Conversion of differentiated cancer cells into cancer stem-like cells in a glioblastoma model after primary chemotherapy

Cell Death and Differentiation

Volumn 21, Issue 7, 2014, Pages 1119-1131

  Auffinger, B ^a   Tobias, A L ^a   Han, Y ^a   Lee, G ^a   Guo, D ^a   Dey, M ^a   Lesniak, M S ^a   Ahmed, A U ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; CELL MARKER; HYPOXIA INDUCIBLE FACTOR; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SOX2; ALKYLATING AGENT; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DACARBAZINE; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CANCER TRANSPLANTATION; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; GLIOMA CELL; GLIOMA CELL LINE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL EXPANSION; TUMOR MODEL; TUMOR RECURRENCE; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN NEOPLASMS; CELL TRANSFORMATION; DRUG EFFECTS; DRUG SCREENING; MALE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DACARBAZINE; GLIOBLASTOMA; HUMANS; MALE; MICE, NUDE; NEOPLASTIC STEM CELLS; PHENOTYPE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902269863     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.31     Document Type: Article

References (45)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-996.
2. Hau P, Koch D, Hundsberger T, Marg E, Bauer B, Rudolph R et al. Safety and feasibility of long-term temozolomide treatment in patients with high-grade glioma. Neurology 2007; 68: 688-690.
3. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488: 522-526.
4. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009; 4: 226-235.
5. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol cancer 2011; 10: 128.
6. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 2008; 14: 123-129.
7. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
8. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006; 13: 1238-1241.
9. Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 2008; 68: 5706-5715.
10. Rosso L, Brock CS, Gallo JM, Saleem A, Price PM, Turkheimer FE et al. A new model for prediction of drug distribution in tumor and normal tissues: pharmacokinetics of temozolomide in glioma patients. Cancer Res 2009; 69: 120-127.
11. Brada M, Judson I, Beale P, Moore S, Reidenberg P, Statkevich P et al. Phase I doseescalation and pharmacokinetic study of temozolomide (SCH 52365) for refractory or relapsing malignancies. Br J Cancer 1999; 81: 1022-1030.
12. Ostermann S, Csajka C, Buclin T, Leyvraz S, Lejeune F, Decosterd LA et al. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res 2004; 10: 3728-3736.
13. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
14. Shackleton M, Quintana E, Fearon ER, Morrison SJ. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009; 138: 822-829.
15. Son MJ, Woolard K, Nam DH, Lee J, Fine HA. SSEA-1 is an enrichment marker for tumorinitiating cells in human glioblastoma. Cell Stem Cell 2009; 4: 440-452.
16. Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009; 8: 3274-3284.
17. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci USA 2011; 108: 7950-7955.
18. Sugiarto S, Persson AI, Munoz EG, Waldhuber M, Lamagna C, Andor N et al. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell 2011; 20: 328-340.
19. Enderling H, Hlatky L, Hahnfeldt P. Cancer stem cells: a minor cancer subpopulation that redefines global cancer features. Front Oncol 2013; 3: 76.
20. Lathia JD, Hitomi M, Gallagher J, Gadani SP, Adkins J, Vasanji A et al. Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death Dis 2011; 2: e200.
21. Apostolou P, Toloudi M, Ioannou E, Chatziioannou M, Kourtidou E, Vlachou I et al. AP-1 gene expression levels may be correlated with changes in gene expression of some stemness factors in colon carcinomas. J Signal Transduction 2013; 2013: 497383.
22. Ligon KL, Huillard E, Mehta S, Kesari S, Liu H, Alberta JA et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007; 53: 503-517.
