Formalin fixation in the '-omics' era: A primer for the surgeon-scientist

ANZ Journal of Surgery

Volumn 82, Issue 6, 2012, Pages 395-402

  Frankel, Adam ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Molecular biology; Translational research

Indexed keywords

DNA; FIXATIVE; FORMALDEHYDE; PARAFFIN; RNA;

DNA MICROARRAY; DNA SEQUENCE; DRUG EFFECT; GENOMICS; HUMAN; METHODOLOGY; REVIEW; SEQUENCE ANALYSIS; TISSUE FIXATION;

DNA; FIXATIVES; FORMALDEHYDE; GENOMICS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARAFFIN EMBEDDING; RNA; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA; TISSUE FIXATION;

EID: 84861856046     PISSN: 14451433     EISSN: 14452197     Source Type: Journal    
DOI: 10.1111/j.1445-2197.2012.06092.x     Document Type: Review

References (90)

1. Blum F. Der Formaldehyde als Hartungsmittel. Zwiss Mikr 1893; 10: 314-5.
2. Feldman MY. Reactions of nucleic acids and nucleoproteins with formaldehyde. Prog. Nucleic Acid Res. Mol. Biol. 1973; 13: 1-49.
3. Jackson V, Chalkley R. Separation of newly synthesized nucleohistone by equilibrium centrifugation in cesium chloride. Biochemistry 1974; 13: 3952-6.
4. Moller K, Rinke J, Ross A, Buddle G, Brimacombe R. The use of formaldehyde in RNA-protein cross-linking studies with ribosomal subunits from Escherichia coli. Eur. J. Biochem. 1977; 76: 175-87.
5. Fraenkel-Conrat H. Reaction of nucleic acid with formaldehyde. Biochim. Biophys. Acta 1954; 15: 307-9.
6. Haselkorn R, Doty P. The reaction of formaldehyde with polynucleotides. J. Biol. Chem. 1961; 236: 2738-45.
7. Kibriya MG, Jasmine F, Roy S, Paul-Brutus RM, Argos M, Ahsan H. Analyses and interpretation of whole-genome gene expression from formalin-fixed paraffin-embedded tissue: an illustration with breast cancer tissues. BMC Genomics 2010; 11: 622.
8. Klopfleisch R, Weiss AT, Gruber AD. Excavation of a buried treasure - DNA, mRNA, miRNA and protein analysis in formalin fixed, paraffin embedded tissues. Histol. Histopathol. 2011; 26: 797-810.
9. Sadi AM, Wang DY, Youngson BJ etal. Clinical relevance of DNA microarray analyses using archival formalin-fixed paraffin-embedded breast cancer specimens. BMC Cancer 2011; 11: 1-13.
10. Dash A, Maine IP, Varambally S, Shen R, Chinnaiyan AM, Rubin MA. Changes in differential gene expression because of warm ischemia time of radical prostatectomy specimens. Am. J. Pathol. 2002; 161: 1743-8.
11. Kingsbury AE, Foster OJ, Nisbet AP etal. Tissue pH as an indicator of mRNA preservation in human post-mortem brain. Brain Res. Mol. Brain Res. 1995; 28: 311-8.
12. Spruessel A, Steimann G, Jung M etal. Tissue ischemia time affects gene and protein expression patterns within minutes following surgical tumor excision. Biotechniques 2004; 36: 1030-7.
13. Bussolati G, Annaratone L, Medico E, D'Armento G, Sapino A. Formalin fixation at low temperature better preserves nucleic acid integrity. PLoS ONE 2011; 6: e21043.
14. Huijsmans CJ, Damen J, van der Linden JC, Savelkoul PH, Hermans MH. Comparative analysis of four methods to extract DNA from paraffin-embedded tissues: effect on downstream molecular applications. BMC Res. Notes 2010; 3: 239.
15. Serth J, Kuczyk MA, Paeslack U, Lichtinghagen R, Jonas U. Quantitation of DNA extracted after micropreparation of cells from frozen and formalin-fixed tissue sections. Am. J. Pathol. 2000; 156: 1189-96.
