Molecular classification of rhabdomyosarcoma - Genotypic and phenotypic determinants of diagnosis: A report from the Children's Oncology Group

American Journal of Pathology

Volumn 174, Issue 2, 2009, Pages 550-564

  Davicioni, Elai ^a,h   Anderson, Michael J ^a,c   Finckenstein, Friedrich Graf ^c   Lynch, James C ^d   Qualman, Stephen J ^e   Shimada, Hiroyuki ^a,c   Schofield, Deborah E ^a,c   Buckley, Jonathan D ^a,b   Meyer, William H ^f   Sorensen, Poul H B ^g   Triche, Timothy J ^a,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e NATIONWIDE CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^g BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^h Genome Diagnostics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A2 PROTEIN; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR AP 2BETA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CLASSIFICATION; CANCER SURVIVAL; CONTROLLED STUDY; DIFFERENTIAL DIAGNOSIS; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOSITY LOSS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 59649085853     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080631     Document Type: Article

References (59)

1. Asmar L, Gehan EA, Newton WA, Webber BL, Marsden HB, van Unnik AJ, Hamoudi AB, Shimada H, Tsokos M, Harms D: Agreement among and within groups of pathologists in the classification of rhabdomyosarcoma and related childhood sarcomas. Report of an international study of four pathology classifications. Cancer 1994, 74:2579-2588
2. Enterline HT, Horn Jr RC: Alveolar rhabdomyosarcoma; a distinctive tumor type. Am J Clin Pathol 1958, 29:356-366
3. Newton Jr WA, Gehan EA, Webber BL, Marsden HB, van Unnik AJ, Hamoudi AB, Tsokos MG, Shimada H, Harms D, Schmidt D: Classification of rhabdomyosarcomas and related sarcomas. Pathologic aspects and proposal for a new classification - an Intergroup Rhabdomyosarcoma Study. Cancer 1995, 76:1073-1085
4. Riopelle JL, Thériault JP: Sur une forme méconnue de sarcome des parties molles: le rhabdomyosarcome alvéolaire. Ann Anat Pathol (Paris) 1956, 1:88-111
5. Tsokos M, Webber BL, Parham DM, Wesley RA, Miser A, Miser JS, Etcubanas E, Kinsella T, Grayson J, Glatstein E: Rhabdomyosarcoma: a new classification scheme related to prognosis. Arch Pathol Lab Med 1992, 116:847-855
6. Leuschner I, Newton Jr WA, Schmidt D, Sachs N, Asmar L, Hamoudi A, Harms D, Maurer HM: Spindle cell variants of embryonal rhabdomyosarcoma in the paratesticular region. A report of the Intergroup Rhabdomyosarcoma Study. Am J Surg Pathol 1993, 17:221-230
7. Newton Jr WA, Soule EH, Hamoudi AB, Reiman HM, Shimada H, Beltangady M, Maurer H: Histopathology of childhood sarcomas. Intergroup Rhabdomyosarcoma Studies I and II: clinicopathologic correlation. J Clin Oncol 1988, 6:67-75
8. Breneman JC, Lyden E, Pappo AS, Link MP, Anderson JR, Parham DM, Qualman SJ, Wharam MD, Donaldson SS, Maurer HM, Meyer WH, Baker KS, Paidas CN, Crist WM: Prognostic factors and clinical outcomes in children and adolescents with metastatic rhabdomyosarcoma - a report from the Intergroup Rhabdomyosarcoma Study IV. J Clin Oncol 2003, 21:78-84
9. Crist WM, Anderson JR, Meza JL, Fryer C, Raney RB, Ruymann FB, Breneman J, Qualman SJ, Wiener E, Wharam M, Lobe T, Webber B, Maurer HM, Donaldson SS: Intergroup rhabdomyosarcoma study-IV: results for patients with nonmetastatic disease. J Clin Oncol 2001, 19:3091-3102