23. Motoda L, Osato M, Yamashita N, Jacob B, Chen LQ, Yanagida M et al. Runx1 protects hematopoietic stem/progenitor cells from oncogenic insult. Stem Cells 2007; 25: 2976-2986.
24. Miyazono K, Ehata S, Koinuma D. Tumor-promoting functions of transforming growth factor-beta in progression of cancer. Upsala J Med Sci 2012; 117: 143-152.
25. Qiu B, Zhang D, Tao J, Tie X, Wu A, Wang Y. Human brain glioma stem cells are more invasive than their differentiated progeny cells in vitro. J Clin Neurosci 2012; 19: 130-134.
26. Wakimoto H, Kesari S, Farrell CJ, Curry Jr WT, Zaupa C, Aghi M et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 2009; 69: 3472-3481.
27. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15: 501-513.
28. Seidel S, Garvalov BK, Wirta V, von Stechow L, Schanzer A, Meletis K et al. A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 2010; 133(Pt 4): 983-995.
29. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
30. Riganti C, Salaroglio IC, Caldera V, Campia I, Kopecka J, Mellai M et al. Temozolomide downregulates P-glycoprotein expression in glioblastoma stem cells by interfering with the Wnt3a/ glycogen synthase-3 kinase/beta-catenin pathway. Neuro-oncology 2013; 15: 1502-1517.
31. Persano L, Pistollato F, Rampazzo E, Della Puppa A, Abbadi S, Frasson C et al. BMP2 sensitizes glioblastoma stem-like cells to Temozolomide by affecting HIF-1alpha stability and MGMT expression. Cell Death Dis 2012; 3: e412.
32. Zhu H, Wang D, Liu Y, Su Z, Zhang L, Chen F et al. Role of the Hypoxia-inducible factor-1 alpha induced autophagy in the conversion of non-stem pancreatic cancer cells into CD133+ pancreatic cancer stem-like cells. Cancer Cell Int 2013; 13: 119.
33. Ahmed AU, Auffinger B, Lesniak MS. Understanding glioma stem cells: rationale, clinical relevance and therapeutic strategies. Exp Rev Neurother 2013; 13: 545-555.
34. Hjelmeland AB, Wu Q, Heddleston JM, Choudhary GS, MacSwords J, Lathia JD et al. Acidic stress promotes a glioma stem cell phenotype. Cell Death Differ 2011; 18: 829-840.
35. Menendez JA, Joven J, Cufi S, Corominas-Faja B, Oliveras-Ferraros C, Cuyas E et al. The Warburg effect version 2.0: metabolic reprogramming of cancer stem cells. Cell Cycle 2013; 12: 1166-1179.
36. Vazquez-Martin A, Oliveras-Ferraros C, Cufi S, Del Barco S, Martin-Castillo B, Menendez JA. Metformin regulates breast cancer stem cell ontogeny by transcriptional regulation of the epithelial-mesenchymal transition (EMT) status. Cell Cycle 2010; 9: 3807-3814.
37. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415-421.
38. Tomita-Mitchell A, Kat AG, Marcelino LA, Li-Sucholeiki XC, Goodluck-Griffith J, Thilly WG. Mismatch repair deficient human cells: spontaneous and MNNG-induced mutational spectra in the HPRT gene. Mut Res 2000; 450: 125-138.
39. Kitange GJ, Carlson BL, Mladek AC, Decker PA, Schroeder MA, Wu W et al. Evaluation of MGMT promoter methylation status and correlation with temozolomide response in orthotopic glioblastoma xenograft model. J Neuro-oncol 2009; 92: 23-31.
40. Kitange GJ, Carlson BL, Schroeder MA, Grogan PT, Lamont JD, Decker PA et al. Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro-oncology 2009; 11: 281-291.
41. Prasad G, Sottero T, Yang X, Mueller S, James CD, Weiss WA et al. Inhibition of PI3K/mTOR pathways in glioblastoma and implications for combination therapy with temozolomide. Neuro-oncology 2011; 13: 384-392.
42. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
43. Tyler MA, Ulasov IV, Sonabend AM, Nandi S, Han Y, Marler S et al. Neural stem cells target intracranial glioma to deliver an oncolytic adenovirus in vivo. Gene Ther 2009; 16: 262-278.
44. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008; 22: 659-661.
45. Tobias AL, Thaci B, Auffinger B, Rincon E, Balyasnikova IV, Kim CK et al. The timing of neural stem cell-based virotherapy is critical for optimal therapeutic efficacy when applied with radiation and chemotherapy for the treatment of glioblastoma. Stem Cells Transl Med 2013; 2: 655-666.