16. Gündisch S, Hauck SM, Sarioglu H etal. Investigating the impact of pre-analytical variables on protein quality of human tissue samples. In Institute of Pathology MUoG, Austria, Department of Pathology JNI, Erasmus Medical Center Rotterdam, The Netherlands (eds), 2011 BRN Symposium, 2011.
17. Micke P, Ohshima M, Tahmasebpoor S etal. Biobanking of fresh frozen tissue: RNA is stable in nonfixed surgical specimens. Lab. Invest. 2006; 86: 202-11.
18. Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S. Ancient DNA. Nat. Rev. Genet. 2001; 2: 353-9.
19. Loudig O, Brandwein-Gensler M, Kim RS etal. Illumina whole-genome complementary DNA-mediated annealing, selection, extension and ligation platform: assessing its performance in formalin-fixed, paraffin-embedded samples and identifying invasion pattern-related genes in oral squamous cell carcinoma. Hum. Pathol. 2011; 42: 1911-22.
20. Koshiba M, Ogawa K, Hamazaki S, Sugiyama T, Ogawa O, Kitajima T. The effect of formalin fixation on DNA and the extraction of high-molecular-weight DNA from fixed and embedded tissues. Pathol. Res. Pract. 1993; 189: 66-72.
21. Gilbert MT, Haselkorn T, Bunce M etal. The isolation of nucleic acids from fixed, paraffin-embedded tissues-which methods are useful when? PLoS ONE 2007; 2: e537.
22. Ghazani AA, Arneson NC, Warren K, Done SJ. Limited tissue fixation times and whole genomic amplification do not impact array CGH profiles. J. Clin. Pathol. 2006; 59: 311-5.
23. Bonin S, Hlubek F, Benhattar J etal. Multicentre validation study of nucleic acids extraction from FFPE tissues. Virchows Arch. 2010; 457: 309-17.
24. Fedorowicz G, Guerrero S, Wu TD, Modrusan Z. Microarray analysis of RNA extracted from formalin-fixed, paraffin-embedded and matched fresh-frozen ovarian adenocarcinomas. BMC Med. Genomics 2009; 2: 23.
25. Waddell N, Cocciardi S, Johnson J etal. Gene expression profiling of formalin-fixed, paraffin-embedded familial breast tumours using the whole genome-DASL assay. J. Pathol. 2010; 221: 452-61.
26. Okello JB, Zurek J, Devault AM etal. Comparison of methods in the recovery of nucleic acids from archival formalin-fixed paraffin-embedded autopsy tissues. Anal. Biochem. 2010; 400: 110-7.
27. Lu X, van der Straaten T, Tiller M, Li X. Evidence for qualified quantitative mRNA analysis in formalin-fixed and paraffin-embedded colorectal carcinoma cells and tissue. J. Clin. Lab. Anal. 2011; 25: 166-73.
28. Roberts L, Bowers J, Sensinger K, Lisowski A, Getts R, Anderson MG. Identification of methods for use of formalin-fixed, paraffin-embedded tissue samples in RNA expression profiling. Genomics 2009; 94: 341-8.
29. Johnson NA, Hamoudi RA, Ichimura K etal. Application of array CGH on archival formalin-fixed paraffin-embedded tissues including small numbers of microdissected cells. Lab. Invest. 2006; 86: 968-78.
30. Fan JB, Yeakley JM, Bibikova M etal. A versatile assay for high-throughput gene expression profiling on universal array matrices. Genome Res. 2004; 14: 878-85.
31. April C, Klotzle B, Royce T etal. Whole-genome gene expression profiling of formalin-fixed, paraffin-embedded tissue samples. PLoS ONE 2009; 4: e8162.
32. Lee CH, Bang SH, Lee SK, Song KY, Lee IC. Gene expression profiling reveals sequential changes in gastric tubular adenoma and carcinoma in situ. World J. Gastroenterol. 2005; 11: 1937-45.
33. Schoor O, Weinschenk T, Hennenlotter J etal. Moderate degradation does not preclude microarray analysis of small amounts of RNA. Biotechniques 2003; 35: 1192-6, 8-201.
