Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells

Cancer Letters

Volumn 299, Issue 2, 2010, Pages 150-160

  Zhong, Yong ^a   Guan, Kaopeng ^a   Guo, Sujuan ^a   Zhou, Chunxia ^a   Wang, Dongmei ^a   Ma, Wenbo ^a   Zhang, Youhui ^a   Li, Changling ^a   Zhang, Shuren ^a  

^a CANCER HOSPITAL   (China)

Author keywords

Cancer stem cells; Immune evasion; Immunological phenotype; Renal cell carcinoma; Tumor spheres

Indexed keywords

B7 ANTIGEN; BASIC FIBROBLAST GROWTH FACTOR; BETA ACTIN; BETA CATENIN; BMI1 PROTEIN; CD59 ANTIGEN; CD86 ANTIGEN; DECAY ACCELERATING FACTOR; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FAS ANTIGEN; FAS LIGAND; FLUOROURACIL; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE COFACTOR PROTEIN; MESSENGER RNA; MITOMYCIN C; NATURAL KILLER CELL RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NANOG;

ADHERENT CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL CULTURE; CANCER STEM CELL; CARCINOGENICITY; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL GROWTH; CELL PROLIFERATION; CELL RENEWAL; CELL SUBPOPULATION; CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; TUMOR GROWTH;

ANIMALS; ANTIGENS, CD; ANTIMETABOLITES, ANTINEOPLASTIC; CARCINOMA, RENAL CELL; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FLOW CYTOMETRY; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPHENOTYPING; KIDNEY NEOPLASMS; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS;

EID: 78049279685     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.08.013     Document Type: Article

