The histopathology of a human mesenchymal stem cell experimental tumor model: Support for an hMSC origin for Ewing's sarcoma?

Histology and Histopathology

Volumn 23, Issue 10, 2008, Pages 1229-1240

  Burns, Jorge S ^a   Abdallah, Basem M ^a   Shrøder, Henrik D ^a   Kassem, Moustapha ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Adult bone marrow stem cells; Angiogenesis; Cancer stem cells; Cell culture

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CD34 ANTIGEN; CD99 ANTIGEN; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; ENDOGLIN; HERMES ANTIGEN; VIMENTIN; ACTIN; CELL CYCLE PROTEIN; TELOMERASE; TERT PROTEIN, HUMAN; TUMOR MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CULTURE; CELL INTERACTION; CHROMOSOME ABERRATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DIPLOIDY; ENDOTHELIUM CELL; EWING SARCOMA; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; ANIMAL; BONE DEVELOPMENT; BONE TUMOR; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL TRANSFORMATION; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOHISTOCHEMISTRY; KARYOTYPING; METABOLISM; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PATHOLOGY; TIME; TUMOR CELL LINE; VASCULARIZATION;

MURINAE;

ACTINS; ANIMALS; BONE NEOPLASMS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KARYOTYPING; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED NOD; MICE, SCID; OSTEOGENESIS; PHENOTYPE; SARCOMA, EWING'S; TELOMERASE; TIME FACTORS; TRANSFECTION; TUMOR MARKERS, BIOLOGICAL;

