Sphere-forming cell subsets with cancer stem cell properties in human musculoskeletal sarcomas

International Journal of Oncology

Volumn 43, Issue 1, 2013, Pages 95-102

  Salerno, Manuela ^a,b   Avnet, Sofia ^a   Bonuccelli, Gloria ^a,b   Eramo, Adriana ^c   De Maria, Ruggero ^d   Gambarotti, Marco ^a   Gamberi, Gabriella ^a   Baldini, Nicola ^a,b  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Cancer stem cells; Hypoxia; Sarcoma; Sarcosphere

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER STEM CELL; CHILD; CHONDROSARCOMA; CLINICAL ARTICLE; EMBRYONIC STEM CELL; EWING SARCOMA; FEMALE; HUMAN; LIPOSARCOMA; MALE; OSTEOSARCOMA; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHABDOMYOSARCOMA; SARCOMA; SCHOOL CHILD; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CHILD; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MIDDLE AGED; MUSCLE, SKELETAL; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; SARCOMA; SOXB1 TRANSCRIPTION FACTORS; SPHEROIDS, CELLULAR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84879659043     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1927     Document Type: Article

References (44)

1. Luis ÁM, Aguilar DP and Martín JA: Multidisciplinary management of soft tissue sarcomas. Clin Transl Oncol 12: 543-553, 2010.
2. Burningham Z, Hashibe M, Spector L and Schiffman JD: The epidemiology of sarcoma. Clin Sarcoma Res 2: 13-16, 2012.
3. Keedy VL: Treating metastatic soft-tissue or bone sarcomas - potential role of ridaforolimus. Onco Targets Ther 5: 153-160, 2012.
4. Lapidot T, Sirard C, Vormoor J, et al: A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 17: 645-648, 1994. (Pubitemid 24067706)
5. Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737, 1997. (Pubitemid 27298715)
6. Reya T, Morrison SJ, Clarke MF and Weissman IL: Stem cells, cancer, and cancer stem cells. Nature 414: 105-111, 2001. (Pubitemid 33041634)
7. Jordan CT, Guzman ML and Noble M: Cancer stem cells. N Engl J Med 355: 1253-1261, 2006. (Pubitemid 44427449)
8. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003. (Pubitemid 36418143)
9. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB: Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828, 2003. (Pubitemid 37187480)
10. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C and De Maria R: Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115, 2007. (Pubitemid 46067311)
11. Li C, Heidt DG, Dalerba P, et al: Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037, 2007.
12. Schatton T, Murphy GF, Frank, NY, et al: Identification of cells initiating human melanomas. Nature 451: 345-349, 2008.
13. Zhang S, Balch C, Chan MW, et al: Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68: 4311-4320, 2008.
14. Lang Sh, Frame F and Collins A: Prostate cancer stem cells. J Pathol 217: 299-306, 2009.
15. Ponti D, Costa A, Zaffaroni N, et al: Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511, 2005. (Pubitemid 40911148)
16. Deleyrolle LP, Ericksson G, Morrison BJ, et al: Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS One 6: e15844, 2011.
17. Liu T, Cheng W, Lai D, Huang Y and Guo L: Characterization of primary ovarian cancer cells in different culture systems. Oncol Rep 23: 1277-1284, 2010.
18. Gibbs CP, Kukekov VG, Reith JD, et al: Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 7: 967-976, 2005.
19. Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K and Takakura Y: Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol 34: 1381-1386, 2009.
20. Wang L, Park P and Lin CY: Characterization of stem cell attributes in human osteosarcoma cell lines. Cancer Biol Ther 8: 543-552, 2009.
21. Rainusso N, Man TK, Lau CC, et al: Identification and gene expression profiling of tumor-initiating cells isolated from human osteosarcoma cell lines in an orthotopic mouse model. Cancer Biol Ther 12: 278-287, 2011.
22. Basu-Roy U, Seo E, Ramanathapuram L, et al: Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene 31: 2270-2282, 2012.
23. Suvà ML, Riggi N, Stehle JC, et al: Identification of cancer stem cells in Ewing's sarcoma. Cancer Res 69: 1776-1781, 2009.
24. Sette G, Salvati V, Memeo L, et al: EGFR inhibition abrogates leiomyosarcoma cell chemoresistance through inactivation of survival pathways and impairment of CSC potential. PLoS One 7: e46891, 2012.
25. Murase M, Kano M, Tsukahara T, et al: Side population cells have the characteristics of cancer stem-like cells/cancer-initiating cells in bone sarcomas. Br J Cancer 101: 1425-1432, 2009.
26. Lohberger B, Rinner B, Stuendl N, et al: Aldehyde dehydrogenase 1, a potential marker for cancer stem cells in human sarcoma. PLoS One 7: e43664, 2012.
27. Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB and Rich JN: Hypoxia inducible factors in cancer stem cells. Br J Cancer 102: 789-795, 2010.
28. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001. (Pubitemid 34164012)
29. Felipe Rico J, Hassane DC and Guzman ML: Acute myelogenous leukemia stem cells: from bench to bedside. Cancer Lett: Jun 17, 2012 (Epub ahead of print).
30. Reynolds BA and Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710, 1992.
31. Hallett RM, Kondratyev MK, Giacomelli AO, Nixon AM, Girgis-Gabardo A, Ilieva D and Hassell JA: Small molecule antagonists of the Wnt/β-catenin signaling pathway target breast tumor-initiating cells in a Her2/Neu mouse model of breast cancer. PLoS One 7: e33976, 2012.
32. Gibbs CP Jr, Levings PP and Ghivizzani SC: Evidence for the osteosarcoma stem cell. Curr Orthop Pract 22: 322-326, 2011.
33. Trucco M and Loeb D: Sarcoma stem cells: do we know what we are looking for? Sarcoma 2012: 291705: May 9, 2012 (Epub ahead of print). doi: 10.1155/2012/291705.
34. Galli R, Borello U, Gritti A, et al: Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci 3: 986-991, 2000.
35. Toguchida J and Nakayama T: Molecular genetics of sarcomas: applications to diagnoses and therapy. Cancer Sci 100: 1573-1580, 2009.
36. Tolar J, Nauta AJ, Osborn MJ, et al: Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25: 371-379, 2007. (Pubitemid 46232791)
37. Tirino V, Desiderio V, Paino F, et al: Human primary bone sarcomas contain CD133+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J 25: 2022-2030, 2011.
38. Jiang X, Gwye Y, Russell D, et al: CD133 expression in chemoresistant Ewing sarcoma cells. BMC Cancer 10: 116-127, 2012.
39. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M and Kornblum HI: Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100: 15178-15183, 2003. (Pubitemid 37518036)
40. Gupta PB, Chaffer CL and Weinberg RA: Cancer stem cells: mirage or reality? Nat Med 5: 1010-1012, 2009.
41. Mohyeldin A, Garzón-Muvdi T and Quiñones-Hinojosa A: Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7: 150-161, 2010.
42. Rosová I, Dao M, Capoccia B, Link D and Nolta JA: Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26: 2173-2182, 2008.
43. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K and Tofilon PJ: Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol Cancer Res 7: 489-497, 2009.
44. Okita K, Ichisaka T and Yamanaka S: Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317, 2008. Research