Microarray gene expression analysis of fixed archival tissue permits molecular classification and identification of potential therapeutic targets in diffuse large B-cell lymphoma

Journal of Molecular Diagnostics

Volumn 14, Issue 3, 2012, Pages 223-232

  Linton, Kim ^a   Howarth, Christopher ^a   Wappett, Mark ^b   Newton, Gillian ^b   Lachel, Cynthia ^b   Iqbal, Javeed ^c   Pepper, Stuart ^b   Byers, Richard ^a   Chan, Wing ^c   Radford, John ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b University of Manchester   (United Kingdom)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FORMALDEHYDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARAFFIN;

ADULT; ARTICLE; BAYES THEOREM; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; GENE EXPRESSION; GERMINAL CENTER; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LARGE CELL LYMPHOMA; MICROARRAY ANALYSIS; PROBABILITY;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA, LARGE B-CELL, DIFFUSE; MOLECULAR DIAGNOSTIC TECHNIQUES; MOLECULAR TARGETED THERAPY; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARAFFIN EMBEDDING; TISSUE FIXATION;

EID: 84859576433     PISSN: 15251578     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmoldx.2012.01.008     Document Type: Article

References (50)

1. C. Gisselbrecht, B. Glass, N. Mounier, G.D. Singh, D.C. Linch, M. Trneny, A. Bosly, N. Ketterer, O. Shpilberg, H. Hagberg, D. Ma, J. Briere, C.H. Moskowitz, N. Schmitz Salvage regimens with autologous transplantation for relapsed large B-cell lymphoma in the rituximab era J Clin Oncol 28 2010 4184 4190
2. A. Pavan, M. Spina, V. Canzonieri, S. Sansonno, G. Toffoli, V. De Re Recent prognostic factors in diffuse large B-cell lymphoma indicate NF-kappaB pathway as a target for new therapeutic strategies Leuk Lymphoma 49 2008 2048 2058
3. K. Dunleavy, S. Pittaluga, M.S. Czuczman, S.S. Dave, G. Wright, N. Grant, M. Shovlin, E.S. Jaffe, J.E. Janik, L.M. Staudt, W.H. Wilson Differential efficacy of bortezomib plus chemotherapy within molecular subtypes of diffuse large B-cell lymphoma Blood 113 2009 6069 6076
4. J. Ruan, P. Martin, R.R. Furman, S.M. Lee, K. Cheung, J.M. Vose, A. Lacasce, J. Morrison, R. Elstrom, S. Ely, A. Chadburn, E. Cesarman, M. Coleman, J.P. Leonard Bortezomib plus CHOP-rituximab for previously untreated diffuse large B-cell lymphoma and mantle cell lymphoma J Clin Oncol 29 2011 690 697
5. T.E. Witzig, J.M. Vose, Z.P. Luigi, C.B. Reeder, R. Buckstein, J.A. Polikoff, R. Bouabdallah, C. Haioun, H. Tilly, P. Guo, D. Pietronigro, A.L. Ervin-Haynes, M.S. Czuczman An international phase II trial of single-agent lenalidomide for relapsed or refractory aggressive B-cell non-Hodgkin's lymphoma Ann Oncol 22 2011 1622 1627
6. A. Sawas, C. Diefenbach, O.A. O'Connor New therapeutic targets and drugs in non-Hodgkin's lymphoma Curr Opin Hematol 18 2011 280 287
7. A. Alizadeh, M. Eisen, R.E. Davis, C. Ma, H. Sabet, T. Tran, J.I. Powell, L. Yang, G.E. Marti, D.T. Moore, J.R. Hudson Jr, W.C. Chan, T. Greiner, D. Weisenburger, J.O. Armitage, I. Lossos, R. Levy, D. Botstein, P.O. Brown, L.M. Staudt The lymphochip: a specialized cDNA microarray for the genomic-scale analysis of gene expression in normal and malignant lymphocytes Cold Spring Harb Symp Quant Biol 64 1999 71 78
8. G. Wright, B. Tan, A. Rosenwald, E.H. Hurt, A. Wiestner, L.M. Staudt A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma Proc Natl Acad Sci U S A 100 2003 9991 9996
9. G. Lenz, G.W. Wright, N.C. Emre, H. Kohlhammer, S.S. Dave, R.E. Davis, S. Carty, L.T. Lam, A.L. Shaffer, W. Xiao, J. Powell, A. Rosenwald, G. Ott, H.K. Muller-Hermelink, R.D. Gascoyne, J.M. Connors, E. Campo, E.S. Jaffe, J. Delabie, E.B. Smeland, L.M. Rimsza, R.I. Fisher, D.D. Weisenburger, W.C. Chan, L.M. Staudt Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways Proc Natl Acad Sci U S A 105 2008 13520 13525