34. Abdueva D, Wing M, Schaub B, Triche T, Davicioni E. Quantitative expression profiling in formalin-fixed paraffin-embedded samples by Affymetrix microarrays. J. Mol. Diagn. 2010; 12: 409-17.
35. Budczies J, Weichert W, Noske A etal. Genome-wide gene expression profiling of formalin-fixed paraffin-embedded breast cancer core biopsies using microarrays. J. Histochem. Cytochem. 2011; 59: 146-57.
36. Linton KM, Hey Y, Saunders E etal. Acquisition of biologically relevant gene expression data by Affymetrix microarray analysis of archival formalin-fixed paraffin-embedded tumours. Br. J. Cancer 2008; 98: 1403-14.
37. Paik S, Kim CY, Song YK, Kim WS. Technology insight: application of molecular techniques to formalin-fixed paraffin-embedded tissues from breast cancer. Nat. Clin. Pract. Oncol. 2005; 2: 246-54.
38. Reinholz MM, Eckel-Passow JE, Anderson SK etal. Expression profiling of formalin-fixed paraffin-embedded primary breast tumors using cancer-specific and whole genome gene panels on the DASL(R) platform. BMC Med. Genomics 2010; 3: 60.
39. Freedman JA, Augustine CK, Selim MA etal. A methodology for utilization of predictive genomic signatures in FFPE samples. BMC Med. Genomics 2011; 4: 58.
40. Farragher SM, Tanney A, Kennedy RD, Paul Harkin D. RNA expression analysis from formalin fixed paraffin embedded tissues. Histochem. Cell Biol. 2008; 130: 435-45.
41. Ravo M, Mutarelli M, Ferraro L etal. Quantitative expression profiling of highly degraded RNA from formalin-fixed, paraffin-embedded breast tumor biopsies by oligonucleotide microarrays. Lab. Invest. 2008; 88: 430-40.
42. Chien J, Fan JB, Bell DA etal. Analysis of gene expression in stage I serous tumors identifies critical pathways altered in ovarian cancer. Gynecol. Oncol. 2009; 114: 3-11.
43. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009; 10: 57-63.
44. Krijgsman O, Israeli D, Haan JC etal. CGH arrays compared for DNA isolated from formalin-fixed, paraffin-embedded material. Genes Chromosomes Cancer 2012; 51: 344-52.
45. Lo KC, Bailey D, Burkhardt T, Gardina P, Turpaz Y, Cowell JK. Comprehensive analysis of loss of heterozygosity events in glioblastoma using the 100K SNP mapping arrays and comparison with copy number abnormalities defined by BAC array comparative. Genes Chromosomes Cancer 2008; 47: 221-37.
46. Alvarez K, Kash SF, Lyons-Weiler MA etal. Reproducibility and performance of virtual karyotyping with SNP microarrays for the detection of chromosomal imbalances in formalin-fixed paraffin-embedded tissues. Diagn. Mol. Pathol. 2010; 19: 127-34.
47. Lyons-Weiler M, Hagenkord J, Sciulli C, Dhir R, Monzon FA. Optimization of the Affymetrix GeneChip Mapping 10K 2.0 Assay for routine clinical use on formalin-fixed paraffin-embedded tissues. Diagn. Mol. Pathol. 2008; 17: 3-13.
48. Monzon FA, Hagenkord JM, Lyons-Weiler MA etal. Whole genome SNP arrays as a potential diagnostic tool for the detection of characteristic chromosomal aberrations in renal epithelial tumors. Mod. Pathol. 2008; 21: 599-608.
49. Lips EH, Dierssen JW, van Eijk R etal. Reliable high-throughput genotyping and loss-of-heterozygosity detection in formalin-fixed, paraffin-embedded tumors using single nucleotide polymorphism arrays. Cancer Res. 2005; 65: 10188-91.
50. Oosting J, Lips EH, van Eijk R etal. High-resolution copy number analysis of paraffin-embedded archival tissue using SNP BeadArrays. Genome Res. 2007; 17: 368-76.
51. Jacobs S, Thompson ER, Nannya Y etal. Genome-wide, high-resolution detection of copy number, loss of heterozygosity, and genotypes from formalin-fixed, paraffin-embedded tumor tissue using microarrays. Cancer Res. 2007; 67: 2544-51.