EID: 54449089173     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Abdallah B.M., Haack-Sorensen M., Burns J.S., Elsnab B., Jakob F., Hokland P. and Kassem M. (2005). Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation. Biochem. Biophys. Res. Commun. 326, 527-538.
2. Alldinger I., Schaefer K.L., Goedde D., Ottaviano L., Dirksen U., Ranft A., Juergens H., Gabbert H.E., Knoefel W.T. and Poremba C. (2007). Microsatellite instability in Ewing tumor is not associated with loss of mismatch repair protein expression. J. Cancer Res. Clin. Oncol. 133, 749-759.
3. Bagley R.G., Weber W., Rouleau C. and Teicher B.A. (2005). Pericytes and endothelial precursor cells: cellular interactions and contributions to malignancy. Cancer Res. 65, 9741-9750.
4. Bjerkvig R., Tysnes B.B., Aboody K.S., Najbauer J. and Terzis A.J. (2005). Opinion: the origin of the cancer stem cell: current controversies and new insights. Nat. Rev. Cancer 5, 899-904.
5. Bolontrade M.F., Zhou R.R. and Kleinerman E.S. (2002). Vasculogenesis plays a role in the growth of ewing's sarcoma in vivo. Clin. Cancer Res. 8, 3629-3627.
6. Braunreiter C.L., Hancock J.D., Coffin C.M., Boucher K.M. and Lessnick S.L. (2006). Expression of EWS-ETS fusions in NIH3T3 cells reveals significant differences to Ewing's sarcoma. Cell Cycle 5, 2753-2759.
7. Burns J.S., Abdallah B.M., Guldberg P., Rygaard J., Schroder H.D. and Kassem M. (2005). Tumorigenic heterogeneity in cancer stem cells evolved from long-term cultures of telomerase-immortalized human mesenchymal stem cells. Cancer Res. 65, 3126-3135.
8. Castillero-Trejo Y., Eliazer S., Xiang L., Richardson J.A. and Ilaria R.L.J. (2005). 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. 65, 8698-8705.
9. Clark M.A., Fisher C., Judson I. and Thomas J.M. (2005). Soft-tissue sarcomas in adults. N. Engl. J. Med. 353, 701-711.
10. Crowe D.L., Parsa B. and Sinha U.K. (2004). Relationships between stem cells and cancer stem cells. Histol. Histopathol. 19, 505-509.
11. Darbro B.W., Lee K.M., Nguyen N.K., Domann F.E. and Klingelhutz A.J. (2006). Methylation of the p16(INK4a)-promoter-region in telomerase immortalized human keratinocytes co-cultured with feeder cells. Oncogene 25, 7421-7433.
12. Delattre O., Zucman J., Melot T., Garau X.S., Zucker J.M., Lenoir G.M., Ambros P.F., Sheer D., Turc-Carel C. and Triche T.J. (1994). The Ewing family of tumors - a subgroup of small-round-cell tumors defined by specific chimeric transcripts. N. Engl. J. Med. 331, 294-299.
13. Deneen B. and Denny C.T. (2001)Loss of p16 pathways stabilizes EWS/FLI1 expression and complements EWS/FLI1 mediated transformation. Oncogene 20, 6731-6741.
14. Dvorak H.F. (1986). Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659.
15. Ewing J. (2006). The Classic: Diffuse endothelioma of bone. Proceedings of the New York Pathological Society. 1921;12:171. Clin Orthop Relat Res 450, 25-27.
16. Folberg R. and Maniotis A.J. (2004). Vasculogenic mimicry. APMIS 112, 508-525.
17. Fuchs B., Inwards C., Scully S.P. and Janknecht R. (2004). hTERT Is highly expressed in Ewing's sarcoma and activated by EWS-ETS oncoproteins. Clin. Orthop. Relat. Res. 64-68.
18. Garcia-Barros M., Paris, F., Cordon-Cardo C., Lyden D., Rafii S., Haimovitz-Friedman A., Fuks Z. and Kolesnick R. (2063). Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300, 1155-1159.
19. Gibbs C.P., Kukekov.V.G., Reith J.D., Tchigrinova O., Suslov O.N., Scott E.W. Ghivizzani S. C., Ignatova T.N. and Steindler D.A. (2005). Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 7, 967-976.
20. Grier H.E., Krailo M.D., Tarbell N.J., Link M.P., Fryer C.J., Pritchard D.J., Gebhardt M.C., Dickman P.S., Pellman E.J., Meyers P.A., Donaldson S.S., Moore S., Rausen A.R., Vietti T.J. and Miser J.S. (2003). Addition of ifosfamide and etoposide to standard chemotherapy for Ewing's sarcoma and primitive neuroectodermal tumor of bone. N. Engl J. Med. 348, 694-701.
