Mouse mesenchymal stem cells expressing PAX-FKHR form alveolar rhabdomyosarcomas by cooperating with secondary mutations

Cancer Research

Volumn 68, Issue 16, 2008, Pages 6587-6597

  Ren, Yue Xin ^a,c   Finckenstein, Friedrich Graf ^a   Abdueva, Diana A ^b   Shahbazian, Violette ^a   Chung, Brile ^d   Weinberg, Kenneth I ^d   Triche, Timothy J ^a,b   Shimada, Hiroyuki ^a,b   Anderson, Michael J ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; MYOD PROTEIN; MYOGENIN; PAIRED BOX TRANSCRIPTION FACTOR; PROTEIN P53; TRANSCRIPTION FACTOR FKHR; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; ONCOPROTEIN; PAX3 PROTEIN, MOUSE; PAX7 PROTEIN, MOUSE; TRANSCRIPTION FACTOR PAX7; VIRUS T ANTIGEN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL LINEAGE; CONTROLLED STUDY; FUSION GENE; GENE MUTATION; MESENCHYMAL STEM CELL; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; BONE MARROW; C57BL MOUSE; CELL DIFFERENTIATION; CHILD; CYTOLOGY; FIBROBLAST; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MACROPHAGE; METABOLISM; MUTATION; NUDE MOUSE; ONCOGENE RAS; PATHOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; ANTIGENS, VIRAL, TUMOR; BLOTTING, WESTERN; BONE MARROW; CELL DIFFERENTIATION; CHILD; FIBROBLASTS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; HUMANS; MACROPHAGES; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, NUDE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MUTATION; MYOGENIN; ONCOGENE PROTEINS, FUSION; PAIRED BOX TRANSCRIPTION FACTORS; PAX7 TRANSCRIPTION FACTOR; RHABDOMYOSARCOMA, ALVEOLAR; TUMOR SUPPRESSOR PROTEIN P53;

EID: 53049083206     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0859     Document Type: Article

References (47)