52. Tuefferd M, de Bondt A, Van den Wyngaert I, Talloen W, Gohlmann H. Microarray profiling of DNA extracted from FFPE tissues using SNP 6.0 Affymetrix platform. Methods Mol. Biol. 2011; 724: 147-60.
53. Tuefferd M, De Bondt A, Van Den Wyngaert I etal. Genome-wide copy number alterations detection in fresh frozen and matched FFPE samples using SNP 6.0 arrays. Genes Chromosomes Cancer 2008; 47: 957-64.
54. Nasri S, Anjomshoaa A, Song S etal. Oligonucleotide array outperforms SNP array on formalin-fixed paraffin-embedded clinical samples. Cancer Genet. Cytogenet. 2010; 198: 1-6.
55. Mc Sherry EA, Mc Goldrick A, Kay EW, Hopkins AM, Gallagher WM, Dervan PA. Formalin-fixed paraffin-embedded clinical tissues show spurious copy number changes in array-CGH profiles. Clin. Genet. 2007; 72: 441-7.
56. Wang Y, Carlton VE, Karlin-Neumann G etal. High quality copy number and genotype data from FFPE samples using Molecular Inversion Probe (MIP) microarrays. BMC Med. Genomics 2009; 2: 8.
57. Liang CW, Lee YS, Marino-Enriquez A, Tsui K, Huang SH. The utility and limitation of single nucleotide polymorphism analysis on whole genome amplified mesenchymal tumour DNA in formalin fixed tumour samples. Pathology 2012; 44: 33-41.
58. Stokes A, Drozdov I, Guerra E etal. Copy number and loss of heterozygosity detected by SNP array of formalin-fixed tissues using whole-genome amplification. PLoS ONE 2011; 6: e24503.
59. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. U.S.A. 1977; 74: 5463-7.
60. Ross JS, Cronin M. Whole cancer genome sequencing by next-generation methods. Am. J. Clin. Pathol. 2011; 136: 527-39.
61. Williams C, Ponten F, Moberg C etal. A high frequency of sequence alterations is due to formalin fixation of archival specimens. Am. J. Pathol. 1999; 155: 1467-71.
62. Kerick M, Isau M, Timmermann B etal. Targeted high throughput sequencing in clinical cancer settings: formaldehyde fixed-paraffin embedded (FFPE) tumor tissues, input amount and tumor heterogeneity. BMC Med. Genomics 2011; 4: 68.
63. Solassol J, Ramos J, Crapez E etal. KRAS mutation detection in Paired Frozen and Formalin-Fixed Paraffin-Embedded (FFPE) colorectal cancer tissues. Int. J. Mol. Sci. 2011; 12: 3191-204.
64. Schweiger MR, Kerick M, Timmermann B etal. Genome-wide massively parallel sequencing of formaldehyde fixed-paraffin embedded (FFPE) tumor tissues for copy-number- and mutation-analysis. PLoS ONE 2009; 4: e5548.
65. Chiang DY, Getz G, Jaffe DB etal. High-resolution mapping of copy-number alterations with massively parallel sequencing. Nat. Methods 2009; 6: 99-103.
66. Gusnanto A, Wood HM, Pawitan Y, Rabbitts P, Berri S. Correcting for cancer genome size and tumour cell content enables better estimation of copy number alterations from next-generation sequence data. Bioinformatics 2012; 28: 40-7.
67. Wood HM, Belvedere O, Conway C etal. Using next-generation sequencing for high resolution multiplex analysis of copy number variation from nanogram quantities of DNA from formalin-fixed paraffin-embedded specimens. Nucleic Acids Res. 2010; 38: e151.
68. Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer 2011; 11: 726-34.
69. Han YC, Yu YP, Tseng GC, Luo JH. Trypsin and reduction method to prepare DNA from formalin-fixed paraffin-embedded samples for methylation analysis. Histopathology 2009; 54: 773-5.