21. Hansen M.F., Koufos A., Gallie B.L., Phillips R.A., Fodstad O., Brogger A., Gedde-Dahl T. and Cavenee W.K. (1985). Osteosarcoma and retinoblastoma: a shared chromosomal mechanism revealing recessive predisposition. Proc. Natl. Aced. Sci. USA 82, 6216-6220.
22. Helman L.J. and Meltzer P. (2003). Mechanisms of sarcoma development. Nat. Rev. Cancer 3, 685-694.
23. Kendall S.D., Linardic C.M., Adam S.J. and Counter C.M. (2005). A network of genetic events sufficient to convert normal human cells to a tumorigenic state. Cancer Res. 65, 9824-9828.
24. Kinnaird T., Stabile E., Burnett M.S. and Epstein S.E. (2004). Bone-marrow-derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences. Circ. Res. 95, 354-363.
25. Kovar H. and Bernard A. (2006). CD99-positive "Ewing's sarcoma" from mouse-bone marrow-derived mesenchymal progenitor cells? Cancer Res. 66, 9786; author reply 9786.
26. Kovar H., Jug G., Aryee D.N., Zoubek A., Ambros P., Gruber B., Windhager R. and Gadner H. (1997). Among genes involved in the RB dependent cell cycle regulatory cascade, the p16 tumor suppressor gene is frequently lost in the Ewing family of tumors. Onoogene 15, 2225-2232.
27. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., Park J.K. and Fine H.A. (2006a). Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9, 391-403.
28. Lee T.H., Bolontrade M.F., Worth L.L., Guan H., Ellis L.M. and Kleinerman E.S. (2006b). Production of VEGF165 by Ewing's sarcoma cells induces vasculogenesis and the incorporation of CD34+ stem cells into the expanding tumor vasculature. Int. J. Cancer 119, 839-846.
29. Lessnick S.L., Dacwag C.S. and Golub T.R. (2002). The Ewing's sarcoma oncoprotein EWS/FLI induces a p53-dependent growth arrest in primary human fibroblasts. Cancer Cell 1, 393-401.
30. Lin A.Y., Maniotis A.J., Valyi-Nagy K., Majumdar D., Setty S., Kadkol S., Leach L., Pe'er J. and Folberg R. (2005). Distinguishing fibrovascular septa from vasculogenic mimicry patterns. Arch. Pathol. Lab. Med. 129, 884-892.
31. Llombart-Bosch A. and Navarro S. (2001). Immunohistochemical detection of EWS and FLI-1 proteinss in Ewing sarcoma and primitive neuroectodermal tumors: comparative analysis with CD99 (MIC-2) expression. Appl. Immunohistochem. Mol. Morphol. 9, 255-260.
32. Martinez-Ramirez A., Rodriguez-Perales S., Melendez B., Martinez-Delgado B., Urioste M., Cigudosa J.C. and Benitez J. (2003). Characterization of the A673 cell line (Ewing tumor) by molecular cytogenetic techniques. Cancer Genet. Cytogenet. 141, 138-142.
33. Matsunobu T., Tanaka K., Matsumoto Y., Nakatani F., Sakimura R., Hanada M., Li X., Oda Y., Naruse I., Hoshino H., Tsuneyoshi M., Miura H. and Iwamoto Y. (2004). The prognostic and therapeutic relevance of p27kip1 in Ewing's family tumors. Clin. Cancer Res. 10, 1003-1012.
34. May W.A., Lessnick S.L., Braun B.S., Klemsz M., Lewis B.C., Lunsford L.B., Hromas R. and Denny C.T. (1993). The Ewing's sarcoma EWS/FLI-1 fusion gene encodes a more potent transcriptional activator and is a more powerful transforming gene than FLI-1. Mol. Cell Biol. 13, 7393-7398.
35. Mizumoto Y., Kyo S., Ohno S., Hashimoto M., Nakamura M., Maida Y., Sakaguchi J., Takakura M., Inoue M. and Kiyono T. (2006). Creation of tumorigenic human endometrial epithelial cells with intact chromosomes by introducing defined genetic elements. Oncogene 25, 5673-5682.
36. Ozerdem U. (2006). Targeting pericytes diminishes neovascularization in orthotopic uveal melanoma in nerve/glial antigen 2 proteoglycan knockout mouse. Ophthalmic Res. 38, 251-254.
37. Riggi N., Cironi L., Provero P., Suva M. L., Kaloulis K., Garcia-Echeverria C., Hoffmann F., Trumpp A. and Stamenkovic I. (2005). Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res. 65, 11459-11468.
38. Riggi N., Suva M.-L., Suva D., Cironi L., Provero P., Tercier S., Joseph J.-M., Stehle J.-C., Baumer K., Kindler V. and Stamenovic I., (2008). EWS-FLI-1 expression triggers a Ewing's sarcoma initiation program in primary human mesenchymal stem cells. Cancer Res. 68, 2176-2185.
