Identification and expansion of human osteosarcoma-cancer-stem cells by long-term 3-aminobenzamide treatment

Journal of Cellular Physiology

Volumn 219, Issue 2, 2009, Pages 301-313

  Di Fiore, Riccardo ^a   Santulli, Andrea ^a,b   Drago Ferrante, Rosa ^a   Giuliano, Michela ^a   De Blasio, Anna ^a   Messina, Concetta ^a,b   Pirozzi, Giuseppe ^c   Tirino, Virginia ^c   Tesoriere, Giovanni ^a   Vento, Renza ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b Erice Casa Santa   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOBENZAMIDE; ABC TRANSPORTER; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; FLICE INHIBITORY PROTEIN; HOE 33342; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN BCL 2; RHODAMINE 123; SURVIVIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR NUCLEOSTEMIN; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; 3-AMINOBENZAMIDE; BENZAMIDE DERIVATIVE; BENZIMIDAZOLE DERIVATIVE; BIOLOGICAL MARKER; CALCIUM CHANNEL BLOCKING AGENT; ENZYME INHIBITOR; FLUORESCENT DYE; VERAPAMIL;

APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL SHAPE; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; LONG TERM CARE; MULTIDRUG RESISTANCE; OSTEOBLAST; OSTEOSARCOMA; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINDLE CELL; ADOLESCENT; ADULT; CHILD; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

INTRACISTERNAL A-PARTICLES;

ADOLESCENT; ADULT; APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; BENZAMIDES; BENZIMIDAZOLES; BIOLOGICAL MARKERS; CALCIUM CHANNEL BLOCKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SHAPE; CHILD; DRUG RESISTANCE, MULTIPLE; ENZYME INHIBITORS; FLUORESCENT DYES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASTIC STEM CELLS; OSTEOSARCOMA; RHODAMINE 123; VERAPAMIL; YOUNG ADULT;

EID: 62149151311     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21667     Document Type: Article

References (67)

