Identification of a PAX-FKHR gene expression signature that defines molecular classes and determines the prognosis of alveolar rhabdomyosarcomas

Cancer Research

Volumn 66, Issue 14, 2006, Pages 6936-6946

  Davicioni, Elai ^a,b   Finckenstein, Friedrich Graf ^d   Shahbazian, Violette ^d   Buckley, Jonathan D ^b,c   Triche, Timothy J ^a,b,d   Anderson, Michael J ^a,b,d  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d CHILDREN S HOSPITAL LOS ANGELES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7;

ARTICLE; CANCER RESEARCH; CANCER SURVIVAL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; FUSION GENE; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; RHABDOMYOSARCOMA; RISK FACTOR; SURVIVAL TIME;

CELL LINE, TUMOR; CHILD; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ONCOGENE PROTEINS, FUSION; PAIRED BOX TRANSCRIPTION FACTORS; PAX7 TRANSCRIPTION FACTOR; PROGNOSIS; RHABDOMYOSARCOMA, ALVEOLAR; TUMOR MARKERS, BIOLOGICAL;

EID: 33746895755     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-4578     Document Type: Article

References (61)

1. Pappo AS, Shapio DN, Crist WM, Maurer HM. Biology and therapy of pediatric rhabdomyosarcoma. J Clin Oncol 1995;13:2123-39.
2. Merlino G, Helman LJ. Rhabdomyosarcoma-working out the pathways. Oncogene 1999;18:5340-8.
3. Qualman SJ, Morotti RA. Risk assignment in pediatric soft-tissue sarcomas: an evolving molecular classification. Curr Oncol Rep 2002;4:123-30.
4. Breneman JC, Lyden E, Pappo AS, et al. 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.
5. Tobar A, Avigad S, Zoldan M, Mor C, Goshen Y, Zaizov R. Clinical relevance of molecular diagnosis in childhood rhabdomyosarcoma. Diagn Mol Pathol 2000;9:9-13.
6. Sorenson PH, Lynch JC, Qualman SJ, et al. 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;20:2672-9
7. Barr FG, Qualman SJ, Macris MH, et al. Genetic heterogeneity in the alveolar rhabdomyosarcoma subset without typical gene fusions. Cancer Res 2002;62:4704-10.
8. Anderson J, Gordon T, McManus A, et al. Detection of the PAX3-FKHR fusion gene in paediatric rhabdomyosarcoma: a reproducible predictor of outcome? Br J Cancer 2001;85:831-5.
9. Kilpatrick SE, Teot LA, Geisinger KR, et al. Relationship of DNA ploidy to histology and prognosis in rhabdomyosarcoma. Comparison of flow cytometry and image analysis. Cancer 1994;74:3227-33.
10. Galili N, Davis RJ, Fredericks WJ, et al. Fusion of a fork head, domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;5:230-5.
11. Sublett JE, Jeon IS, Shapiro DN. The alveolar rhabdomyosarcoma PAX3/FKHR fusion protein is a transcriptional activator. Oncogene 1995;11:545-52.
12. del Peso L, Gonzalez VM, Hernandez R, Barr FG, Nunez G. Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene 1999;18:7328-33.
13. Bennicelli JL, Fredericks WJ, Wilson RB, Rauscher FJ III, Barr FG. Wild type PAX3 protein and the PAX3-FKHR fusion protein of alveolar rhabdomyosarcoma contain potent, structurally distinct transcriptional activation domains. Oncogene 1995;11:119-30.
14. Khan J, Bittner ML, Saal LH, et al. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc Natl Acad Sci U S A 1999;96:13264-9.
15. Barber TD, Barber MC, Tomescu O, Barr FG, Ruben S, Friedman TB. Identification of target genes regulated by PAX3 and PAX3-FKHR in embryogenesis and alveolar rhabdomyosarcoma. Genomics 2002;79:278-84.
16. Begum S, Emani N, Cheung A, Wilkins O, Der S, Hamel PA. Cell-type-specific regulation of distinct sets of gene targets by Pax3 and Pax3/FKHR. Oncogene 2005;24:1860-72.
17. Xia SJ, Barr FG. Analysis of the transforming and growth suppressive activities of the PAX3-FKHR oncoprotein. Oncogene 2004;23:6864-71.
18. Newton WA, Jr., Gehan EA, Webber BL, et al. Classification of rhabdomyosarcomas and related sarcomas. Pathologic aspects and proposal for a new classification-an Intergroup Rhabdomyosarcoma Study. Cancer 1995;76:1073-85.
19. Anderson MJ, Shelton GD, Cavenec WK, Arden KC. Fmbryonic expression of the tumor-associated PAX3-FKHR fusion protein interferes with the developmental functions of Pax3. Proc Natl Acad Sci U S A 2001;98:1589-94.
20. Persons DA, Allay JA, Allay ER, et al. Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood 1999;93:488-99.
21. Torchia EC, Jaishankur S, Baker SJ. Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res 2003;63:3464-8.
22. Soneoka Y, Cannon PM, Ramsdale EE, et al. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res 1995;23:628-33.
23. Han JY, Cannon PM, Lai KM, Zhao Y, Eiden MV, Anderson WF. Identification of envelope protein residues required for the expanded host range of 10AI murine leukemia virus. J Virol 1997;71:8103-8.
24. Page KA, Landau NR, Littman DK. Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity. J Virol 1990;64:5270-6.
25. Peter M, Gilbert E, Delattre O. A multiplex real-time PCR assay for the detection of gene fusions observed in solid tumors. Lab Invest 2001;81:905-12.
26. Plattner R, Anderson MJ, Sato KY, Fasching CL, Der CJ, Stanbridge KJ. Loss of oncogenic ras expression does not correlate with loss of tumorigenicity in human cells. Proc Natl Acad Sci U S A 1996;93:6665-70.