1. Ries LAG, Smith MA, Gurney JG, et al. Cancer incidence and survival among children and adolescents: United States SEER Program 1975-1995. Bethesda (MD): National Cancer Institute, SEER Program NIH Pub. No. 99-4649; 1999.
2. 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.
3. Weiss SW, Goldblum JR. Enzinger and Weiss's soft tissue tumors. 4th ed. St. Louis (MO):2001.
4. Breneman JC, Lyden E, Pappo AS, et al. Prognostic factors and clinical outcomes in children and adolescents with metastatic rhabdomyo sarcoma-a report from the Intergroup Rhabdomyosarcoma Study IV. J Clin Oncol 2003;21:78-84.
5. Crist WM, Anderson JR, Meza JL, et al. Intergroup rhabdomyosarcoma study-IV: results for patients with nonmetastatic disease. J Clin Oncol 2001;19:3091-102.
6. Mercado GE, Barr FG. Fusions involving PAX and FOX genes in the molecular pathogenesis of alveolar rhabdomyosarcoma: recent advances. Curr Mol Med 2007;7:47-61.
7. Bennicelli JL, Edwards RH, Barr FG. Mechanism for transcriptional gain of function resulting from chromosomal translocation in alveolar rhabdomyosarcoma. Proc Natl Acad Sci U S A 1996;93:5455-9.
8. Fredericks WJ, Galili N, Mukhopadhyay S, et al. The PAX3-FKHR fusion protein created by the t(2;13) translocation in alveolar rhabdomyosarcomas is a more potent transcriptional activator than PAX3. Mol Cell Biol 1995;15:1522-35.
9. Sublett JE, Jeon IS, Shapiro DN. The alveolar rhabdomyosarcoma PAX3/FKHR fusion protein is a transcriptional activator. Oncogene 1995; 11:545-52.
10. Sorensen 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.
11. 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;66:6936-46.
12. Morotti RA, Nicol KK, Parham DM, et al. An immunohistochemical algorithm to facilitate diagnosis and subtyping of rhabdomyosarcoma: the Children's Oncology Group experience. Am J Surg Pathol 2006;30:962-8.
13. Perry RL, Rudnick MA. Molecular mechanisms regulating myogenic determination and differentiation. Front Biosci 2000;5:D750-67.
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 USA 1999;96:13264-9.
15. Graf Finckenstein F, Shahbazian V, Davicioni E, Ren YX, Anderson MJ. PAX-FKHR function as pangenes by simultaneously inducing and inhibiting myogenesis. Oncogene 2008;27:2004-14.
16. Zhang L, Wang C. Identification of a new class of PAX3-FKHR target promoters: a role of the Pax3 paired box DNA binding domain. Oncogene 2007;26:595-605.
17. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002;20:530-41.
18. Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 1995;18:1417-26.
19. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 2001;25:402-8.
20. Hahn WC, Dessain SK, Brooks MW, et al Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol Cell Biol 2002;22:2111-23.
21. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and pl6INK4a. Cell 1997;88:593-602.
22. Shaulian E, Zauberman A, Ginsberg D, Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequencespecific DNA binding. Mol Cell Biol 1992;12:5581-92.
23. Morgenstern JP, Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 1990;18:3587-96.
24. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 2004;103:1662-8.
25. Djouad F, Bony C, Haupl T, et al. Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther 2005;7:R1304-15.
26. Hawley RG, Lieu EH, Fong AZ, Hawley TS. Versatile retroviral vectors for potential use in gene therapy. Gene Ther 1994;1:136-8.
27. Anderson MJ, Shelton GD, Cavenee WK, Arden KC. Embryonic 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.
28. Finckenstein FG, Davicioni E, Osborn KG, Cavenee WK, Arden KC, Anderson MJ. Transgenic mice expressing PAX3-FKHR have multiple defects in muscle development, including ectopic skeletal myogenesis in the developing neural tube. Transgenic Res 2006;15:595-614.
29. Dyson N, Buchkovich K, Whyte P, Harlow E. Cellular proteins that are targeted by DNA tumor viruses for transformation. Princess Takamatsu Symposia 1989;20:191-8.
30. Levine AJ. The p53 protein and its interactions with the oncogene products of the small DNA tumor viruses. Virology 1990;177:419-26.
31. 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.
32. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3: Article3.
33. Mathur S, Dolo S. A new efficient statistical test for detecting variability in the gene expression data. Stat Methods Med Res. Epub 2007 Aug. 14.
34. Sharp R, Recio JA, Jhappan C, et al. Synergism between INK4a/ARF inactivation and aberrant HGF/SF signaling in rhabdomyosarcomagenesis. Nat Med 2002;8:1276-80.
35. Linardic CM, Downie DL, Qualman S, Bentley RC, Counter CM. Genetic modeling of human rhabdomyosarcoma. Cancer Res 2005;65:4490-5.
36. Scuoppo C, Riess I, Schmitt-Ney M, et al. The oncogenic transcription factor PAX3-FKHR can convert fibroblasts into contractile myotubes. Exp Cell Res 2007; 313:2308-17.
37. Xia SJ, Barr FG. Analysis of the transforming and growth suppressive activities of the PAX3-FKHR oncoprotein. Oncogene 2004;23:6864-71.
38. Xia SJ, Pressey JG, Barr FG. Molecular pathogenesis of rhabdomyosarcoma. Cancer Biol Ther 2002;1:97-104.
39. Williamson D, Lu YJ, Gordon T, et al. Relationship between MYCN copy number and expression in rhabdomyosarcomas and correlation with adverse prognosis in the alveolar subtype. J Clin Oncol 2005;23:880-8.
40. Merlino G, Helman LJ. Rhabdomyosarcoma-working out the pathways. Oncogene 1999;18:5340-8.
41. 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.
42. Keller C, Arenkiel BR, Coffin CM, El-Bardeesy N, DePinho RA, Capecchi MR. Alveolar rhabdomyosarcomas in conditional Pax3: Fkhr mice: cooperativity of Ink4a/ARF and Trp53 loss of function. Genes Dev 2004; 18:2614-26.
43. Castillero-Trejo Y, Eliazer S, Xiang L, Richardson JA, Ilaria RL, Jr. Expression of the EWS/FLI-1 oncogene in murine primary bone-derived cells results in EWS/FLI-1-dependent, Ewing sarcoma-like tumors. Cancer Res 2005;65:8698-705.
44. Riggi N, Cironi L, Provero P, et al. Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res 2005;65:11459-68.
45. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, Delattre O. Mesenchymal stem cell features of Ewing tumors. Cancer Cell 2007;11:421-9.
46. Riggi N, Cironi L, Provero P, et al. Expression of the FUS-CHOP fusion protein in primary mesenchymal progenitor cells gives rise to a model of myxoid liposarcoma. Cancer Res 2006;66:7016-23.
47. Matushansky I, Hernando E, Socci ND, et al. Derivation of sarcomas from mesenchymal stem cells via inactivation of the Wnt pathway. J Clin Inv 2007;117:3248-57.