References (54)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics. CA Can. J. Clin. 2009, 59:225-249.
2. Costa L.J., Drabkin H.A. Renal cell carcinoma: new developments in molecular biology and potential for targeted therapies. Oncologist 2007, 12:1404-1415.
3. Flanigan R.C., Campbell S.C., Clark J.I., Picken M.M. Metastatic renal cell carcinoma. Curr. Treat. Options Oncol. 2003, 4:385-390.
4. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:3983-3988.
5. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Can. Res. 2003, 63:5821-5828.
6. Addla S.K., Brown M.D., Hart C.A., Ramani V.A., Clarke N.W. Characterization of the Hoechst 33342 side population from normal and malignant human renal epithelial cells. Am. J. Physiol. Renal Physiol. 2008, 295:F680-F687.
7. Bussolati B., Bruno S., Grange C., Ferrando U., Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 2008, 22:3696-3705.
8. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
9. Ponti D., Costa A., Zaffaroni N., Pratesi G., Petrangolini G., Coradini D., Pilotti S., Pierotti M.A., Daidone M.G. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Can. Res. 2005, 65:5506-5511.
10. Cariati M., Naderi A., Brown J.P., Smalley M.J., Pinder S.E., Caldas C., Purushotham A.D. Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. Int. J. Can. 2008, 122:298-304.
11. Yu S.C., Ping Y.F., Yi L., Zhou Z.H., Chen J.H., Yao X.H., Gao L., Wang J.M., Bian X.W. Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Can. Lett. 2008, 265:124-134.
12. Fang D., Nguyen T.K., Leishear K., Finko R., Kulp A.N., Hotz S., Van Belle P.A., Xu X., Elder D.E., Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Can. Res. 2005, 65:9328-9337.
13. Eramo A., Lotti F., Sette G., Pilozzi E., Biffoni M., Di Virgilio A., Conticello C., Ruco L., Peschle C., De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008, 15:504-514.
14. Gibbs C.P., Kukekov V.G., Reith J.D., Tchigrinova O., Suslov O.N., Scott E.W., Ghivizzani S.C., Ignatova T.N., Steindler D.A. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 2005, 7:967-976.
15. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., Kornblum H.I., Liu X., Wu H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 2001, 294:2186-2189.
16. Zhong Y., Zhou C., Ma W., Wang D., Guo S., Su X., Zhang S. Most MCF7 and SK-OV3 cells were deprived of their stem nature by Hoechst 33342. Biochem. Biophys. Res. Commun. 2007, 364:338-343.
17. Ghods A.J., Irvin D., Liu G., Yuan X., Abdulkadir I.R., Tunici P., Konda B., Wachsmann-Hogiu S., Black K.L., Yu J.S. Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem Cells 2007, 25:1645-1653.
18. Ho M.M., Ng A.V., Lam S., Hung J.Y. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Can. Res. 2007, 67:4827-4833.
19. Wu C., Wei Q., Utomo V., Nadesan P., Whetstone H., Kandel R., Wunder J.S., Alman B.A. Side population cells isolated from mesenchymal neoplasms have tumor initiating potential. Can. Res. 2007, 67:8216-8322.
20. Sagrinati C., Netti G.S., Mazzinghi B., Lazzeri E., Liotta F., Frosali F., Ronconi E., Meini C., Gacci M., Squecco R., Carini M., Gesualdo L., Francini F., Maggi E., Annunziato F., Lasagni L., Serio M., Romagnani S., Romagnani P. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J. Am. Soc. Nephrol. 2006, 17:2443-2456.
21. Patrawala L., Calhoun T., Schneider-Broussard R., Li H., Bhatia B., Tang S., Reilly J.G., Chandra D., Zhou J., Claypool K., Coghlan L., Tang D.G. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006, 25:1696-1708.
22. Seliger B., Rongcun Y., Atkins D., Hammers S., Huber C., Storkel S., Kiessling R. HER-2/neu is expressed in human renal cell carcinoma at heterogeneous levels independently of tumor grading and staging and can be recognized by HLA-A2.1-restricted cytotoxic T lymphocytes. Int. J. Can. 2000, 87:349-359.
23. Fan Y., Liu Z., Fang X., Ge Z., Ge N., Jia Y., Sun P., Lou F., Bjorkholm M., Gruber A., Ekman P., Xu D. Differential expression of full-length telomerase reverse transcriptase mRNA and telomerase activity between normal and malignant renal tissues. Clin. Can. Res. 2005, 11:4331-4337.
24. Schatton T., Schutte U., Frank N.Y., Zhan Q., Hoerning A., Robles S.C., Zhou J., Hodi F.S., Spagnoli G.C., Murphy G.F., Frank M.H. Modulation of T-cell activation by malignant melanoma initiating cells. Can. Res. 2010, 70:697-708.
25. Kawasaki B.T., Farrar W.L. Cancer stem cells, CD200 and immunoevasion. Trends Immunol. 2008, 29:464-468.
26. Kawasaki B.T., Mistree T., Hurt E.M., Kalathur M., Farrar W.L. Co-expression of the toleragenic, glycoprotein, CD200, with markers for cancer stem cells. Biochem. Biophys. Res. Commun. 2007, 364:778-782.