1. Abbott BL. 2003. ABCG2 (BCRP) expression in normal and malignant hematopoietic cells. Hematol Oncol 21:115-130.
2. Ahmed F, Arseni N, Glimm H, Hiddemann W, Buske C, Feuring-Buske M. 2008. Constitutive expression of the ATP-binding cassette transporter ABCG2 enhances the growth potential of early human hematopoietic progenitors. Stem Cells 26:810-818.
3. Ailles LE, Weissman IL. 2007. Cancer stem cells in solid tumors. Curr Opin Biotechnol 18:460-466.
4. Al-Hajj M, Clarke MF. 2004. Self-renewal and solid tumor stem cells. Oncogene 23:7274-7282.
5. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. 2003. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci 100:3983-3988.
6. Baguley BC. 2006. Tumor stem cell niches: A new functional framework for the action of anticancer drugs. Recent Patents Anticancer Drug Discov 1:121-127.
7. Bart J, Hollema H, Groen HJ, de Vries EG, Hendrikse NH, Sleijfer DT, Wegman TD, Vaalburg W, van derGraaf WT. 2004. The distribution of drug-efflux pumps, P-gp, BCRP, MRP1 and MRP2, in the normal blood-testis barrier and in primary testicular tumours. Eur J Cancer 40:2064-2070.
8. Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J, Terzis AJA. 2005. The origin of the cancer stem cell: Current controversies and new insights. Nat Rev Cancer 5:899-904.
9. Bunting KD. 2002. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20:11-20.
10. Burns JS, Abdallah BM, Guldberg P, Rygaard J, Schrøder HD, 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.
11. Challen GA, Little MH. 2006. A side order of stemcells: The Sp phenotype. Stem Cells 24:3-12.
12. Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, Miyoshi H, Nakano M, Zen Y, Nakanuma Y, Nakauchi H, Iwama A, Taniguchi H. 2007. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology 133:937-950.
13. Choi CH. 2005. ABC transporters as multidrug resistance mechanisms and the development of chemosensitizers for their reversal. Cancer Cell Int 5:30.
14. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. 2006. Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res 66:9339-9344.
15. Dalerba P, Cho RW, Clarke MF. 2007. Cancer stem cells: Models and concepts. Annu Rev Med 58:267-284.
16. Darr H, Mayshar Y, Benvenisty N. 2006. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 133:1193-1201.
17. De Blasio A, Musmeci MT, Giuliano M, Lauricella M, Emanuele S, D'Anneo A, Vassallo B, Tesoriere G, Vento R. 2003. The effect of 3-aminobenzamide, inhibitor of poly(ADP-ribose) polymerase, on human osteosarcoma cells. Int J Oncol 23:1521-1528.
18. De Blasio A, Messina C, Santulli A, Mangano V, Di Leonardo E, D'Anneo A, Tesoriere G, Vento R. 2005. Differentiative pathway activated by 3-aminobenzamide, an inhibitor of PARP, in human osteosarcoma MG-63 cells. FEBS Lett 579:615-620.
19. De Paiva CS, Pflugfelder SC, Li DQ. 2006. Cell size correlates with phenotype and proliferative capacity in human corneal epithelial cells. Stem Cells 24:368-375.
20. Dean M, Fojo T, Bates S. 2005. Tumour stem cells and drug resistance. Nat Rev Cancer 5:275-284.
21. Deshpande A, Sicinski P, Hinds PW. 2005. Cyclins and cdks in development and cancer: A perspective. Oncogene 24:2909-2915.
22. Doyle LA, Ross DD. 2003. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 22:7340-7358.
23. Gibbs PC, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, Steindler DA. 2005. Stem-like cells in bone sarcomas: Implications for tumorigenesis. Neoplasia 7:967-976.
24. Graziano A, D'Aquino R, Tirino V, Desiderio V, Rossi A, Pirozzi G. 2008. The stem cell hypothesis in head and neck cancer. J Cell Biochem 103:408-412.
25. Hadnagy A, Gabouryb L, Beaulieua R, Balickia D. 2006. SP analysis may be used to identify cancer stem cell populations. Exp Cell Res 312:3701-3710.
26. Hartmann C. 2006. A Wnt canon orchestrating osteoblastogenesis. Trends Cell Biol 16:151-159.
27. Herrera RE, Sah VP, Williams BO, MaKela TP, Weinberg RA, Jacks T. 1996. Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol Cell Biol 16:2402-2407.
28. Hoang BH, Kubo T, Healey JH, Yang R, Nathan SS, Kolb EA, Mazza BA, Meyers PA, Gorlick R. 2004. Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-β-catenin pathway. Cancer Res 64:2734-2739.
29. Hoei-Hansen CE, Sehested A, Juhler M, Lau YF, Skakkebaek NE, Laursen H, Rajpert-de Meyts E. 2006. New evidence for the origin of intracranial germ cell tumours from primordial germ cells: Expression of pluripotency and cell differentiationmarkers. J Pathol 209:25-33.
30. Ieiri I, Takane H, Otsubo K. 2004. The MDR1 (ABCB1) gene polymorphism and its clinical implications. Clin Pharmacokinet 43:553-576.
31. Immervoll H, Hoem D, Sakariassen PØ, Steffensen OJ, Molven A. 2008. Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 8:48.
32. Jordan CT, Guzman ML, Noble M. 2006. Cancer stem cells. N Engl J Med 355:1253-1261.
33. Kawabata S, Oka M, Soda H, Shiozawa K, Nakatomi K, Tsurutani J, Nakamura Y, Doi S, Kitazaki T, Sugahara K, Yamada Y, Kamihira S, Kohno S. 2003. Expression and functional analyses of breast cancer resistance protein in lung cancer. Clin Cancer Res 9:3052-3057.