10. Barr FG: Fusions involving paired box and fork head family transcription factors in the pediatric cancer alveolar rhabdomyosarcoma. Curr Top Microbiol Immunol 1997, 220:113-129
11. Barr FG: Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 2001, 20:5736-5746
12. Barr FG, Qualman SJ, Macris MH, Melnyk N, Lawlor ER, Strzelecki DM, Triche TJ, Bridge JA, Sorensen PH: Genetic heterogeneity in the alveolar rhabdomyosarcoma subset without typical gene fusions. Cancer Res 2002, 62:4704-4710
13. Sorensen PH, Lynch JC, Qualman SJ, Tirabosco R, Lim JF, Maurer HM, Bridge JA, Crist WM, Triche TJ, Barr FG: PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children's oncology group. J Clin Oncol 2002, 20:2672-2679
14. Parham DM, Qualman SJ, Teot L, Barr FG, Morotti R, Sorensen PH, Triche TJ, Meyer WH: Correlation between histology and PAX/FKHR fusion status in alveolar rhabdomyosarcoma: a report from the Children's Oncology Group. Am J Surg Pathol 2007, 31:895-901
15. Besnard-Guérin C, Newsham I, Winqvist R, Cavenee WK: A common region of loss of heterozygosity in Wilms' tumor and embryonal rhabdomyosarcoma distal to the D11S988 locus on chromosome 11p15.5. Hum Genet 1996, 97:163-170
16. Visser M, Sijmons C, Bras J, Arceci RJ, Godfried M, Valentijn LJ, Voute PA, Baas F: Allelotype of pediatric rhabdomyosarcoma. Oncogene 1997, 15:1309-1314
17. Cessna MH, Zhou H, Perkins SL, Tripp SR, Layfield L, Daines C, Coffin CM: Are myogenin and myoD1 expression specific for rhabdomyosarcoma? A study of 150 cases, with emphasis on spindle cell mimics. Am J Surg Pathol 2001, 25:1150-1157
18. Tsokos M: The role of immunocytochemistry in the diagnosis of rhabdomyosarcoma. Arch Pathol Lab Med 1986, 110:776-778
19. Qualman SJ, Coffin CM, Newton WA, Hojo H, Triche TJ, Parham DM, Crist WM: Intergroup Rhabdomyosarcoma Study: update for pathologists. Pediatr Dev Pathol 1998, 1:550-561
20. Morotti RA, Nicol KK, Parham DM, Teot LA, Moore J, Hayes J, Meyer W, Qualman SJ: An immunohistochemical algorithm to facilitate diagnosis and subtyping of rhabdomyosarcoma: the Children's Oncology Group experience. Am J Surg Pathol 2006, 30:962-968
21. Raney RB, Anderson JR, Barr FG, Donaldson SS, Pappo AS, Qualman SJ, Wiener ES, Maurer HM, Crist WM: Rhabdomyosarcoma and undifferentiated sarcoma in the first two decades of life: a selective review of intergroup rhabdomyosarcoma study group experience and rationale for Intergroup Rhabdomyosarcoma Study V. J Pediatr Hematol Oncol 2001, 23:215-220
22. Schmidt D, Reimann O, Treuner J, Harms D: Cellular differentiation and prognosis in embryonal rhabdomyosarcoma. A report from the Cooperative Soft Tissue Sarcoma Study 1981 (CWS 81). Virchows Arch A Pathol Anat Histopathol 1986, 409:183-194
23. Crist WM, Garnsey L, Beltangady MS, Gehan E, Ruymann F, Webber B, Hays DM, Wharam M, Maurer HM: Prognosis in children with rhabdomyosarcoma: a report of the intergroup rhabdomyosarcoma studies I and II. Intergroup Rhabdomyosarcoma Committee. J Clin Oncol 1990, 8:443-452
24. Meyer WH, Spunt SL: Soft tissue sarcomas of childhood. Cancer Treat Rev 2004, 30:269-280
25. Quackenbush J: Microarray analysis and tumor classification. N Engl J Med 2006, 354:2463-2472
26. Lakhani SR, Ashworth A: Microarray and histopathological analysis of tumours: the future and the past? Nat Rev Cancer 2001, 1:151-157