39. Roessner A., Voss B., Rauterberg J., Immenkamp M., and Grundmann E. (1982). Biologic characterization of human bone tumors. I. Ewing's sarcoma. A comparative electron and immunofluorescence microscopic study. J. Cancer Res. Clin. Oncol. 104, 171-180.
40. Rubio D., Garcia-Castro J., Martin M.C., de la Fuente R., Cigudosa J.C., Lloyd A.C. and Bernad A. (2005). Spontaneous human adult stem cell transformation. Cancer Res. 65, 3035-3039.
41. Schrock E., Veldman T., Padilla-Nash H., Ning Y., Spurbeck J., Jalal S., Shaffer L.G., Papenhausen P., Kozma C., Phelan M.C., Kjeldsen E., Schonberg S.A., O'Brien P., Biesecker L., du Manoir S. and Ried T. (1997). Spectral karyotyping refines cytogenetic diagnostics of constitutional chromosomal abnormalities. Hum. Genet. 101, 255-262.
42. Serakinci N., Guldberg P., Burns J.S., Abdallah B., Schrodder H., Jensen T. and Kassem M. (2004). Adult human mesenchymal stem cell as a target for neoplastic transformation. Oncogene 23, 5095-5098.
43. Simonsen J.L., Rosada C., Serakinci N., Justesen J., Stenderup K., Rattan S.I., Jensen T.G. and Kassem M. (2002). Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat. Biotechnol. 20, 592-596.
44. Smith R., Owen L.A., Trem D.J., Wong J.S., Whangbo J.S., Golub T.R. and Lessnick S.L. (2006). Expression profiling of EWS/FLI identifies NKX2.2 as a critical target gene in Ewing's sarcoma. Cancer Cell 9, 405-416.
45. Takahashi A., Higashino F., Aoyagi M., Yoshida K., Itoh M., Kyo S., Ohno T., Taira T., Ariga H., Nakajima K., Hatta M., Kobayashi M., Sano H., Kohgo T. and Shindoh M. (2003). EWS/ETS fusions activate telomerase in Ewing's tumors. Cancer Res. 63, 8338-8344.
46. Thies A., Mangold U., Moll I. and Schumacher U. (2001). PAS-positive loops and networks as a prognostic indicator in cutaneous malignant melanoma. J. Pathol. 195, 537-542.
47. Tirode F., Laud-Duval K., Prieur A., Delorme B., Charbord P. and Delattre O. (2007). Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11, 421-429.
48. Torchia E.C., Jaishankar S. and Baker S.J. (2003). Ewing tumor fusion proteins block the differentiation of pluripotent marrow stromal cells. Cancer Res. 63 3464-3468.
49. van der Schaft D.W. Hillen F., Pauwels P., Kirschmann D.A., Castermans K., Egbrink M.G. Tran M.G. Sciot R. Hauben E., Hogendoorn P.C. Delattre O., Maxwell P.H., Hendrix M.J. and Griffioen A.W. (2005). Tumor cell plasticity in Ewing sarcoma, an alternative circulatory system stimulated by hypoxia. Cancer Res. 65, 11520-11528.
50. Vermeulen P.B., Gasparini G., Fox S.B., Colpaert C., Marson L.P., Gion M., Belien J.A., de Waal R.M., Van Marck E., Magnani E., Weidner N., Harris A.L. and Dirix LY. (2002). Second international consensus on the methodology and criteria of evaluation of angiogenesis quantification in solid human tumours. Eur. J. Cancer 38, 1564-1579.
51. Wei G., Antonescu C.R., de Alava E., Leung D., Huvos A.G., Meyers P. A., Healey J.H. and Ladanyi M. (2000). Prognostic impact of INK4A deletion in Ewing sarcoma. Cancer 89, 793-799.
52. Weitz J., Antonescu C.R. and Brennan M.F. (2003). Localized extremity soft tissue sarcoma: improved knowledge with unchanged survival over time. J. Clin. Oncol. 21, 2719-2725.
53. West C.C., Brown N.J., Mangham D.C., Grimer R.J., and Reed M.W. (2005). Microvessel density does not predict outcome in high grade soft tissue sarcoma. Eur. J. Surg. Oncol. 31, 1198-1205.
54. Xu W., Qian H., Zhu W., Chen Y., Shao Q., Sun X., Hu J., Han C. and Zhang X. (2004). A novel tumor cell line cloned from mutated human embryonic bone marrow mesenchymal stem cells. Oncol. Rep. 12, 501-508.
55. Yunis J.J. (1976). High resolution of human chromosomes. Science 191, 1268-1270.
56. Zhang J., Hu S., Schofield D.E., Sorensen P.H. and Triche T.J. (2004). Selective usage of D-Type cyclins by Ewing's tumors and rhabdomyosarcomas. Cancer Res. 64, 6026-6034.