27. Zou W., Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat. Rev. Immunol. 2008, 8:467-477.
28. Rabinovich G.A., Gabrilovich D., Sotomayor E.M. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 2007, 25:267-296.
29. Ebert L.M., Tan B.S., Browning J., Svobodova S., Russell S.E., Kirkpatrick N., Gedye C., Moss D., Ng S.P., MacGregor D., Davis I.D., Cebon J., Chen W. The regulatory T cell-associated transcription factor FoxP3 is expressed by tumor cells. Can. Res. 2008, 68:3001-3009.
30. Hinz S., Pagerols-Raluy L., Oberg H.H., Ammerpohl O., Grussel S., Sipos B., Grutzmann R., Pilarsky C., Ungefroren H., Saeger H.D., Kloppel G., Kabelitz D., Kalthoff H. Foxp3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer. Can. Res. 2007, 67:8344-8350.
31. Kohga K., Tatsumi T., Takehara T., Tsunematsu H., Shimizu S., Yamamoto M., Sasakawa A., Miyagi T., Hayashi N. Expression of CD133 confers malignant potential by regulating metalloproteinases in human hepatocellular carcinoma. J. Hepatol. 2010, 52:872-879.
32. Di Tomaso T., Mazzoleni S., Wang E., Sovena G., Clavenna D., Franzin A., Mortini P., Ferrone S., Doglioni C., Marincola F.M., Galli R., Parmiani G., Maccalli C. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin. Can. Res. 2010, 16:800-813.
33. Fishelson Z., Donin N., Zell S., Schultz S., Kirschfink M. Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol. Immunol. 2003, 40:109-123.
34. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., Wahl G.M. Cancer stem cells - perspectives on current status and future directions: AACR workshop on cancer stem cells. Can. Res. 2006, 66:9339-9344.
35. Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: models and concepts. Annu. Rev. Med. 2007, 58:267-284.
36. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat. Rev. Can. 2005, 5:275-284.
37. Chambers I., Smith A. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 2004, 23:7150-7160.
38. Hurt E.M., Kawasaki B.T., Klarmann G.J., Thomas S.B., Farrar W.L. CD44+ CD24(-) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br. J. Can. 2008, 98:756-765.
39. Valk-Lingbeek M.E., Bruggeman S.W., van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell 2004, 118:409-418.
40. Shiina H., Igawa M., Breault J., Ribeiro-Filho L., Pookot D., Urakami S., Terashima M., Deguchi M., Yamanaka M., Shirai M., Kaneuchi M., Kane C.J., Dahiya R. The human T-cell factor-4 gene splicing isoforms Wnt signal pathway, and apoptosis in renal cell carcinoma. Clin. Can. Res. 2003, 9:2121-2132.
41. Guo W., Lasky J.L., Chang C.J., Mosessian S., Lewis X., Xiao Y., Yeh J.E., Chen J.Y., Iruela-Arispe M.L., Varella-Garcia M., Wu H. Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature 2008, 453:529-533.
42. Malanchi I., Peinado H., Kassen D., Hussenet T., Metzger D., Chambon P., Huber M., Hohl D., Cano A., Birchmeier W., Huelsken J. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008, 452:650-653.
43. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
44. Gu G., Yuan J., Wills M., Kasper S. Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo. Can. Res. 2007, 67:4807-4815.
45. Wei J., Barr J., Kong L.Y., Wang Y., Wu A., Sharma A.K., Gumin J., Henry V., Colman H., Priebe W., Sawaya R., Lang F.F., Heimberger A.B. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway. Mol. Can. Ther. 2010, 9:67-78.
46. Khong H.T., Restifo N.P. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 2002, 3:999-1005.
47. Martin F., Ladoire S., Mignot G., Apetoh L., Ghiringhelli F. Human FOXP3 and cancer. Oncogene 2010.
48. Cerwenka A., Lanier L.L. Natural killer cells viruses and cancer. Nat. Rev. Immunol. 2001, 1:41-49.
49. Bottino C., Castriconi R., Moretta L., Moretta A. Cellular ligands of activating NK receptors. Trends Immunol. 2005, 26:221-226.
50. El-Sherbiny Y.M., Meade J.L., Holmes T.D., McGonagle D., Mackie S.L., Morgan A.W., Cook G., Feyler S., Richards S.J., Davies F.E., Morgan G.J., Cook G.P. The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Can. Res. 2007, 67:8444-8449.
51. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 2005, 5:201-214.
52. Castriconi R., Daga A., Dondero A., Zona G., Poliani P.L., Melotti A., Griffero F., Marubbi D., Spaziante R., Bellora F., Moretta L., Moretta A., Corte G., Bottino C. NK cells recognize and kill human glioblastoma cells with stem cell-like properties. J. Immunol. 2009, 182:3530-3539.
53. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 2003, 3:781-790.
54. Maccalli C., Nonaka D., Piris A., Pende D., Rivoltini L., Castelli C., Parmiani G. NKG2D-mediated antitumor activity by tumor-infiltrating lymphocytes and antigen-specific T-cell clones isolated from melanoma patients. Clin. Can. Res. 2007, 13:7459-7468.