27. Greer BT, Khan J: Diagnostic classification of cancer using DNA microarrays and artificial intelligence. Ann NY Acad Sci 2004, 1020:49-66
28. Khan J, Wei JS, Ringner M, Saal LH, Ladanyi M, Westermann F, Berthold F, Schwab M, Antonescu CR, Peterson C, Meltzer PS: Classification and diagnostic prediction of cancers using gene expression profiling and artificial neural networks. Nat Med 2001, 7:673-679
29. Ebert BL, Golub TR: Genomic approaches to hematologic malignancies. Blood 2004, 104:923-932
30. James AC, Veitch JG, Zareh AR, Triche T: Sensitivity and specificity of five abundance estimators for high-density oligonucleotide microarrays. Bioinformatics 2004, 20:1060-1065
31. Davicioni E, Finckenstein FG, Shahbazian V, Buckley JD, Triche TJ, Anderson MJ: Identification of a PAX-FKHR gene expression signature that defines molecular classes and determines the prognosis of alveolar rhabdomyosarcomas. Cancer Res 2006, 66:6936-6946
32. Tibshirani R, Hastie T, Narasimhan B, Chu G: Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci USA 2002, 99:6567-6572
33. Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121
34. Hosack DA, Dennis Jr G, Sherman BT, Lane HC, Lempicki RA: Identifying biological themes within lists of genes with EASE. Genome Biol 2003, 4:R70
35. Wachtel M, Runge T, Leuschner I, Stegmaier S, Koscielniak E, Treuner J, Odermatt B, Behnke S, Niggli FK, Schafer BW: Subtype and prognostic classification of rhabdomyosarcoma by immunohistochemistry. J Clin Oncol 2006, 24:816-822
36. Wachtel M, Dettling M, Koscielniak E, Stegmaier S, Treuner J, Simon-Klingenstein K, Buhlmann P, Niggli FK, Schafer BW: Gene expression signatures identify rhabdomyosarcoma subtypes and detect a novel t(2;2)(q35;p23) translocation fusing PAX3 to NCOA1. Cancer Res 2004, 64:5539-5545
37. Laé M, Ahn EH, Mercado GE, Chuai S, Edgar M, Pawel BR, Olshen A, Barr FG, Ladanyi M: Global gene expression profiling of PAX-FKHR fusion-positive alveolar and PAX-FKHR fusion-negative embryonal rhabdomyosarcomas. J Pathol 2007, 212:143-151
38. Mercado GE, Xia SJ, Zhang C, Ahn EH, Gustafson DM, Lae M, Ladanyi M, Barr FG: Identification of PAX3-FKHR-regulated genes differentially expressed between alveolar and embryonal rhabdomyosarcoma: focus on MYCN as a biologically relevant target. Genes Chromosom Cancer 2008, 47:510-520
39. Simon R, Radmacher MD, Dobbin K, McShane LM: Pitfalls in the use of DNA microarray data for diagnostic and prognostic classification. J Natl Cancer Inst 2003, 95:14-18
40. Carter RL, Jameson CF, Philp ER, Pinkerton CR: Comparative phenotypes in rhabdomyosarcomas and developing skeletal muscle. Histopathology 1990, 17:301-309
41. Tonin PN, Scrable H, Shimada H, Cavenee WK: Muscle-specific gene expression in rhabdomyosarcomas and stages of human fetal skeletal muscle development. Cancer Res 1991, 51:5100-5106
42. Huang J, Wei W, Zhang J, Liu G, Bignell GR, Stratton MR, Futreal PA, Wooster R, Jones KW, Shapero MH: Whole genome DNA copy number changes identified by high density oligonucleotide arrays. Hum Genomics 2004, 1:287-299
43. Hoque MO, Lee CC, Cairns P, Schoenberg M, Sidransky D: Genome-wide genetic characterization of bladder cancer: a comparison of high-density single-nucleotide polymorphism arrays and PCR-based microsatellite analysis. Cancer Res 2003, 63:2216-2222