70. Kitazawa S, Kitazawa R, Maeda S. Identification of methylated cytosine from archival formalin-fixed paraffin-embedded specimens. Lab. Invest. 2000; 80: 275-6.
71. Doyle B, O'Riain C, Appleton K. Pyrosequencing of DNA extracted from formalin-fixed paraffin-embedded tissue. Methods Mol. Biol. 2011; 724: 181-90.
72. Mikeska T, Felsberg J, Hewitt CA, Dobrovic A. Analysing DNA methylation using bisulphite pyrosequencing. Methods Mol. Biol. 2011; 791: 33-53.
73. Zon G, Barker MA, Kaur P etal. Formamide as a denaturant for bisulfite conversion of genomic DNA: bisulfite sequencing of the GSTPi and RARbeta2 genes of 43 formalin-fixed paraffin-embedded prostate cancer specimens. Anal. Biochem. 2009; 392: 117-25.
74. Balic M, Pichler M, Strutz J etal. High quality assessment of DNA methylation in archival tissues from colorectal cancer patients using quantitative high-resolution melting analysis. J. Mol. Diagn. 2009; 11: 102-8.
75. Dallol A, Al-Ali W, Al-Shaibani A, Al-Mulla F. Analysis of DNA methylation in FFPE tissues using the MethyLight technology. Methods Mol. Biol. 2011; 724: 191-204.
76. Harbeck N, Nimmrich I, Hartmann A etal. Multicenter study using paraffin-embedded tumor tissue testing PITX2 DNA methylation as a marker for outcome prediction in tamoxifen-treated, node-negative breast cancer patients. J. Clin. Oncol. 2008; 26: 5036-42.
77. Kristensen LS, Wojdacz TK, Thestrup BB, Wiuf C, Hager H, Hansen LL. Quality assessment of DNA derived from up to 30 years old formalin fixed paraffin embedded (FFPE) tissue for PCR-based methylation analysis using SMART-MSP and MS-HRM. BMC Cancer 2009; 9: 453.
78. Vlassenbroeck I, Califice S, Diserens AC etal. Validation of real-time methylation-specific PCR to determine O6-methylguanine-DNA methyltransferase gene promoter methylation in glioma. J. Mol. Diagn. 2008; 10: 332-7.
79. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc. 2011; 6: 468-81.
80. Conway K, Edmiston SN, Khondker ZS etal. DNA-methylation profiling distinguishes malignant melanomas from benign nevi. Pigment Cell Melanoma Res. 2011; 24: 352-60.
81. Eberle FC, Hanson JC, Killian JK etal. Immunoguided laser assisted microdissection techniques for DNA methylation analysis of archival tissue specimens. J. Mol. Diagn. 2010; 12: 394-401.
82. Thirlwell C, Eymard M, Feber A etal. Genome-wide DNA methylation analysis of archival formalin-fixed paraffin-embedded tissue using the Illumina Infinium HumanMethylation27 BeadChip. Methods 2010; 52: 248-54.
83. Wilhelm-Benartzi CS, Koestler DC, Houseman EA etal. DNA methylation profiles delineate etiologic heterogeneity and clinically important subgroups of bladder cancer. Carcinogenesis 2010; 31: 1972-6.
84. Boerno ST, Grimm C, Lehrach H, Schweiger MR. Next-generation sequencing technologies for DNA methylation analyses in cancer genomics. Epigenomics 2010; 2: 199-207.
85. Gu H, Bock C, Mikkelsen TS etal. Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution. Nat. Methods 2010; 7: 133-6.
86. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-8.
87. Lu J, Getz G, Miska EA etal. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834-8.
88. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006; 6: 857-66.
89. Liu A, Xu X. MicroRNA isolation from formalin-fixed, paraffin-embedded tissues. Methods Mol. Biol. 2011; 724: 259-67.
90. Lehmann U. MicroRNA-profiling in formalin-fixed paraffin-embedded specimens. In: Monticelli S (ed.). Micrornas and the Immune System: Methods and Protocols. New York: Humana Press Inc., 2010; 113-25.