Understanding glioma stem cells: Rationale, clinical relevance and therapeutic strategies

Expert Review of Neurotherapeutics

Volumn 13, Issue 5, 2013, Pages 545-555

  Ahmed, Atique U ^a   Auffinger, Brenda ^a   Lesniak, Maciej S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

glioblastoma multiforme; glioma stem cells; intratumoral heterogeneity; markers; microenvironment; targeted therapies; therapeutic resistance

Indexed keywords

A2B5 PROTEIN; ADENOVIRUS VECTOR; ALPHA6 INTEGRIN; CD133 ANTIGEN; MEMBRANE ANTIGEN; MICRORNA; MOLECULAR MARKER; STAGE SPECIFIC EMBRYO ANTIGEN 1; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

CANCER PROGNOSIS; CANCER STEM CELL; CELL DIFFERENTIATION; CELL TYPE; DNA DAMAGE; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE TARGETING; GENE THERAPY; GLIOMA; HUMAN; IMMUNOREACTIVITY; IMMUNOTHERAPY; MALIGNANT TRANSFORMATION; NONHUMAN; ONCOLYTIC VIROTHERAPY; REVIEW; TUMOR MICROENVIRONMENT;

ANIMALS; BRAIN NEOPLASMS; CHEMORADIOTHERAPY; GLIOBLASTOMA; HUMANS; NEOPLASTIC STEM CELLS;

EID: 84876942581     PISSN: 14737175     EISSN: 17448360     Source Type: Journal    
DOI: 10.1586/ern.13.42     Document Type: Review

References (99)