44. Mei R, Galipeau PC, Prass C, Berno A, Ghandour G, Patil N, Wolff RK, Chee MS, Reid BJ, Lockhart DJ: Genome-wide detection of allelic imbalance using human SNPs and high-density DNA arrays. Genome Res 2000, 10:1126-1137
45. Nielsen TO, West RB, Linn SC, Alter O, Knowling MA, O'Connell JX, Zhu S, Fero M, Sherlock G, Pollack JR, Brown PO, Botstein D, van de Rijn M: Molecular characterisation of soft tissue tumours: a gene expression study. Lancet 2002, 359:1301-1307
46. Segal NH, Pavlidis P, Antonescu CR, Maki RG, Noble WS, DeSantis D, Woodruff JM, Lewis JJ, Brennan MF, Houghton AN, Cordon-Cardo C: Classification and subtype prediction of adult soft tissue sarcoma by functional genomics. Am J Pathol 2003, 163:691-700
47. Anderson J, Ramsay A, Gould S, Pritchard-Jones K: PAX3-FKHR induces morphological change and enhances cellular proliferation and invasion in rhabdomyosarcoma. Am J Pathol 2001, 159:1089-1096
48. Bridge JA, Liu J, Qualman SJ, Suijkerbuijk R, Wenger G, Zhang J, Wan X, Baker KS, Sorensen P, Barr FG: Genomic gains and losses are similar in genetic and histologic subsets of rhabdomyosarcoma, whereas amplification predominates in embryonal with anaplasia and alveolar subtypes. Genes Chromosom Cancer 2002, 33:310-321
49. Chi N, Epstein JA: Getting your Pax straight: Pax proteins in development and disease. Trends Genet 2002, 18:41-47
50. Robson EJ, He SJ, Eccles MR: A PANorama of PAX genes in cancer and development. Nat Rev Cancer 2006, 6:52-62
51. Bridge JA, Liu J, Weibolt V, Baker KS, Perry D, Kruger R, Qualman S, Barr F, Sorensen P, Triche T, Suijkerbuijk R: Novel genomic imbalances in embryonal rhabdomyosarcoma revealed by comparative genomic hybridization and fluorescence in situ hybridization: an intergroup rhabdomyosarcoma study. Genes Chromosom Cancer 2000, 27:337-344
52. Gordon T, McManus A, Anderson J, Min T, Swansbury J, Pritchard-Jones K, Shipley J: Cytogenetic abnormalities in 42 rhabdomyosarcomas: a United Kingdom Cancer Cytogenetics Group Study. Med Pediatr Oncol 2001, 36:259-267
53. Barr FG, Smith LM, Lynch JC, Strzelecki D, Parham DM, Qualman SJ, Breitfeld PP: Examination of gene fusion status in archival samples of alveolar rhabdomyosarcoma entered on the Intergroup Rhabdomyosarcoma Study-III trial: a report from the Children's Oncology Group. J Mol Diagn 2006, 8:202-208
54. Anderson J, Gordon A, McManus A, Shipley J, Pritchard-Jones K: Disruption of imprinted genes at chromosome region 11p15.5 in paediatric rhabdomyosarcoma. Neoplasia 1999, 1:340-348
55. Anderson J, Gordon A, Pritchard-Jones K, Shipley J: Genes, chromosomes, and rhabdomyosarcoma. Genes Chromosom Cancer 1999, 26:275-285
56. Kamb A: Consequences of nonadaptive alterations in cancer. Mol Biol Cell 2003, 14:2201-2205
57. Cavazzana AO, Schmidt D, Ninfo V, Harms D, Tollot M, Carli M, Treuner J, Betto R, Salviati G: Spindle cell rhabdomyosarcoma. A prognostically favorable variant of rhabdomyosarcoma. Am J Surg Pathol 1992, 16:229-235
58. Herrera-Gayol A, Royal A, Babai F: Correlation between cell differentiation stage, types of invasion, and hematogenous metastasis in experimental rhabdomyosarcomas. Exp Mol Pathol 1995, 63:1-15
59. Massi D, Beltrami G, Capanna R, Franchi A: Histopathological reclassification of extremity pleomorphic soft tissue sarcoma has clinical relevance. Eur J Surg Oncol 2004, 30:1131-1136