Cancer stem cells and brain tumors: Uprooting the bad seeds

Expert Review of Anticancer Therapy

Volumn 7, Issue 11, 2007, Pages 1581-1590

  Lee, Da Yong ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glioma; Medulloblastoma; Progenitor cell; Self renewal; Stem cell; Stem cell niche; Tumor microenvironment; Tumor suppressor gene

Indexed keywords

ANTINEOPLASTIC AGENT; APC PROTEIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; CANNABINOID DERIVATIVE; CARBOPLATIN; CD133 ANTIGEN; CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1; EPIDERMAL GROWTH FACTOR; ETOPOSIDE; GAMMA SECRETASE INHIBITOR; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PACLITAXEL; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN P53; PROTEIN TYROSINE KINASE; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1ALPHA; TEMOZOLOMIDE; TRANSCRIPTION FACTOR SOX2; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN;

ANTINEOPLASTIC ACTIVITY; BRAIN TUMOR; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL HETEROGENEITY; CELL ISOLATION; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; GLIOMA; HISTOPATHOLOGY; HUMAN; IN VIVO CULTURE; MEDULLOBLASTOMA; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PROMYELOCYTIC LEUKEMIA; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASTIC STEM CELLS;

EID: 37349039723     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/14737140.7.11.1581     Document Type: Review

References (107)