1. Stupp R, Mason WP, van den Bent MJ et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352(10), 987-996 (2005)
2. Kang MK, Kang SK. Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem Cells Dev. 16(5), 837-847 (2007)
3. Liu G, Yuan X, Zeng Z et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 5, 67 (2006)
4. Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120), 756-760 (2006)
5. Polyak K, Hahn WC. Roots and stems: stem cells in cancer. Nat. Med. 12(3), 296-300 (2006)
6. Galli R, Binda E, Orfanelli U et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64(19), 7011-7021 (2004)
7. Dirks PB. Brain tumor stem cells: bringing order to the chaos of brain cancer. J. Clin. Oncol. 26(17), 2916-2924 (2008)
8. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat. Rev. Cancer 6(6), 425-436 (2006)
9. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8(10), 755-768 (2008)
10. Fuchs E, Segre JA. Stem cells: a new lease on life. Cell 100(1), 143-155 (2000)
11. Calabrese C, Poppleton H, Kocak M et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11(1), 69-82 (2007)
12. Visvader JE. Cells of origin in cancer. Nature 469(7330), 314-322 (2011)
13. Alcantara Llaguno S, Chen J, Kwon CH et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15(1), 45-56 (2009)
14. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet. 25(1), 55-57 (2000)
15. Jacques TS, Swales A, Brzozowski MJ et al. Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J. 29(1), 222-235 (2010)
16. Marumoto T, Tashiro A, Friedmann-Morvinski D et al. Development of a novel mouse glioma model using lentiviral vectors. Nat. Med. 15(1), 110-116 (2009)
17. Wang Y, Yang J, Zheng H et al. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell 15(6), 514-526 (2009)
18. Mani SA, Guo W, Liao MJ et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133(4), 704-715 (2008)
19. Chaffer CL, Brueckmann I, Scheel C et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc. Natl Acad. Sci. USA 108(19), 7950-7955 (2011)
20. Friedmann-Morvinski D, Bushong EA, Ke E et al. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338(6110), 1080-1084 (2012)
21. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat. Med. 15(9), 1010-1012 (2009)
22. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 317(5836), 337 (2007)
23. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3(7), 730-737 (1997)
24. Lapidot T, Sirard C, Vormoor J et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367(6464), 645-648 (1994)
25. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100(7), 3983-3988 (2003)
26. Hemmati HD, Nakano I, Lazareff JA et al. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl Acad. Sci. USA 100(25), 15178-15183 (2003)
27. Singh SK, Clarke ID, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63(18), 5821-5828 (2003)
28. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445(7123), 106-110 (2007)
29. Fang D, Nguyen TK, Leishear K et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65(20), 9328-9337 (2005)
30. Hermann PC, Huber SL, Herrler T et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1(3), 313-323 (2007)
31. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65(23), 10946-10951 (2005)
32. Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res. 65(8), 3025-3029 (2005)
33. Eramo A, Lotti F, Sette G et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 15(3), 504-514 (2008)
34. Fukuda K, Saikawa Y, Ohashi M et al. Tumor initiating potential of side population cells in human gastric cancer. Int. J. Oncol. 34(5), 1201-1207 (2009)
35. Beier D, Hau P, Proescholdt M et al. CD133(+) and CD133(-) glioblastomaderived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67(9), 4010-4015 (2007)
36. Ogden AT, Waziri AE, Lochhead RA et al. Identification of A2B5+CD133- tumorinitiating cells in adult human gliomas. Neurosurgery 62(2), 505-514; discussion
37. Son MJ, Woolard K, Nam DH, Lee J, Fine HA. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4(5), 440-452 (2009)
38. Sun Y, Liou B, Quinn B, Ran H, Xu YH, Grabowski GA. In vivo and ex vivo evaluation of L-type calcium channel blockers on acid beta-glucosidase in Gaucher disease mouse models. PLoS ONE 4(10), e7320 (2009)
39. Read TA, Fogarty MP, Markant SL et al. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 15(2), 135-147 (2009)
40. Lathia JD, Gallagher J, Heddleston JM et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 6(5), 421-432 (2010)
41. Shin HY, Hong YH, Jang SS et al. A role of canonical transient receptor potential 5 channel in neuronal differentiation from A2B5 neural progenitor cells. PLoS ONE 5(5), e10359 (2010)
42. Wu Y, Wu PY. CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev. 18(8), 1127-1134 (2009)
43. Alison MR, Lim SM, Nicholson LJ. Cancer stem cells: problems for therapy? J. Pathol. 223(2), 147-161 (2011)
44. Pece S, Tosoni D, Confalonieri S et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140(1), 62-73 (2010)
45. Laks DR, Masterman-Smith M, Visnyei K et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells 27(4), 980-987 (2009)
46. Zhang M, Song T, Yang L et al. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J. Exp. Clin. Cancer Res. 27, 85 (2008)
47. Zeppernick F, Ahmadi R, Campos B et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin. Cancer Res. 14(1), 123-129 (2008)
48. Sato A, Sakurada K, Kumabe T et al.; Tohoku Brain Tumor Study Group. Association of stem cell marker CD133 expression with dissemination of glioblastomas. Neurosurg. Rev. 33(2), 175-183; discussion 183 (2010)
49. Kim KJ, Lee KH, Kim HS et al. The presence of stem cell marker-expressing cells is not prognostically significant in glioblastomas. Neuropathology 31(5), 494-502 (2011)
50. Horst D, Kriegl L, Engel J, Kirchner T, Jung A. Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest. 27(8), 844-850 (2009)
51. Cheung AM, Wan TS, Leung JC et al. Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/SCID engrafting potential. Leukemia 21(7), 1423-1430 (2007)
52. Morimoto K, Kim SJ, Tanei T et al. Stem cell marker aldehyde dehydrogenase 1-positive breast cancers are characterized by negative estrogen receptor, positive human epidermal growth factor receptor type 2, and high Ki67 expression. Cancer Sci. 100(6), 1062-1068 (2009)