10. G. Lenz, G. Wright, S.S. Dave, W. Xiao, J. Powell, H. Zhao, W. Xu, B. Tan, N. Goldschmidt, J. Iqbal, J. Vose, M. Bast, K. Fu, D.D. Weisenburger, T.C. Greiner, J.O. Armitage, A. Kyle, L. May, R.D. Gascoyne, J.M. Connors, G. Troen, H. Holte, S. Kvaloy, D. Dierickx, G. Verhoef, J. Delabie, E.B. Smeland, P. Jares, A. Martinez, A. Lopez-Guillermo Stromal gene signatures in large-B-cell lymphomas N Engl J Med 359 2008 2313 2323
11. C.P. Hans, D.D. Weisenburger, T.C. Greiner, R.D. Gascoyne, J. Delabie, G. Ott, H.K. Muller-Hermelink, E. Campo, R.M. Braziel, E.S. Jaffe, Z. Pan, P. Farinha, L.M. Smith, B. Falini, A.H. Banham, A. Rosenwald, L.M. Staudt, J.M. Connors, J.O. Armitage, W.C. Chan Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray Blood 103 2004 275 282
12. W.W. Choi, D.D. Weisenburger, T.C. Greiner, M.A. Piris, A.H. Banham, J. Delabie, R.M. Braziel, H. Geng, J. Iqbal, G. Lenz, J.M. Vose, C.P. Hans, K. Fu, L.M. Smith, M. Li, Z. Liu, R.D. Gascoyne, A. Rosenwald, G. Ott, L.M. Rimsza, E. Campo, E.S. Jaffe, D.L. Jaye, L.M. Staudt, W.C. Chan A new immunostain algorithm classifies diffuse large B-cell lymphoma into molecular subtypes with high accuracy Clin Cancer Res 15 2009 5494 5502
13. G. Gutierrez-Garcia, T. Cardesa-Salzmann, F. Climent, E. Gonzalez-Barca, S. Mercadal, J.L. Mate, J.M. Sancho, L. Arenillas, S. Serrano, L. Escoda, S. Martinez, A. Valera, A. Martinez, P. Jares, M. Pinyol, A. Garcia-Herrera, A. Martinez-Trillos, E. Gine, N. Villamor, E. Campo, L. Colomo, A. Lopez-Guillermo Gene expression profiling and not immunophenotypic algorithms predicts prognosis in patients with diffuse large B-cell lymphoma treated with immunochemotherapy Blood 117 2011 4836 4843
14. J.J. Anderson, S. Fordham, L. Overman, H. Dignum, K. Wood, S.J. Proctor, S. Crosier, B. Angus, R.E. Culpin, T. Mainou-Fowler Immunophenotyping of diffuse large B-cell lymphoma (DLBCL) defines multiple sub-groups of germinal centre-like tumours displaying different survival characteristics Int J Oncol 35 2009 961 971
15. T.A. Dunn, H. Fedor, W.B. Isaacs, A.M. De Marzo, J. Luo Genome-wide expression analysis of recently processed formalin-fixed paraffin embedded human prostate tissues Prostate 69 2009 214 218
16. G. Fedorowicz, S. Guerrero, T.D. Wu, Z. Modrusan Microarray analysis of RNA extracted from formalin-fixed, paraffin-embedded and matched fresh-frozen ovarian adenocarcinomas BMC Med Genomics 2 2009 23
17. D. Abdueva, M. Wing, B. Schaub, T. Triche, E. Davicioni Quantitative expression profiling in formalin-fixed paraffin-embedded samples by affymetrix microarrays J Mol Diagn 12 2010 409 417
18. S. Lassmann, C. Kreutz, A. Schoepflin, U. Hopt, J. Timmer, M. Werner A novel approach for reliable microarray analysis of microdissected tumor cells from formalin-fixed and paraffin-embedded colorectal cancer resection specimens J Mol Med 87 2009 211 224
19. M.L. Cox, S.M. Eddy, Z.S. Stewart, M.R. Kennel, M.Z. Man, J.D. Paulauskis, R.W. Dunstan Investigating fixative-induced changes in RNA quality and utility by microarray analysis Exp Mol Pathol 84 2008 156 172
20. L. Roberts, J. Bowers, K. Sensinger, A. Lisowski, R. Getts, M.G. Anderson Identification of methods for use of formalin-fixed, paraffin-embedded tissue samples in RNA expression profiling Genomics 94 2009 341 348
21. K. Linton, Y. Hey, S. Dibben, C. Miller, A. Freemont, J. Radford, S. Pepper Methods comparison for high-resolution transcriptional analysis of archival material on Affymetrix Plus 2.0 and Exon 1.0 microarrays Biotechniques 47 2009 587 596