1. Stewart BW, Kleihues P. World Cancer Report. IARC Press, Lyon, France (2003).
2. De Groot JF, Aldape KD, Colman H. High grade astrocytomas. In: Principles of Neuro-Oncology. Schiff D, O'Neill BP (Eds). McGraw Hill, NY, USA 259-288 (2005).
3. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK. WHO Classification of Tumours of the Central Nervous System (4th Edition). IARC Press, Lyon, France (2007).
4. Rossi ML, Hughes JT, Esiri MM, Coakham HB, Brownell DB. Immunohistological study of mononuclear cell infiltrate in malignant gliomas. Acta Neuropathol. (Berl.) 74(3), 269-277 (1987).
5. Rossi ML, Jones NR, Candy E et al. The mononuclear cell infiltrate compared with survival in high-grade astrocytomas. Acta Neuropathol. (Berl.) 78(2), 189-193 (1989).
6. Graeber MB, Scheithauer BW, Kreutzberg GW. Microglia in brain tumors. Glia 40(2), 252-259 (2002).
7. Watters JJ, Schartner JM, Badie B. Microglia function in brain tumors. J. Neurosci. Res. 81(3), 447-455 (2005).
8. Platten M, Kretz A, Naumann U et al. Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann. Neurol. 54(3), 388-392 (2003).
9. Sliwa M, Markovic D, Gabrusiewicz K et al. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain 130(Pt 2), 476-489 (2007).
10. Daginakatte GC, Gutmann DH. Neurofibromatosis-1 (NF1) heterozygous brain microglia elaborate paracrine factors that promote NF1-deficient astrocyte and glioma growth. Hum. Mol. Genet. 16(9), 1098-1112 (2007).
11. Rubin JB, Kung AL, Klein RS et al. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc. Natl Acad. Sci. USA 100(23), 13513-13518 (2003).
12. Yang L, Jackson E, Woerner BM, Perry A, Piwnica-Worms D, Rubin JB. Blocking CXCR4-mediated cyclic AMP suppression inhibits brain tumor growth in vivo. Cancer Res. 67(2), 651-658 (2007).
13. Warrington NM, Woerner BM, Daginakatte GC et al. Spatiotemporal differences in CXCL12 expression and cyclic AMP underlie the unique pattern of optic glioma growth in neurofibromatosis type 1. Cancer Res. 67(18), 8588-8595 (2007).
14. Listernick R, Charrow J, Greenwald M, Mets M. Natural history of optic pathway tumors in children with neurofibromatosis type 1: a longitudinal study. J. Pediatr. 125(1), 63-66 (1994).
15. Gong X, He X, Qi L, Zuo H, Xie Z. Stromal cell derived factor-1 acutely promotes neural progenitor cell proliferation in vitro by a mechanism involving the ERK1/2 and PI-3K signal pathways. Cell Biol. Int. 30(5), 466-471 (2006).
16. Claps CM, Corcoran KE, Cho KJ, Rameshwar P. Stromal derived growth factor-1 α as a beacon for stem cell homing in development and injury. Curr. Neurovasc. Res. 2(4), 319-329 (2005).
17. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro. Oncol. 7(2), 134-153 (2005).
18. Bao S, Wu Q, Sathomsumetee S et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 66(16), 7843-7848 (2006).
19. Calabrese C, Poppleton H, Kocak M et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11(1), 69-82 (2007).
20. Farin A, Suzuki SO, Weiker M, Goldman JE, Bruce JN, Canoll P. Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 53(8), 799-808 (2006).
21. 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).
22. Ramírez-Castillejo C, Sánchez-Sánchez F, Andreu-Agulló C et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat. Neurosci. 9(3), 331-339 (2006).
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. 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).
25. Li C, Heidt DG, Dalerba P et al. Identification of pancreatic cancer stem cells. Cancer Res. 67(3), 1030-1037 (2007).
26. Prince ME, Sivanandan R, Kaczorowski A et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl Acad. Sci. USA 104(3), 973-9789 (2007).
27. O' Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating turnout growth in immunodeficient mice. Nature 445 (7123), 106-110 (2007).
28. 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).
29. 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).
30. 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).
31. Taylor MD, Poppleton H, Fuller C et al. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8 (4), 323-335 (2005).
32. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 432 (7015), 396-401 (2004).
33. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 414 (6859), 105-111 (2001).
34. 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).
35. Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39 (3), 193-206 (2002).
36. Lee J, Kotliarova S, Kotliarov Y et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9 (5), 391-403 (2006).
37. Dahlstrand J, Zimmerman LB, McKay RD, Lendahl U. Characterization of the human nestin gene reveals a close evolutionary relationship to neurofilaments. J. Cell Sci. 103(Pt 2), 589-597 (1992).
38. Tohyama T, Lee VM, Rorke LB, Marvin M, McKay RD, Trojanowski JQ. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest. 66(3), 303-313 (1992).
39. Zappone MV, Galli R, Catena R et al. Sox2 regulatory sequences direct expression of a (β)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127(11), 2367-2382 (2000).
40. Hegedus B, Dasgupta B, Shin JE et al. Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP-and Ras-dependent mechanisms. Cell Stem Cell (2007) (In Press).
41. Nakano I, Paucar AA, Bajpai R et al. Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J, Cell Biol. 170(3), 413-427 (2005).
42. - glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67(9), 4010-4015 (2007).
43. Yuan X, Curtin J, Xiong Y et al. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene23(58), 9392-9400 (2004).
44. Ligon KL, Huillard E, Mehta S et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 53(4), 503-517 (2007).
45. Sanai N, Tramontin AD, Quiñones-Hinojosa A et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427(6976), 740-744 (2004).
46. Eriksson PS, Perfilieva E, Björk-Eriksson T et al. Neurogenesis in the adult human hippocampus. Nat. Med 4 (11), 1313-1317 (1998).
47. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 41(5), 683-686 (2004).
48. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425(4), 479-494 (2000).
49. Shen Q, Goderie SK, Jin L et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304(5675), 1338-1340 (2004).
50. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277(5329), 1109-1113 (1997).
51. Raffel C, Jenkins RB, Frederick L et al. Sporadic medulloblastomas contain PTCH mutations. Cancer Res. 57(5), 842-845 (1997).
52. Reifenberger J, Wolter M, Weber RG et al. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. CancerRes. 58(9), 1798-1803 (1998).
53. Palma V, Ruiz i Altaba A. Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131(2), 337-345 (2004).
54. Taylor MD, Liu L, Raffel C et al. Mutations in SUFU predispose to medulloblastoma. Nat. Genet. 31(3), 306-310 (2002).
55. Kinzler KW, Bigner SH, Bigner DD et al. Identification of an amplified, highly expressed gene in a human glioma. Science 236(4797), 70-73 (1987).