34. Lauricella M, Emanuele S, D'Anneo A, Calvaruso G, Vassallo B, Carlisi D, Portanova P, Vento R, Tesoriere G. 2006. JNK and AP-1 mediate apoptosis induced by bortezomib in HepG2 cells via FasL/caspase-8 and mitochondria-dependent pathways. Apoptosis 11:607-625.
35. Li L, Neaves WB. 2006. Normal stem cells and cancer stem cells: The niche matters. Cancer Res 66:4553-4557.
36. Lin TH, Yang RS, Tang CH, Lin CP, Fu WM. 2007. PPARγ inhibits osteogenesis via the downregulation of the expression of COX-2 and iNOS in rats. Bone 41:562-574.
37. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. 2006. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67.
38. Liu Y, Bhat RA, Seestaller-Wehr LM, Fukayama S, Mangine A, Moran RA, Komm BS, Bodine PV, Billiard J. 2007. The orphan receptor tyrosine kinase Ror2 promotes osteoblast differentiation and enhances ex vivo bone formation. Mol Endocrinol 21:376-387.
39. Maitland NJ, Collins AT. 2008. Prostate cancer stem cells: A new target for therapy. J Clin Oncol 26:2862-2870.
40. Marina N, Gerbhardt M, Teot L, Gorlick R. 2004. Biology and therapeutic advances for pediatric osteosarcoma. Oncologist 9:422-441.
41. Mizrak D, Brittan M, Alison MR. 2008. CD133: Molecule of the moment. J Pathol 214:3-9.
42. Molofsky AV, Pardal R, Morrison J. 2004. Diverse mechanisms regulate stem cell self-renewal. Curr Opin Cell Biol 16:700-707.
43. Nadri S, Soleimani M, Kiani J, Atashi A, Izadpanah R. 2008. Multipotent mesenchymal stem cells from adult human eye conjunctiva stromal cells. Differentiation 76:223-231.
44. Neuzil J, Stantic M, Zobalova R, Chladova J, Wang X, Prochazka L, Dong L, Andera L, Ralph SJ. 2007. Tumour-initiating cells vs. cancer 'stem' cells and CD133: What's in the name? Biochem Biophys Res Commun 355:855-859.
45. O'Brien CA, Pollett A, Gallinger S, Dick JE. 2007. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106-110.
46. Pan G, Thomson JA. 2007. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res 17:42-49.
47. Park BW, Hah YS, Kim DR, Kim JR, Byun JH. 2007. Osteogenic phenotypes and mineralization of cultured human periosteal-derived cells. Arch Oral Biol 52:983-989.
48. Picci P. 2007. Osteosarcoma (osteogenic sarcoma). Orphanet J Rare Dis 23:2-6.
49. Reger RL, Tucker AH, Wolfe MR. 2008. Differentiation and characterization of human MSCs. Methods Mol Biol 449:93-107.
50. Reya T, Morrison SJ, Clarke F, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105-111.
51. Robey RW, Shukla S, Finley EM, Oldham RK, Barnett D, Ambudkarb SV, Fojo T, Bates SE. 2008. Inhibition of P-glycoprotein (ABCB1)- and multidrug resistance-associated protein 1 (ABCC1)-mediated transport by the orally administered inhibitor, CBT-1W. Biochem Pharmacol 75:1302-1312.
52. Salasznyk RM, Klees RF, Williams WA, Boskey A, Plopper GE. 2007. Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp Cell Res 313:22-37.
53. Schaffer D. 2007. Exploring and engineering stem cells and their niches. Curr Opin Chem Biol 11:355-356.
54. Schreiber E, Matthias P, Muller M, Schaffner W. 1989. Rapid detection of DNA binding proteins with mini-extracts prepared from a small number of cells. Nucleic Acid Res 17:6419-6424.
55. Semenza GL. 2007. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov Today 12:853-859.
56. Shiratsuchi H, Nakashima T, Hirakawa N, Toh S, Nakagawa T, Saito T, Tsuneyoshi M, Komune S. 2007. beta-Catenin nuclear accumulation in head and neck mucoepidermoid carcinoma: Its role in cyclin D1 overexpression and tumor progression. Head Neck 29:577-584.
57. Shmelkov SV, St. Clair R, Lyden D, Rafii S. 2005. Molecules in focus: AC133/CD133/Prominin-1. Int J Biochem Cell Biol 37:715-719.
58. Simon MC, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9:285-296.
59. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. 2004. Identification of human brain tumour initiating cells. Nature 432:396-401.
60. Spangler JG. 2008. Bone biology and physiology: Implications for novel osteoblastic osteosarcoma treatments? Med Hypotheses 70:281-286.
61. Stark GR, Taylor WR. 2006. Control of the G2/M transition. Mol Biotechnol 32:227-248.
62. Tang N, Song WX, Luo J, Haydon RC, He TC. 2008. Osteosarcoma development and stem cell differentiation. Clin Orthop Relat Res 466:2114-2130.
63. Wang JC, Dick JE. 2005. Cancer stem cells: Lessons from leukemia. Trends Cell Biol 15:494-501.
64. Yanagisawa M, Suzuki N, Mitsui N, Koyama Y, Otsuka K, Shimizu N. 2007. Effects of compressive force on the differentiation of pluripotent mesenchymal cells. Life Sci 81:405-412.
65. Yang YM, Chang JW. 2008. Current status and issues in cancer stem cell study. Cancer Invest 26:741-755.
66. Ye F, Zhou C, Cheng Q, Shen J, Chen H. 2008. Stem-cell-abundant proteins Nanog, Nucleostemin and Musashi1 are highly expressed in malignant cervical epithelial cells.BMC Cancer 8:108-113.
67. Zou GM. 2008. Cancer initiating cells or cancer stem cells in the gastrointestinal tract and liver. J Cell Physiol 217:598-604. Review.