22. P.M. Williams, R. Li, N.A. Johnson, G. Wright, J.D. Heath, R.D. Gascoyne A novel method of amplification of FFPET-derived RNA enables accurate disease classification with microarrays J Mol Diagn 12 2010 680 686
23. C. April, B. Klotzle, T. Royce, E. Wickham-Garcia, T. Boyaniwsky, J. Izzo, D. Cox, W. Jones, R. Rubio, K. Holton, U. Matulonis, J. Quackenbush, J.B. Fan Whole-genome gene expression profiling of formalin-fixed, paraffin-embedded tissue samples PLoS One 4 2009 e8162
24. C.C. Ton, N. Vartanian, X. Chai, M.G. Lin, X. Yuan, K.E. Malone, C.I. Li, A. Dawson, C. Sather, J. Delrow, L. Hsu, P.L. Porter Gene expression array testing of FFPE archival breast tumor samples: an optimized protocol for WG-DASL sample preparation Breast Cancer Res Treat 125 2011 879 883
25. A. Rosenwald, G. Wright, W.C. Chan, J.M. Connors, E. Campo, R.I. Fisher, R.D. Gascoyne, H.K. Muller-Hermelink, E.B. Smeland, J.M. Giltnane, E.M. Hurt, H. Zhao, L. Averett, L. Yang, W.H. Wilson, E.S. Jaffe, R. Simon, R.D. Klausner, J. Powell, P.L. Duffey, D.L. Longo, T.C. Greiner, D.D. Weisenburger, W.G. Sanger, B.J. Dave, J.C. Lynch, J. Vose, J.O. Armitage, E. Montserrat, A. Lopez-Guillermo The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma N Engl J Med 346 2002 1937 1947
26. M.A. Shipp, K.N. Ross, P. Tamayo, A.P. Weng, J.L. Kutok, R.C. Aguiar, M. Gaasenbeek, M. Angelo, M. Reich, G.S. Pinkus, T.S. Ray, M.A. Koval, K.W. Last, A. Norton, T.A. Lister, J. Mesirov, D.S. Neuberg, E.S. Lander, J.C. Aster, T.R. Golub Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning Nat Med 8 2002 68 74
27. Y. Klipper-Aurbach, M. Wasserman, N. Braunspiegel-Weintrob, D. Borstein, S. Peleg, S. Assa, M. Karp, Y. Benjamini, Y. Hochberg, Z. Laron Mathematical formulae for the prediction of the residual beta cell function during the first two years of disease in children and adolescents with insulin-dependent diabetes mellitus Med Hypotheses 45 1995 486 490
28. The International Non-Hodgkin's Lymphoma Prognostic Factors Project A predictive model for aggressive non-Hodgkin's lymphoma N Engl J Med 329 1993 987 994
29. C.L. Wilson, S.D. Pepper, Y. Hey, C.J. Miller Amplification protocols introduce systematic but reproducible errors into gene expression studies Biotechniques 36 2004 498 506
30. A.A. Alizadeh, M.B. Eisen, R.E. Davis, C. Ma, I.S. Lossos, A. Rosenwald, J.C. Boldrick, H. Sabet, T. Tran, X. Yu, J.I. Powell, L. Yang, G.E. Marti, T. Moore, J. Hudson Jr, L. Lu, D.B. Lewis, R. Tibshirani, G. Sherlock, W.C. Chan, T.C. Greiner, D.D. Weisenburger, J.O. Armitage, R. Warnke, R. Levy, W. Wilson, M.R. Grever, J.C. Byrd, D. Botstein, P.O. Brown Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling Nature 403 2000 503 511
31. J.S. Hall, H.S. Leong, L.S. Armenoult, G.E. Newton, H.R. Valentine, J.J. Irlam, C. Moller-Levet, K.A. Sikand, S.D. Pepper, C.J. Miller, C.M. West Exon-array profiling unlocks clinically and biologically relevant gene signatures from formalin-fixed paraffin-embedded tumour samples Br J Cancer 104 2011 971 981
32. S. Bonin, F. Hlubek, J. Benhattar, C. Denkert, M. Dietel, P.L. Fernandez, G. Hofler, H. Kothmaier, B. Kruslin, C.M. Mazzanti, A. Perren, H. Popper, A. Scarpa, P. Soares, G. Stanta, P.J. Groenen Multicentre validation study of nucleic acids extraction from FFPE tissues Virchows Arch 457 2010 309 317
33. J. Chen, G.E. Byrne Jr, I.S. Lossos Optimization of RNA extraction from formalin-fixed, paraffin-embedded lymphoid tissues Diagn Mol Pathol 16 2007 61 72
34. N. Masuda, T. Ohnishi, S. Kawamoto, M. Monden, K. Okubo Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples Nucleic Acids Res 27 1999 4436 4443