27. Chalepakis G, Fritsch R, Fickenscher H, Deutsch U, Goulding M, Gruss P. The molecular basis of the undulated/Pax-1 mutation. Cell 1991;66:873-84.
28. James AC, Veitch JG, Zareh AR, Triche T. Sensitivity and specificity of five abundance estimators for high-density oligonucleotide microarrays. Bioinformatics 2004;20:1060-5.
29. Hosack DA, Dennis G, Jr., Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol 2003;4:R70.
30. Zeng F, Schultz RM. RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 2005;283:40-57.
31. Becker KG, Hosack DA, Dennis G, Jr., et al. PubMatrix: a tool for multiplex literature mining. BMC Bioinformatics 2003;4:61.
32. Tiffin N, Williams RD, Shipley J, Pritchard-Jones K. PAX7 expression in embryonal rhabdomyosarcoma suggests an origin in muscle satellite cells. Br J Cancer 2003;89:327-32.
33. 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;159:1089-96.
34. Barr FG. Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 2001;20:5736-46.
35. Wachtel M, Dettling M, Koscielniak K, et al. Gene expression signatures identify rhabdomyosarcoma subtypes and detect a novel t(2;2)(q35;p23) translocation fusing PAX3 to NCOA1. Cancer Res 2004;64:5539-45.
36. Hu-Lieskovan S, Zhang J, Wu L, Shimada H, Schofield DE, Triche TJ. EWS-FLI1 fusion protein up-regulates critical genes in neural crest development and is responsible for the observed phenotype of Ewing's family of tumors. Cancer Res 2005;65:4633-44.
37. Keller C, Hansen MS, Coffin CM, Capecchi MR. Pax3:Fkhr interferes with embryonic Pax3 and Pax7 function: implications for alveolar rhabdomyosarcoma cell of origin. Genes Dev 2004;18:2608-13.
38. Linardic CM, Downie DL, Qualman S, Bentley RC, Counter CM. Genetic modeling of human rhabdomyosarcoma. Cancer Res 2005;65:4490-5.
39. Epstein JA, Lam P, Jepeal L, Maas RL, Shapiro DN. Pax3 inhibits myogenic differentiation of cultured myoblast cells. J Biol Chem 1995;270:11719-22.
40. Blais A, Tsikitis M, Acosta-Alvear D, Sharan R, Kluger Y, Dynlacht BD. An initial blueprint for myogenic differentiation. Genes Dev 2005;19:553-69.
41. Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 2002;9:587-600.
42. 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;51:5100-6.
43. Berkes CA, Tapscott SJ. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 2005. 16:585-95.
44. McKinsey TA, Zhang CL, Olson EN. Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 2001;11:497-504.
45. Slack A, Chen Z, Tonelli R, et al. The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc Natl Acad Sci U S A 2005;102:731-6.
46. Butt AJ, Williams AC. IGFBP-3 and apoptosis-a license to kill? Apoptosis 2001;6:199-205.
47. Chen P, Hutter D, Yang X, Gorospe M, Davis RJ, Liu Y. Discordance between the binding affinity of mitogen-activated protein kinase subfamily members for MAP kinase phosphatase-2 and their ability to activate the phosphatase catalytically. J Biol Chem 2001;276:29440-9.
48. Sasaki A, Taketomi T, Kato H, et al. Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat Cell Biol 2003;5:427-32.
49. Hart KC, Robertson SC, Kanemitsu MY, Meyer AN, Tynan JA, Donoghue DJ. Transformation and Stat activation by derivatives of FGFR1, FGFR3, and FGFR4. Oncogene 2000;19:3309-20.
50. Li L, Zhou J, James G, Heller-Harrison R, Czech MP, Olson EN. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains. Cell 1992;71:1181-94.
51. Shaoul E, Reich-Slotky R, Berman B, Ron D. Fibroblast growth factor receptors display both common and distinct signaling pathways. Oncogene 1995;10:1553-61.
52. Asmar L, Gehan EA, Newton WA, et al. 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;74:2579-88.
53. Ruymann FB, Grovas AC. Progress in the diagnosis and treatment of rhabdomyosarcoma and related soft tissue sarcomas. Cancer Invest 2000;18:223-41.
54. Crist WM, Garnsey L, Beltangady MS, et al. Prognosis in children with rhabdomyosarcoma: a report of the Intergroup Rhabdomyosarcoma Studies I and II. Intergroup Rhabdomyosarcoma Committee. J Clin Oncol 1990;8:443-52.
55. Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004;351:2159-69.
56. Pittman J, Huang E, Dressman H, et al. Integrated modeling of clinical and gene expression information for personalized prediction of disease outcomes. Proc Natl Acad Sci U S A 2004;101:8431-6.
57. Mayanil CS, George D, Freilich L, et al. Microarray analysis detects novel Pax3 downstream target genes. J Biol Chem 2001;276:49299-309.
58. Ginsberg JP, Davis RJ, Bennicelli JL, Nauta LE, Barr FG. Up-regulation of MET but not neural cell adhesion molecule expression by the PAX3-FKHR fusion protein in alveolar rhabdomyosarcoma. Cancer Res 1998;58:3542-6.
59. Epstein JA, Shapiro DN, Cheng J, Lam PY, Maas RL. Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc Natl Acad Sci U S A 1996;93:4213-8.
60. Maroto M, Reshef R, Munsterberg AE, Koester S, Goulding M, Lassar AB. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 1997;89:139-48.
61. Zhang L, Wang C. PAX3-FKHR transformation increases 26S proteasome-dependent degradation of p27Kip1, a potential role for elevated Skp2 expression. Biol Chem 2003;278:27-36.