcinoma and may respond to epidermal growth factor inhibition,” European Urology, vol. 70, no. 5, pp. 771–775, 2016. View at Publisher · View at Google Scholar · View at Scopus
  97. B. Jelakovic, X. Castells, K. Tomic, M. Ardin, S. Karanovic, and J. Zavadil, “Renal cell carcinomas of chronic kidney disease patients harbor the mutational signature of carcinogenic aristolochic acid,” International Journal of Cancer, vol. 136, no. 12, pp. 2967–2972, 2015. View at Publisher · View at Google Scholar · View at Scopus
  98. R. Menon, M. Deng, K. Rüenauver et al., “Somatic copy number alterations by whole-exome sequencing implicates YWHAZ and PTK2 in castration-resistant prostate cancer,” The Journal of Pathology, vol. 231, no. 4, pp. 505–516, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. E. M. Van Allen, N. Wagle, P. Stojanov et al., “Whole-exome sequencing and clinical interpretation of formalin-fixed, paraffin-embedded tumor samples to guide precision cancer medicine,” Nature Medicine, vol. 20, no. 6, pp. 682–688, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Kriegsmann, V. Endris, T. Wolf et al., “Mutational profiles in triple-negative breast cancer defined by ultradeep multigene sequencing show high rates of PI3K pathway alterations and clinically relevant entity subgroup specific differences,” Oncotarget, vol. 5, no. 20, pp. 9952–9965, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. F. Meric-Bernstam, G. M. Frampton, J. Ferrer-Lozano et al., “Concordance of genomic alterations between primary and recurrent breast cancer,” Molecular Cancer Therapeutics, vol. 13, no. 5, pp. 1382–1389, 2014. View at Publisher · View at Google Scholar · View at Scopus
  102. J. S. Ross, K. Wang, J. V. Rand et al., “Next-generation sequencing of adrenocortical carcinoma reveals new routes to targeted therapies,” Journal of Clinical Pathology, vol. 67, no. 11, pp. 968–973, 2014. View at Publisher · View at Google Scholar · View at Scopus
  103. N. Wagle, M. F. Berger, M. J. Davis et al., “High-throughput detection of actionable genomic alterations in clinical tumor samples by targeted, massively parallel sequencing,” Cancer Discovery, vol. 2, no. 1, pp. 82–93, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. D. Korbie, E. Lin, D. Wall et al., “Multiplex bisulfite PCR resequencing of clinical FFPE DNA,” Clinical Epigenetics, vol. 7, no. 1, article no. 28, 2015. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Fang, L. Hutchinson, A. Deng, and M. R. Green, “Common BRAF(V600E)-directed pathway mediates widespread epigenetic silencing in colorectal cancer and melanoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 5, pp. 1250–1255, 2016. View at Publisher · View at Google Scholar · View at Scopus
  106. H. Gu, C. Bock, T. S. Mikkelsen et al., “Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution,” Nature Methods, vol. 7, no. 2, pp. 133–136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. D. McCarthy, W. Pulverer, A. Weinhaeusel et al., “MethylMeter®: bisulfite-free quantitative and sensitive DNA methylation profiling and mutation detection in FFPE samples,” Epigenomics, vol. 8, no. 6, pp. 747–765, 2016. View at Publisher · View at Google Scholar · View at Scopus
  108. R. P. Darst, C. E. Pardo, L. Ai, K. D. Brown, and M. P. Kladde, “Bisulfite sequencing of DNA,” Current Protocols in Molecular Biology, chapter 7, Unit 7.9, pp. 1–17, 2010. View at Publisher · View at Google Scholar
  109. M. Fanelli, S. Amatori, I. Barozzi et al., “Pathology tissue-chromatin immunoprecipitation, coupled with high-throughput sequencing, allows the epigenetic profiling of patient samples,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 50, pp. 21535–21540, 2010. View at Publisher · View at Google Scholar · View at Scopus
  110. P. Cejas, L. Li, N. K. O'Neill et al., “Chromatin immunoprecipitation from fixed clinical tissues reveals tumor-specific enhancer profiles,” Nature Medicine, vol. 22, no. 6, pp. 685–691, 2016. View at Publisher · View at Google Scholar · View at Scopus
  111. G. K. Geiss, R. E. Bumgarner, B. Birditt et al., “Direct multiplexed measurement of gene expression with color-coded probe pairs,” Nature Biotechnology, vol. 26, no. 3, pp. 317–325, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Adam, B. Afzali, K. M. Dominy et al., “Multiplexed color-coded probe-based gene expression assessment for clinical molecular diagnostics in formalin-fixed paraffin-embedded human renal allograft tissue,” Clinical Transplantation, vol. 30, no. 3, pp. 295–305, 2016. View at Publisher · View at Google Scholar · View at Scopus
  113. C. P. Kolbert, R. M. Feddersen, F. Rakhshan et al., “Multi-platform analysis of microRNA expression measurements in RNA from fresh frozen and FFPE tissues,” PLoS ONE, vol. 8, no. 1, Article ID e52517, 2013. View at Publisher · View at Google Scholar · View at Scopus
  114. P. P. Reis, L. Waldron, R. S. Goswami et al., “mRNA transcript quantification in archival samples using multiplexed, color-coded probes,” BMC Biotechnology, vol. 11, no. 1, article 46, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Chatterjee, A. L. Leichter, V. Fan et al., “A cross comparison of technologies for the detection of microRNAs in clinical FFPE samples of hepatoblastoma patients,” Scientific Reports, vol. 5, Article ID 10438, 2015. View at Publisher · View at Google Scholar
  116. X. Chen, N. G. Deane, K. B. Lewis et al., “Comparison of nanostring nCounter® data on FFPE colon cancer samples and affymetrix microarray data on matched frozen tissues,” PLoS ONE, vol. 11, no. 5, Article ID e0153784, 2016. View at Publisher · View at Google Scholar · View at Scopus
  117. J. Zhu, N. G. Deane, K. B. Lewis et al., “Evaluation of frozen tissue-derived prognostic gene expression signatures in FFPE colorectal cancer samples,” Scientific Reports, vol. 6, p. 33273, 2016. View at Publisher · View at Google Scholar
  118. M. H. Veldman-Jones, Z. Lai, M. Wappett et al., “Reproducible, quantitative, and flexible molecular subtyping of clinical DLBCL samples using the NanoString nCounter system,” Clinical Cancer Research, vol. 21, no. 10, pp. 2367–2378, 2015. View at Publisher · View at Google Scholar · View at Scopus