56. Wallace VA. Purkinje-cell-derived sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9(8), 445-448 (1999).
57. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22(1), 103-114 (1999).
58. Corrales JD, Rocco GL, Blaess S, Guo Q, Joyner AL. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131(22), 5581-5590 (2004).
59. Corrales JD, Blaess S, Mahoney EM, Joyner AL. The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133 (9), 1811-1821 (2006).
60. Dahmane N, Sánchez P, Gitton Y et al. The sonic hedgehog - Gli pathway regulates dorsal brain growth and tumorigenesis. Development 128(24), 5201-5212 (2001).
61. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. Hedgehog-Glil signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr. Biol. 17(2), 165-172 (2007).
62. Huang H, Mahler-Araujo BM, Sankila. A et al. APC mutations in sporadic medulloblastomas. Am. J. Pathol. 156 (2), 433-437 (2000).
63. Zurawel RH, Chiappa SA, Allen C, Raffel C. Sporadic medulloblastomas contain oncogenic β-catenin mutations. Cancer Res. 58(5), 896-899 (1998).
64. Dahmen RP, Koch A, Denkhaus D et al. Deletions of AXIN1, a component of the WNT/wingless pathway, in sporadic medulloblastomas. Cancer Res. 61(19), 7039-7043 (2001).
65. McMahon AP, Bradley A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell62(6), 1073-1085 (1990).
66. Thomas KR, Musci TS, Neumann PE, Capecchi MR. Swaying is a mutant allele of the proto-oncogene Wnt-1. Cell67(5), 969-976 (1991).
67. Lie DC, Colamarino SA, Song HJ et al. Wnt signaling regulates adult hippocampal neurogenesis. Nature 437 (7063), 1370-1375 (2005).
68. Willert K, Brown JD, Danenberg E et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423(6938), 448-452 (2003).
69. Wei Q, Clarke L, Scheidenhelm DK et al. High-grade glioma formation results from postnatal pten loss or mutant epidermal growth factor receptor expression in a transgenic mouse glioma model. Cancer Res. 66(15), 7429-7437 (2006).
70. Holland EC, Hively WP, DePinho RA, Varmus HE. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 12 (23), 3675-3685 (1998).
71. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S et al. PDGFR α-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51(2), 187-199 (2006).
72. Lokker NA, Sullivan CM, Hollenbach SJ, Israel MA, Giese NA. Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res. 62(13), 3729-3735 (2002).
73. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomnas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 15 (15), 1913-1925 (2001).
74. Clarke ID, Dirks PB. A human brain tumor-derived PDGFR-α deletion mutant is transforming. Oncogene 22(5), 722-733 (2003).
75. Dasgupta B, Gutmann DH. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J. Neurosci. 25(23), 5584-5594 (2005).
76. Bajenaru ML, Hernandez MR, Perry A et al. Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res. 63(24), 8573-8577 (2003).
77. Zhu Y, Harada T, Liu L et al. Inactivation of NF1 in CNS causes increased glial progenitor proliferation and optic glioma formation. Development 132(24), 5577-5588 (2005).
78. Groszer M, Erickson R, Scripture-Adams SD et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294(5549), 2186-2189 (2001).
79. Groszer M, Erickson R, Scripture-Adams DD et al. PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc. Natl Acad. Sci. USA 103(1), 111-116 (2006).
80. Xiao A, Yin C, Yang C, Di Cristofano A, Pandolfi PP, Van Dyke T. Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res. 65(12), 5172-5180 (2005).
81. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am, J. Pathol. 170(5), 1445-1453 (2007).
82. Gil-Perotin S, Marin-Husstege M, Li J et al. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J. Neurosci. 26(4), 1107-1116 (2006).
83. Arf senescence pathways. Genes Dev. 19(12), 1432-1437 (2005).
84. Bruggeman SW, Valk-Lingbeek ME, van der Stoop PP et al. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmil-deficient mice. Genes Dev. 19 (12), 1438-1443 (2005).
85. Reilly KM, Loisel DA, Bronson RT, McLaughlin ME, Jacks T. Nf1; Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat. Genet. 26(1), 109-113 (2000).
86. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14(8), 994-1004 (2000).
87. Zhu Y, Guignard F, Zhao D et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8 (2), 119-130 (2005).
88. Kim HT, Kim IS, Lee IS et al. Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed. Exp. Neurol. 199(1), 222-235 (2006).
89. Hitoshi S, Tropepe V, Ekker M, van der Kooy D. Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development 129(1), 233-244 (2002).
90. Fu SL, Ma ZW, Yin L, Iannotti C, Lu PH, Xu XM. Region-specific growth properties and trophic requirements of brain- and spinal cord-derived rat embryonic neural precursor cells. Neuroscience 135(3), 851-862 (2005).
91. Horiguchi S, Takahashi J, Kishi Y et al. Neural precursor cells derived from human embryonic brain retain regional specificity. J. Neurosci. Res. 75(6), 817-824 (2004).
92. Sharma MK, Mansur DB, Reifenberger G et al. Distinct genetic signatures among pilocytic astrocytomas relate to their brain region origin. Cancer Res. 67(3), 890-900 (2007).
93. Gilbertson RJ, Gutmann DH. Tumorigenesis in the brain: location, location, location. Cancer Res. 67(12), 5579-5582 (2007).
94. 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).
95. Hambardzumyan D, Squatrito M, Holland EC. Radiation resistance and stem-like cells in brain tumors. Cancer Cell 10(6), 454-456 (2006).
96. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5(4), 275-284 (2005).
97. + cancer stem cells in glioblastoma. Mol. Cancer 5, 67 (2006).
98. Eramo A, Ricci-Vitiani L, Zeuner A et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 13(7), 1238-1241 (2006).
99. Spira AI, Carducci MA. Differentiation therapy. Curr Opin. Pharmacol. 3(4), 338-343 (2003).
100. Ohno R, Asou N, Ohnishi K. Treatmentof acute promyelocytic leukemia: strategy toward further increase of cure rate. Leukemia 17(8), 1454-1463 (2003).
101. Sell S. Stem cell origin of cancer and differentiation therapy. Crit. Rev. Oncol. Hermatol. 51(1), 1-28 (2004).
102. 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).
103. Aguado T, Carracedo A, Julien B et al. Cannabinoids induce glioma stem-like cell differentiation and inhibit gliomagenesis. J. Biol. Chem. 282(9), 6854-6862 (2007).
104. Cheng T. Cell cycle inhibitors in normal and tumor stem cells. Oncogene 23(43), 7256-7266 (2004).
105. Berman DM, Karhadkar SS, Hallahan AR et al. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 297(5586), 1559-1561 (2002).
106. Bar EE, Chaudhry A, Lin A et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 25(10), 2524-2533 (2007).
107. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat. Rev. Neurosci. 8(8), 610-622 (2007).