Ewing tumors that do not overexpress BMI-1 are a distinct molecular subclass with variant biology: A report from the children's oncology group

Clinical Cancer Research

Volumn 17, Issue 1, 2011, Pages 56-66

  Cooper, Aaron ^a   Van Doorninck, John ^a   Ji, Lingyun ^a   Russell, Darren ^a   Ladanyi, Marc ^b   Shimada, Hiroyuki ^a,b   Krailo, Mark ^b,c   Womer, Richard B ^d   Hao ru Hsu, Jessie ^e   Thomas, Dafydd ^f   Triche, Timothy J ^a,b   Sposto, Richard ^a,b   Lawlor, Elizabeth R ^e,f  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d CHILDREN S ONCOLOGY GROUP   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN; PROTEIN P16; PROTEIN P53; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TETRAZOLIUM; WNT PROTEIN;

ADOLESCENT; ADULT; ARTICLE; CELL ASSAY; CHILD; CONTROLLED STUDY; DOWN REGULATION; EWING SARCOMA; FEMALE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENOME; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRESCHOOL CHILD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCHOOL CHILD; SIGNAL TRANSDUCTION;

ADOLESCENT; ADULT; CELL LINE, TUMOR; CHILD; CHILD, PRESCHOOL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INFANT; INFANT, NEWBORN; MALE; MIDDLE AGED; NUCLEAR PROTEINS; PHENOTYPE; PROGNOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR, IGF TYPE 1; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOMA, EWING'S; YOUNG ADULT;

EID: 78751525914     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-1417     Document Type: Article

References (44)