53. Rasheed ZA, Yang J, Wang Q et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J. Natl Cancer Inst. 102(5), 340-351 (2010)
54. Chen YC, Chen YW, Hsu HS et al. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem. Biophys. Res. Commun. 385(3), 307-313 (2009)
55. Rich JN, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell 1(4), 353-355 (2007)
56. Maynard S, Swistowska AM, Lee JW et al. Human embryonic stem cells have enhanced repair of multiple forms of DNA damage. Stem Cells 26(9), 2266-2274 (2008)
57. Smith J, Ladi E, Mayer-Proschel M, Noble M. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc. Natl Acad. Sci. USA 97(18), 10032-10037 (2000)
58. Ito K, Hirao A, Arai F et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431(7011), 997-1002 (2004)
59. Kitange GJ, Carlson BL, Schroeder MA et al. Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro-oncology 11(3), 281-291 (2009)
60. Blough MD, Westgate MR, Beauchamp D et al. Sensitivity to temozolomide in brain tumor initiating cells. Neuro-oncology 12(7), 756-760 (2010)
61. Hermisson M, Klumpp A, Wick W et al. O6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J. Neurochem. 96(3), 766-776 (2006)
62. Hegi ME, Diserens AC, Gorlia T et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352(10), 997-1003 (2005)
63. Sato A, Sunayama J, Matsuda K et al. MEK-ERK signaling dictates DNA-repair gene MGMT expression and temozolomide resistance of stem-like glioblastoma cells via the MDM2-p53 axis. Stem Cells 29(12), 1942-1951 (2011)
64. Zhou S, Schuetz JD, Bunting KD et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7(9), 1028-1034 (2001)
65. Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5), 555-567 (2007)
66. Hirschmann-Jax C, Foster AE, Wulf GG et al. A distinct 'side population' of cells with high drug efflux capacity in human tumor cells. Proc. Natl Acad. Sci. USA 101(39), 14228-14233 (2004)
67. Bleau AM, Hambardzumyan D, Ozawa T et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4(3), 226-235 (2009)
68. Schaich M, Kestel L, Pfirrmann M et al. A MDR1 (ABCB1) gene single nucleotide polymorphism predicts outcome of temozolomide treatment in glioblastoma patients. Ann. Oncol. 20(1), 175-181 (2009)
69. Baumann M, Krause M, Hill R. Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer 8(7), 545-554 (2008)
70. Gilbertson RJ, Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat. Rev. Cancer 7(10), 733-736 (2007)
71. Ulasov IV, Nandi S, Dey M, Sonabend AM, Lesniak MS. Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol. Med. 17(1-2), 103-112 (2011)
72. Gupta PB, Onder TT, Jiang G et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138(4), 645-659 (2009)
73. Bao S, Wu Q, Sathornsumetee S et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 66(16), 7843-7848 (2006)
74. Friedman HS, Prados MD, Wen PY et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 27(28), 4733-4740 (2009)
75. Vredenburgh JJ, Desjardins A, Herndon JE 2nd et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J. Clin. Oncol. 25(30), 4722-4729 (2007)
76. Folkins C, Man S, Xu P, Shaked Y, Hicklin DJ, Kerbel RS. Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors. Cancer Res. 67(8), 3560-3564 (2007)
77. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120(3), 694-705 (2010)
78. Folkins C, Shaked Y, Man S et al. Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1. Cancer Res. 69(18), 7243-7251 (2009)
79. Thompson EM, Frenkel EP, Neuwelt EA. The paradoxical effect of bevacizumab in the therapy of malignant gliomas. Neurology 76(1), 87-93 (2011)
80. Verhoeff JJ, van Tellingen O, Claes A et al. Concerns about anti-angiogenic treatment in patients with glioblastoma multiforme. BMC Cancer 9, 444 (2009)
81. Piccirillo SG, Reynolds BA, Zanetti N et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444(7120), 761-765 (2006)
82. Sato A, Sunayama J, Okada M et al. Glioma-initiating cell elimination by metformin activation of FOXO3 via AMPK. Stem Cells Transl. Med. 1(11), 811-824 (2012)
83. Matsuda K, Sato A, Okada M et al. Targeting JNK for therapeutic depletion of stem-like glioblastoma cells. Sci. Rep. 2
84. Di Tomaso T, Mazzoleni S, Wang E et al. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin. Cancer Res. 16(3), 800-813 (2010)
85. Weng D, Song B, Durfee J et al. Induction of cytotoxic T lymphocytes against ovarian cancer-initiating cells. Int. J. Cancer 129(8), 1990-2001(2010)
86. Wang H, Lathia JD, Wu Q et al. Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth. Stem Cells 27(10), 2393-2404 (2009)
87. Brown CE, Starr R, Martinez C et al. Recognition and killing of brain tumor stem-like initiating cells by CD8+ cytolytic T cells. Cancer Res. 69(23), 8886-8893 (2009)
88. Ahmed N, Salsman VS, Kew Y et al. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin. Cancer Res. 16(2), 474-485 (2010)
89. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2), 281-297 (2004)
90. Zhang Y, Dutta A, Abounader R. The role of microRNAs in glioma initiation and progression. Front. Biosci. 17, 700-712 (2012)
91. Gal H, Pandi G, Kanner AA et al. MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem. Biophys. Res. Commun. 376(1), 86-90 (2008)
92. Godlewski J, Nowicki MO, Bronisz A et al. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 68(22), 9125-9130 (2008)
93. Li Y, Guessous F, Zhang Y et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res. 69(19), 7569-7576 (2009)
94. Yu F, Yao H, Zhu P et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 131(6), 1109-1123 (2007)
95. Kambara H, Okano H, Chiocca EA, Saeki Y. An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res. 65(7), 2832-2839 (2005)
96. Kurozumi K, Hardcastle J, Thakur R et al. Oncolytic HSV-1 infection of tumors induces angiogenesis and upregulates CYR61. Mol. Ther. 16(8), 1382-1391 (2008)
97. Ulasov IV, Zhu ZB, Tyler MA et al. Survivin-driven and fiber-modified oncolytic adenovirus exhibits potent antitumor activity in established intracranial glioma. Hum. Gene Ther. 18(7), 589-602 (2007)
98. Nandi S, Ulasov IV, Rolle CE, Han Y, Lesniak MS. A chimeric adenovirus with an Ad 3 fiber knob modification augments glioma virotherapy. J. Gene Med. 11(11), 1005-1011 (2009)
99. Bauerschmitz GJ, Ranki T, Kangasniemi L et al. Tissue-specific promoters active in CD44+CD24-/low breast cancer cells. Cancer Res. 68(14), 5533-5539 (2008)