35. F. van Maldegem, M. de Wit, F. Morsink, A. Musler, J. Weegenaar, C.J. van Noesel Effects of processing delay, formalin fixation, and immunohistochemistry on RNA recovery from formalin-fixed paraffin-embedded tissue sections Diagn Mol Pathol 17 2008 51 58
36. J. Lee, A. Hever, D. Willhite, A. Zlotnik, P. Hevezi Effects of RNA degradation on gene expression analysis of human postmortem tissues FASEB J 19 2005 1356 1358
37. S. Nam, A. Williams, A. Vultur, A. List, K. Bhalla, D. Smith, F.Y. Lee, R. Jove Dasatinib (BMS-354825) inhibits Stat5 signaling associated with apoptosis in chronic myelogenous leukemia cells Mol Cancer Ther 6 2007 1400 1405
38. M. Masuhara, K. Nagao, M. Nishikawa, M. Sasaki, A. Yoshimura, M. Osawa Molecular cloning of murine STAP-1, the stem-cell-specific adaptor protein containing PH and SH2 domains Biochem Biophys Res Commun 268 2000 697 703
39. Z.S. Nagy, M.J. LeBaron, J.A. Ross, A. Mitra, H. Rui, R.A. Kirken STAT5 regulation of BCL10 parallels constitutive NFkappaB activation in lymphoid tumor cells Mol Cancer 8 2009 67
40. V. Joliot, F. Cormier, H. Medyouf, H. Alcalde, J. Ghysdael Constitutive STAT5 activation specifically cooperates with the loss of p53 function in B-cell lymphomagenesis Oncogene 25 2006 4573 4584
41. T. Kazemi, H. Asgarian-Omran, M. Hojjat-Farsangi, M. Shabani, A. Memarian, R.A. Sharifian, S.M. Razavi, M. Jeddi-Tehrani, H. Rabbani, F. Shokri Fc receptor-like 1-5 molecules are similarly expressed in progressive and indolent clinical subtypes of B-cell chronic lymphocytic leukemia Int J Cancer 123 2008 2113 2119
42. J. Mohan, J. Dement-Brown, S. Maier, T. Ise, B. Kempkes, M. Tolnay Epstein-Barr virus nuclear antigen 2 induces FcRH5 expression through CBF1 Blood 107 2006 4433 4439
43. M. Cotto, F. Cabanillas, M. Tirado, M.V. Garcia, E. Pacheco Epigenetic therapy of lymphoma using histone deacetylase inhibitors Clin Transl Oncol 12 2010 401 409
44. M. Snyder, X.Y. Huang, J.J. Zhang Identification of novel direct Stat3 target genes for control of growth and differentiation J Biol Chem 283 2008 3791 3798
45. N. Raffler, J. Rivera-Nieves, K. Ley L-selectin in inflammation, infection and immunity Drug Discov Today 2 2005 213 220
46. K. Uchimura, H. Muramatsu, T. Kaname, H. Ogawa, T. Yamakawa, Q.W. Fan, C. Mitsuoka, R. Kannagi, O. Habuchi, I. Yokoyama, K. Yamamura, T. Ozaki, A. Nakagawara, K. Kadomatsu, T. Muramatsu Human N-acetylglucosamine-6-O- sulfotransferase involved in the biosynthesis of 6-sulfo sialyl Lewis X: molecular cloning, chromosomal mapping, and expression in various organs and tumor cells J Biochem 124 1998 670 678
47. X. Li, T.F. Tedder CHST1 and CHST2 sulfotransferases expressed by human vascular endothelial cells: cDNA cloning, expression, and chromosomal localization Genomics 55 1999 345 347
48. S.D. Belanger, Y. St-Pierre Role of selectins in the triggering, growth, and dissemination of T-lymphoma cells: implication of L-selectin in the growth of thymic lymphoma Blood 105 2005 4800 4806
49. K. Shimizu, K. Karube, F. Arakawa, Y. Nomura, H. Komatani, K. Yamamoto, S. Yoshida, R. Aoki, Y. Sugita, M. Takeshita, K. Ohshima Upregulation of CC chemokine ligand 18 and downregulation of CX3C chemokine receptor 1 expression in human T-cell leukemia virus type 1-associated lymph node lesions: results of chemokine and chemokine receptor DNA chip analysis Cancer Sci 98 2007 1875 1880
50. S. Struyf, E. Schutyser, M. Gouwy, K. Gijsbers, P. Proost, Y. Benoit, G. Opdenakker, J. Van Damme, G. Laureys PARC/CCL18 is a plasma CC chemokine with increased levels in childhood acute lymphoblastic leukemia Am J Pathol 163 2003 2065 2075