1. Burchill SA. Ewing's sarcoma: diagnostic, prognostic, and therapeutic implications of molecular abnormalities. J Clin Pathol 2003;56:96-102.
2. Castillero-Trejo Y, Eliazer S, Xiang L, Richardson JA, Ilaria RL Jr. Expression of the EWS/FLI-1 oncogene in murine primary bonederived cells results in EWS/FLI-1-dependent, Ewing sarcoma-like tumors. Cancer Res 2005;65:8698-705.
3. Riggi N, Cironi L, Provero P, Suva ML, Kaloulis K, Garcia-Echeverria C, et al. Development of Ewing's sarcoma from primary bone marrowderived mesenchymal progenitor cells. Cancer Res 2005;65:11459-68.
4. 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.
5. Meltzer PS. Is Ewing's sarcoma a stem cell tumor? Cell Stem Cell 2007;1:13-5.
6. Coles EG, Lawlor ER, Bronner-Fraser M. EWS-FLI1 causes neuroepithelial defects and abrogates emigration of neural crest stem cells. Stem Cells 2008;26:2237-44.
7. Scotlandi K, Remondini D, Castellani G, Manara MC, Nardi F, Cantiani L, et al. Overcoming resistance to conventional drugs in Ewing sarcoma and identification of molecular predictors of outcome. J Clin Oncol 2009;27:2209-16.
8. Seddon BM, Whelan JS. Emerging chemotherapeutic strategies and the role of treatment stratification in Ewing sarcoma. Paediatr Drugs 2008;10:93-105.
9. Gil J, Bernard D, Peters G. Role of polycomb group proteins in stem cell self-renewal and cancer. DNA Cell Biol 2005;24:117-25.
10. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-60.
11. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006;66:6063-71.
12. Prince ME, Sivanandan R, Kaczorowski A, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007;104:973-8.
13. Chowdhury M, Mihara K, Yasunaga S, Ohtaki M, Takihara Y, Kimura A. Expression of Polycomb-group (PcG) protein BMI-1 predicts prognosis in patients with acute myeloid leukemia. Leukemia 2007;21:1116-22.
14. Feng Y, Song L, Guo B, Liao W, Li M, Liu W, et al. Expression and significance of Bmi-1 in breast cancer. Chinese journal of cancer 2007;26:154-7.
15. Kim JH, Yoon SY, Jeong SH, Kim SY, Moon SK, Joo JH, et al. Overexpression of Bmi-1 oncoprotein correlates with axillary lymph node metastases in invasive ductal breast cancer. Breast 2004;13: 383-8.
16. Liu JH, Song LB, Zhang X, Guo BH, Feng Y, Li XX, et al. Bmi-1 expression predicts prognosis for patients with gastric carcinoma. J Surg Oncol 2008;97:267-72.
17. van Galen JC, Muris JJ, Oudejans JJ, Vos W, Giroth CP, Ossenkoppele GJ, et al. Expression of the polycomb-group gene BMI1 is related to an unfavourable prognosis in primary nodal DLBCL. Journal of Clinical Pathology 2007;60:167-72.
18. Wang H, Pan K, Zhang HK, Weng DS, Zhou J, Li JJ, et al. Increased polycomb-group oncogene Bmi-1 expression correlates with poor prognosis in hepatocellular carcinoma. J Cancer Res Clin Oncol 2008;134:535-41.
19. Douglas D, Hsu JH, Hung L, Cooper A, Abdueva D, van Doorninck J, et al. BMI-1 promotes ewing sarcoma tumorigenicity independent of CDKN2A repression. Cancer Res 2008;68:6507-15.
20. McCabe A, Dolled-Filhart M, Camp RL, Rimm DL. Automated quantitative analysis (AQUA) of in situ protein expression, antibody concentration, and prognosis. J Natl Cancer Inst 2005;97:1808-15.
21. Cox DR, Oakes D. Analysis of Survival Data. Boca Raton: CRC Press; 1984.
22. Song S, Black MA. Microarray-based gene set analysis: a comparison of current methods. BMC Bioinf 2008;9:502.
23. Tian L, Greenberg SA, Kong SW, Altschuler J, Kohane IS, Park PJ. Discovering statistically significant pathways in expression profiling studies. Proc Natl Acad Sci USA 2005;102:13544-9.
24. Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 1995;57:289-300.
25. Hayry V, Tynninen O, Haapasalo HK, Wolfer J, Paulus W, Hasselblatt M, et al. Stem cell protein BMI-1 is an independent marker for poor prognosis in oligodendroglial tumours. Neuropathol Appl Neurobiol 2008;34:555-63.
26. Jenkin RD, Al-Fawaz I, Al-Shabanah M, Allam A, Ayas M, Khafaga Y, et al. Localised Ewing sarcoma/PNET of bone-prognostic factors and international data comparison. Med Pediatr Oncol 2002;39:586-93.
27. Rodriguez-Galindo C, Liu T, Krasin MJ, Wu J, Billups CA, Daw NC, et al. Analysis of prognostic factors in ewing sarcoma family of tumors: review of St. Jude Children's Research Hospital studies. Cancer 2007;110:375-84.
28. de Alava E, Kawai A, Healey JH, Fligman I, Meyers PA, Huvos AG, et al. EWS-FLI1 fusion transcript structure is an independent determinant of prognosis in Ewing's sarcoma. J Clin Oncol 1998;16:1248-55.
29. Deneen B, Denny CT. Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 2001;20:6731-41.
30. Lessnick SL, Dacwag CS, Golub TR. The Ewing's sarcoma oncoprotein EWS/FLI induces a p53-dependent growth arrest in primary human fibroblasts. Cancer Cell 2002;1:393-401.
31. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999; 397:164-8.
32. Huang HY, Illei PB, Zhao Z, Mazumdar M, Huvos AG, Healey JH, et al. Ewing sarcomas with p53 mutation or p16/p14ARF homozygous deletion: a highly lethal subset associated with poor chemoresponse. J Clin Oncol 2005;23:548-58.
33. Girnita A, All-Ericsson C, Economou MA, Astrom K, Axelson M, Seregard S, et al. The insulin-like growth factor-I receptor inhibitor picropodophyllin causes tumor regression and attenuates mechanisms involved in invasion of uveal melanoma cells. Acta Ophthalmol 2008;86 Thesis 4:26-34.
34. Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, Meadows AT, et al. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med 2006;355:1572-82.
35. Houghton PJ, Morton CL, Gorlick R, Kolb EA, Keir ST, Reynolds CP, et al. Initial testing of a monoclonal antibody (IMC-A12) against IGF-1R by the Pediatric Preclinical Testing Program. Pediatr Blood Cancer 2010;54:921-60.
36. Kurmasheva RT, Dudkin L, Billups C, Debelenko LV, Morton CL, Houghton PJ. The insulin-like growth factor-1 receptor-targeting antibody, CP-751,871, suppresses tumor-derived VEGF and synergizes with rapamycin in models of childhood sarcoma. Cancer Res 2009;69:7662-71.
37. Suva ML, Riggi N, Stehle JC, Baumer K, Tercier S, Joseph JM, et al. Identification of cancer stem cells in Ewing's sarcoma. Cancer Res 2009;69:1776-81.
38. Bruggeman SW, Hulsman D, Tanger E, Buckle T, Blom M, Zevenhoven J, et al. Bmi1 controls tumor development in an ink4a/arf-independent manner in a mouse model for glioma. Cancer Cell 2007;12: 328-41.
39. Bruggeman SW, Hulsman D, van Lohuizen M. Bmi1 deficient neural stem cells have increased integrin dependent adhesion to selfsecreted matrix. Biochim Biophys Acta 2009;1790:351-60.
40. Wiederschain D, Chen L, Johnson B, Bettano K, Jackson D, Taraszka J, et al. Contribution of polycomb homologues Bmi-1 and Mel-18 to medulloblastoma pathogenesis. Mol Cell Biol 2007;27: 4968-79.
41. Bachmann IM, Puntervoll HE, Otte AP, Akslen LA. Loss of BMI-1 expression is associated with clinical progress of malignant melanoma. Mod Pathol 2008;21:583-90.
42. Choi YJ, Choi YL, Cho EY, Shin YK, Sung KW, Hwang YK, et al. Expression of Bmi-1 protein in tumor tissues is associated with favorable prognosis in breast cancer patients. Breast Cancer Res Treat 2009;113:83-93.
43. Pietersen AM, Horlings HM, Hauptmann M, Langerod A, Ajouaou A, Cornelissen-Steijger P, et al. EZH2 and BMI1 inversely correlate with prognosis and TP53 mutation in breast cancer. Breast Cancer Res 2008;10:R109.
44. Mitsiades N, Poulaki V, Kotoula V, Leone A, Tsokos M. Fas ligand is present in tumors of the Ewing's sarcoma family and is cleaved into a soluble form by a metalloproteinase. Am J Pathol 1998;153: 1947-56.